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1. Detection of Anaplasma and Ehrlichia bacteria in humans, wildlife, and ticks in the Amazon rainforest

Author

Marie Buysse, Rachid Koual, Florian Binetruy, Benoit de Thoisy, Xavier Baudrimont, Stéphane Garnier, Maylis Douine, Christine Chevillon, Frédéric Delsuc, François Catzeflis, Didier Bouchon, and Olivier Duron

Subjects
Science
Abstract

Abstract Tick-borne bacteria of the genera Ehrlichia and Anaplasma cause several emerging human infectious diseases worldwide. In this study, we conduct an extensive survey for Ehrlichia and Anaplasma infections in the rainforests of the Amazon biome of French Guiana. Through molecular genetics and metagenomics reconstruction, we observe a high indigenous biodiversity of infections circulating among humans, wildlife, and ticks inhabiting these ecosystems. Molecular typing identifies these infections as highly endemic, with a majority of new strains and putative species specific to French Guiana. They are detected in unusual rainforest wild animals, suggesting they have distinctive sylvatic transmission cycles. They also present potential health hazards, as revealed by the detection of Candidatus Anaplasma sparouinense in human red blood cells and that of a new close relative of the human pathogen Ehrlichia ewingii, Candidatus Ehrlichia cajennense, in the tick species that most frequently bite humans in South America. The genome assembly of three new putative species obtained from human, sloth, and tick metagenomes further reveals the presence of major homologs of Ehrlichia and Anaplasma virulence factors. These observations converge to classify health hazards associated with Ehrlichia and Anaplasma infections in the Amazon biome as distinct from those in the Northern Hemisphere.

Published
2024
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2. Reassessment of the genetic basis of natural rifampin resistance in the genus Rickettsia

Author

Julien Amoros, Noor Fattar, Marie Buysse, Meriem Louni, Joanne Bertaux, Didier Bouchon, and Olivier Duron

Subjects
natural antibiotic resistance, Rickettsia, rifampin, RNA polymerase β subunit, rpoB, Microbiology, QR1-502
Abstract

Abstract Rickettsia, a genus of obligate intracellular bacteria, includes species that cause significant human diseases. This study challenges previous claims that the Leucine‐973 residue in the RNA polymerase beta subunit is the primary determinant of rifampin resistance in Rickettsia. We investigated a previously untested Rickettsia species, R. lusitaniae, from the Transitional group and found it susceptible to rifampin, despite possessing the Leu‐973 residue. Interestingly, we observed the conservation of this residue in several rifampin‐susceptible species across most Rickettsia phylogenetic groups. Comparative genomics revealed potential alternative resistance mechanisms, including additional amino acid variants that could hinder rifampin binding and genes that could facilitate rifampin detoxification through efflux pumps. Importantly, the evolutionary history of Rickettsia genomes indicates that the emergence of natural rifampin resistance is phylogenetically constrained within the genus, originating from ancient genetic features shared among a unique set of closely related Rickettsia species. Phylogenetic patterns appear to be the most reliable predictors of natural rifampin resistance, which is confined to a distinct monophyletic subclade known as Massiliae. The distinctive features of the RNA polymerase beta subunit in certain untested Rickettsia species suggest that R. raoultii, R. amblyommatis, R. gravesii, and R. kotlanii may also be naturally rifampin‐resistant species.

Published
2024
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3. Limited association between Wolbachia and Plasmodium falciparum infections in natural populations of the major malaria mosquito Anopheles moucheti

Author

Théo Mouillaud, Audric Berger, Marie Buysse, Nil Rahola, Josquin Daron, Jean‐Pierre Agbor, Sandrine N. Sango, Daniel E. Neafsey, Olivier Duron, and Diego Ayala

Subjects
Anopheles moucheti, malaria control, Plasmodium infection, Wolbachia, Evolution, QH359-425
Abstract

Abstract Since the discovery of natural malaria vector populations infected by the endosymbiont bacterium Wolbachia, a renewed interest has arisen for using this bacterium as an alternative for malaria control. Among naturally infected mosquitoes, Anopheles moucheti, a major malaria mosquito in Central Africa, exhibits one of the highest prevalences of Wolbachia infection. To better understand whether this maternally inherited bacterium could be used for malaria control, we investigated Wolbachia influence in An. moucheti populations naturally infected by the malaria parasite Plasmodium falciparum. To this end, we collected mosquitoes in a village from Cameroon, Central Africa, where this mosquito is the main malaria vector. We found that the prevalence of Wolbachia bacterium was almost fixed in the studied mosquito population, and was higher than previously recorded. We also quantified Wolbachia in whole mosquitoes and dissected abdomens, confirming that the bacterium is also elsewhere than in the abdomen, but at lower density. Finally, we analyzed the association of Wolbachia presence and density on P. falciparum infection. Wolbachia density was slightly higher in mosquitoes infected with the malaria parasite than in uninfected mosquitoes. However, we observed no correlation between the P. falciparum and Wolbachia densities. In conclusion, our study indicates that naturally occurring Wolbachia infection is not associated to P. falciparum development within An. moucheti mosquitoes.

Published
2023
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4. Cross-alteration of murine skin and tick microbiome concomitant with pathogen transmission after Ixodes ricinus bite

Author

Nathalie Boulanger, Jean-Louis-Marie Insonere, Sebastian Van Blerk, Cathy Barthel, Céline Serres, Olivier Rais, Alain Roulet, Florence Servant, Olivier Duron, and Benjamin Lelouvier

Subjects
Microbiota, Metagenome, Lyme disease, Borrelia, Borreliella, Anaplasma, Microbial ecology, QR100-130
Abstract

Abstract Background Ticks are major vectors of diseases affecting humans such as Lyme disease or domestic animals such as anaplasmosis. Cross-alteration of the vertebrate host skin microbiome and the tick microbiome may be essential during the process of tick feeding and for the mechanism of pathogen transmission. However, it has been poorly investigated. Methods We used mice bitten by field-collected ticks (nymphs and adult ticks) in different experimental conditions to investigate, by 16S rRNA gene metabarcoding, the impact of blood feeding on both the mouse skin microbiome and the tick microbiome. We also investigated by PCR and 16S rRNA gene metabarcoding, the diversity of microorganisms transmitted to the host during the process of tick bite at the skin interface and the dissemination of the pathogen in host tissues (blood, heart, and spleen). Results Most of the commensal bacteria present in the skin of control mice were replaced during the blood-feeding process by bacteria originating from the ticks. The microbiome of the ticks was also impacted by the blood feeding. Several pathogens including tick-borne pathogens (Borrelia/Borreliella, Anaplasma, Neoehrlichia, Rickettsia) and opportunistic bacteria (Williamsia) were transmitted to the skin microbiome and some of them disseminated to the blood or spleen of the mice. In the different experiments of this study, skin microbiome alteration and Borrelia/Borreliella transmission were different depending on the tick stages (nymphs or adult female ticks). Conclusions Host skin microbiome at the bite site was deeply impacted by the tick bite, to an extent which suggests a role in the tick feeding, in the pathogen transmission, and a potentially important impact on the skin physiopathology. The diversified taxonomic profiles of the tick microbiome were also modified by the blood feeding. Video Abstract

Published
2023
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5. Emerging infectious diseases and new pandemics: dancing with a ghost! Lessons in inter- and transdisciplinary research in French Guiana, South America

Author

Jean-François Guégan, Loïc Epelboin, Maylis Douine, Paul Le Turnier, Olivier Duron, Lise Musset, Christine Chevillon, Philippe Quénel, Mark Eric Benbow, and Benoît de Thoisy

Subjects
Biomedical research, Public health, Interdisciplinarity, Transdisciplinarity, One Health, Infectious disease, Infectious and parasitic diseases, RC109-216
Abstract

In light of current international public health challenges, calls for inter- and transdisciplinary research are increasing, particularly in response to complex and intersecting issues. Although widely used under the One Health flag, it is still unclear how inter- and transdisciplinary science should be applied to infectious disease research, public health, and the different stakeholders. Here, we present and discuss our common scientific and biomedical experience in French Guiana, South America to conduct and enrich research in vector-borne and zoonotic infectious diseases, with the aim to translate findings to public health and political stakeholders. We highlight the successful progressive dissolution of disciplinary boundaries that go beyond One Health positive-driven assumptions and argue that specific local conditions, as well as strong support from research and medical institutions, have facilitated an emulsion toward inter- and transdisciplinary science. This argument is intended to improve responses to public health concerns in French Guiana and other countries and regions of the world.

Published
2023
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6. Survey of ticks and tick-borne pathogens in wild chimpanzee habitat in Western Uganda

Author

Camille Lacroux, Sarah Bonnet, Emmanuelle Pouydebat, Marie Buysse, Nil Rahola, Sabine Rakotobe, John-Paul Okimat, Rachid Koual, Edward Asalu, Sabrina Krief, and Olivier Duron

Subjects
Amblyomma, Piroplasmids, Borrelia, Cryptoplasma, Ehrlichia, Rickettsia, Infectious and parasitic diseases, RC109-216
Abstract

Abstract Background Ticks and tick-borne pathogens significantly impact both human and animal health and therefore are of major concern to the scientific community. Knowledge of tick-borne pathogens is crucial for prescription of mitigation measures. In Africa, much research on ticks has focused on domestic animals. Little is known about ticks and their pathogens in wild habitats and wild animals like the endangered chimpanzee, our closest relative. Methods In this study, we collected ticks in the forested habitat of a community of 100 chimpanzees living in Kibale National Park, Western Uganda, and assessed how their presence and abundance are influenced by environmental factors. We used non-invasive methods of flagging the vegetation and visual search of ticks both on human team members and in chimpanzee nests. We identified adult and nymph ticks through morphological features. Molecular techniques were used to detect and identify tick-borne piroplasmids and bacterial pathogens. Results A total of 470 ticks were collected, which led to the identification of seven tick species: Haemaphysalis parmata (68.77%), Amblyomma tholloni (20.70%), Ixodes rasus sensu lato (7.37%), Rhipicephalus dux (1.40%), Haemaphysalis punctaleachi (0.70%), Ixodes muniensis (0.70%) and Amblyomma paulopunctatum (0.35%). The presence of ticks, irrespective of species, was influenced by temperature and type of vegetation but not by relative humidity. Molecular detection revealed the presence of at least six genera of tick-borne pathogens (Babesia, Theileria, Borrelia, Cryptoplasma, Ehrlichia and Rickettsia). The Afrotopical tick Amblyomma tholloni found in one chimpanzee nest was infected by Rickettsia sp. Conclusions In conclusion, this study presented ticks and tick-borne pathogens in a Ugandan wildlife habitat whose potential effects on animal health remain to be elucidated. Graphical Abstract

Published
2023
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7. Phylogenetic evidence for a clade of tick-associated trypanosomes

Author

Rachid Koual, Marie Buysse, Justine Grillet, Florian Binetruy, Sofian Ouass, Hein Sprong, Maxime Duhayon, Nathalie Boulanger, Frédéric Jourdain, Aurélien Alafaci, Julien Verdon, Hélène Verheyden, Claude Rispe, Olivier Plantard, and Olivier Duron

Subjects
Trypanosoma pestanai, Trypanosome specificity, Amblyomma, Ixodes, Infectious and parasitic diseases, RC109-216
Abstract

Abstract Background Trypanosomes are protozoan parasites of vertebrates that are of medical and veterinary concern. A variety of blood-feeding invertebrates have been identified as vectors, but the role of ticks in trypanosome transmission remains unclear. Methods In this study, we undertook extensive molecular screening for the presence and genetic diversity of trypanosomes in field ticks. Results Examination of 1089 specimens belonging to 28 tick species from Europe and South America led to the identification of two new trypanosome strains. The prevalence may be as high as 4% in tick species such as the castor bean tick Ixodes ricinus, but we found no evidence of transovarial transmission. Further phylogenetic analyses based on 18S rRNA, EF1-α, hsp60 and hsp85 gene sequences revealed that different tick species, originating from different continents, often harbour phylogenetically related trypanosome strains and species. Most tick-associated trypanosomes cluster in a monophyletic clade, the Trypanosoma pestanai clade, distinct from clades of trypanosomes associated with transmission by other blood-feeding invertebrates. Conclusions These observations suggest that ticks may be specific arthropod hosts for trypanosomes of the T. pestanai clade. Phylogenetic analyses provide further evidence that ticks may transmit these trypanosomes to a diversity of mammal species (including placental and marsupial species) on most continents. Graphical Abstract

Published
2023
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9. Novel Chronic Anaplasmosis in Splenectomized Patient, Amazon Rainforest

Author

Olivier Duron, Rachid Koual, Lise Musset, Marie Buysse, Yann Lambert, Benoît Jaulhac, Denis Blanchet, Kinan Drak Alsibai, Yassamine Lazrek, Loïc Epelboin, Pierre Deshuillers, Céline Michaud, and Maylis Douine

Subjects
anaplasmosis, Amazon rainforest, bacteria, vector-borne infections, zoonoses, French Guiana, Medicine, Infectious and parasitic diseases, RC109-216
Abstract

We report a case of unusual human anaplasmosis in the Amazon rainforest of French Guiana. Molecular typing demonstrated that the pathogen is a novel Anaplasma species, distinct to all known species, and more genetically related to recently described Anaplasma spp. causing infections in rainforest wild fauna of Brazil.

Published
2022
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10. Infection with Borrelia afzelii and manipulation of the egg surface microbiota have no effect on the fitness of immature Ixodes ricinus ticks

Author

Georgia Hurry, Elodie Maluenda, Anouk Sarr, Alessandro Belli, Phineas T. Hamilton, Olivier Duron, Olivier Plantard, and Maarten J. Voordouw

Subjects
Medicine, Science
Abstract

Abstract Arthropod vectors carry vector-borne pathogens that cause infectious disease in vertebrate hosts, and arthropod-associated microbiota, which consists of non-pathogenic microorganisms. Vector-borne pathogens and the microbiota can both influence the fitness of their arthropod vectors, and hence the epidemiology of vector-borne diseases. The bacterium Borrelia afzelii, which causes Lyme borreliosis in Europe, is transmitted among vertebrate reservoir hosts by Ixodes ricinus ticks, which also harbour a diverse microbiota of non-pathogenic bacteria. The purpose of this controlled study was to test whether B. afzelii and the tick-associated microbiota influence the fitness of I. ricinus. Eggs obtained from field-collected adult female ticks were surface sterilized (with bleach and ethanol), which reduced the abundance of the bacterial microbiota in the hatched I. ricinus larvae by 28-fold compared to larvae that hatched from control eggs washed with water. The dysbiosed and control larvae were subsequently fed on B. afzelii-infected or uninfected control mice, and the engorged larvae were left to moult into nymphs under laboratory conditions. I. ricinus larvae that fed on B. afzelii-infected mice had a significantly faster larva-to-nymph moulting time compared to larvae that fed on uninfected control mice, but the effect was small (2.4% reduction) and unlikely to be biologically significant. We found no evidence that B. afzelii infection or reduction of the larval microbiota influenced the four other life history traits of the immature I. ricinus ticks, which included engorged larval weight, unfed nymphal weight, larva-to-nymph moulting success, and immature tick survival. A retrospective power analysis found that our sampling effort had sufficient power (> 80%) to detect small effects (differences of 5% to 10%) of our treatments. Under the environmental conditions of this study, we conclude that B. afzelii and the egg surface microbiota had no meaningful effects on tick fitness and hence on the R0 of Lyme borreliosis.

Published
2021
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12. A dual endosymbiosis supports nutritional adaptation to hematophagy in the invasive tick Hyalomma marginatum

Author

Marie Buysse, Anna Maria Floriano, Yuval Gottlieb, Tiago Nardi, Francesco Comandatore, Emanuela Olivieri, Alessia Giannetto, Ana M Palomar, Benjamin L Makepeace, Chiara Bazzocchi, Alessandra Cafiso, Davide Sassera, and Olivier Duron

Subjects
endosymbiosis, hematophagy, Francisella, Midichloria, Hyalomma, Medicine, Science, Biology (General), QH301-705.5
Abstract

Many animals are dependent on microbial partners that provide essential nutrients lacking from their diet. Ticks, whose diet consists exclusively on vertebrate blood, rely on maternally inherited bacterial symbionts to supply B vitamins. While previously studied tick species consistently harbor a single lineage of those nutritional symbionts, we evidence here that the invasive tick Hyalomma marginatum harbors a unique dual-partner nutritional system between an ancestral symbiont, Francisella, and a more recently acquired symbiont, Midichloria. Using metagenomics, we show that Francisella exhibits extensive genome erosion that endangers the nutritional symbiotic interactions. Its genome includes folate and riboflavin biosynthesis pathways but deprived functional biotin biosynthesis on account of massive pseudogenization. Co-symbiosis compensates this deficiency since the Midichloria genome encompasses an intact biotin operon, which was primarily acquired via lateral gene transfer from unrelated intracellular bacteria commonly infecting arthropods. Thus, in H. marginatum, a mosaic of co-evolved symbionts incorporating gene combinations of distant phylogenetic origins emerged to prevent the collapse of an ancestral nutritional symbiosis. Such dual endosymbiosis was never reported in other blood feeders but was recently documented in agricultural pests feeding on plant sap, suggesting that it may be a key mechanism for advanced adaptation of arthropods to specialized diets.

Published
2021
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13. Natural Wolbachia infections are common in the major malaria vectors in Central Africa

Author

Diego Ayala, Ousman Akone‐Ella, Nil Rahola, Pierre Kengne, Marc F. Ngangue, Fabrice Mezeme, Boris K. Makanga, Martha Nigg, Carlo Costantini, Frédéric Simard, Franck Prugnolle, Benjamin Roche, Olivier Duron, and Christophe Paupy

Subjects
Anopheles, co‐evolution, disease control, diversity, Wolbachia, Evolution, QH359-425
Abstract

Abstract During the last decade, the endosymbiont bacterium Wolbachia has emerged as a biological tool for vector disease control. However, for long time, it was believed that Wolbachia was absent in natural populations of Anopheles. The recent discovery that species within the Anopheles gambiae complex host Wolbachia in natural conditions has opened new opportunities for malaria control research in Africa. Here, we investigated the prevalence and diversity of Wolbachia infection in 25 African Anopheles species in Gabon (Central Africa). Our results revealed the presence of Wolbachia in 16 of these species, including the major malaria vectors in this area. The infection prevalence varied greatly among species, confirming that sample size is a key factor to detect the infection. Moreover, our sequencing and phylogenetic analyses showed the important diversity of Wolbachia strains that infect Anopheles. Co‐evolutionary analysis unveiled patterns of Wolbachia transmission within some Anopheles species, suggesting that past independent acquisition events were followed by co‐cladogenesis. The large diversity of Wolbachia strains that infect natural populations of Anopheles offers a promising opportunity to select suitable phenotypes for suppressing Plasmodium transmission and/or manipulating Anopheles reproduction, which in turn could be used to reduce the malaria burden in Africa.

Published
2019
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14. Surface sterilization methods impact measures of internal microbial diversity in ticks

Author

Florian Binetruy, Marlène Dupraz, Marie Buysse, and Olivier Duron

Subjects
16S rRNA, Bacterial communities, Tick microbiome, Metabarcoding, Amblyomma, Infectious and parasitic diseases, RC109-216
Abstract

Abstract Background Ticks are obligate blood feeders transmitting major pathogens worldwide. Over the past few years, considerable research efforts have focused on the diversity, distribution and impact of gut and intracellular bacterial symbionts on tick development and tick-borne pathogen transmission. The study of this internal microbiome requires the use of a sterilization method to remove external (i.e. cuticular) microbes present on the tick’s surface and to avoid any further contamination. Several sterilization methods exist, including ethanol- or bleach-based treatments that are both effective in killing microbes but with different potential effects on DNA denaturation. Methods We examined how these different sterilization methods impact the measure of internal microbial diversity hosted by the Cayenne tick Amblyomma cajennense (sensu stricto). Bacterial barcoding investigations based on 16S rRNA gene sequences were conducted on two batches of 50 individuals each: Ticks of the first batch were sterilized with bleach diluted at 1% and the second batch with 70% ethanol. Tick external microbiome was also determined from cuticle smearing and water samples used for tick washing. Results Bacterial barcoding investigations showed major differences between ethanol- and bleach-treated specimens. Both methods led to the detection of major intracellular bacteria associated with A. cajennense (s.s.) but ethanol-treated ticks always harbored a higher bacterial diversity than bleach-treated ticks. Further examinations of tick gut and tick external microbiome revealed that ethanol-based surface sterilization method is inefficient to eliminate the DNA of external bacteria. Conclusions We herein provide evidence that studies investigating the internal microbiome of ticks should consider bleach as the gold standard to efficiently remove cuticular bacterial DNA. Indeed, this method does not impact the internal bacterial diversity hosted by ticks and is thus a better method than the ethanol-based one for studying the internal microbiome.

Published
2019
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15. Vector competence of the African argasid tick Ornithodoros moubata for the Q fever agent Coxiella burnetii.

Author

Marie Buysse, Maxime Duhayon, Franck Cantet, Matteo Bonazzi, and Olivier Duron

Subjects
Arctic medicine. Tropical medicine, RC955-962, Public aspects of medicine, RA1-1270
Abstract

Q fever is a widespread zoonotic disease caused by the intracellular bacterium Coxiella burnetii. While transmission is primarily but not exclusively airborne, ticks are usually thought to act as vectors on the basis of early microscopy studies. However, recent observations revealed that endosymbionts of ticks have been commonly misidentified as C. burnetii, calling the importance of tick-borne transmission into question. In this study, we re-evaluated the vector competence of the African soft tick Ornithodoros moubata for an avirulent strain of C. burnetii. To this end, we used an artificial feeding system to initiate infection of ticks, specific molecular tools to monitor further infections, and culture assays in axenic and cell media to check for the viability of C. burnetii excreted by ticks. We observed typical traits associated with vector competence: The exposure to an infected blood meal resulted in viable and persistent infections in ticks, trans-stadial transmissions of infection from nymphs to adults and the ability of adult ticks to transmit infectious C. burnetii. However, in contrast to early studies, we found that infection differed substantially between tick organs. In addition, while adult female ticks were infected, we did not observe C. burnetii in eggs, suggesting that transovarial transmission is not effective. Finally, we detected only a sporadic presence of C. burnetii DNA in tick faeces, but no living bacterium was further isolated in culture assays, suggesting that excretion in faeces is not a common mode of transmission in O. moubata.

Published
2021
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16. Molecular methods routinely used to detect Coxiella burnetii in ticks cross-react with Coxiella-like bacteria

Author

Jourdain Elsa, Olivier Duron, Barry Séverine, Daniel González-Acuña, and Karim Sidi-Boumedine

Subjects
Q fever, tick-borne diseases, tick endosymbiont, false positive, surveillance, PCR primers, Infectious and parasitic diseases, RC109-216
Abstract

Background: Q fever is a widespread zoonotic disease caused by Coxiella burnetii. Ticks may act as vectors, and many epidemiological studies aim to assess C. burnetii prevalence in ticks. Because ticks may also be infected with Coxiella-like bacteria, screening tools that differentiate between C. burnetii and Coxiella-like bacteria are essential. Methods: In this study, we screened tick specimens from 10 species (Ornithodoros rostratus, O. peruvianus, O. capensis, Ixodes ricinus, Rhipicephalus annulatus, R. decoloratus, R. geigy, O. sonrai, O. occidentalis, and Amblyomma cajennense) known to harbor specific Coxiella-like bacteria, by using quantitative PCR primers usually considered to be specific for C. burnetii and targeting, respectively, the IS1111, icd, scvA, p1, and GroEL/htpB genes. Results: We found that some Coxiella-like bacteria, belonging to clades A and C, yield positive PCR results when screened with primers initially believed to be C. burnetii-specific. Conclusions: These results suggest that PCR-based surveys that aim to detect C. burnetii in ticks by using currently available methods must be interpreted with caution if the amplified products cannot be sequenced. Future molecular methods that aim at detecting C. burnetii need to take into account the possibility that cross-reactions may exist with Coxiella-like bacteria.

Published
2015
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17. The Tick Microbiome: Why Non-pathogenic Microorganisms Matter in Tick Biology and Pathogen Transmission

Author

Sarah I. Bonnet, Florian Binetruy, Angelica M. Hernández-Jarguín, and Olivier Duron

Subjects
tick, tick symbionts, tick borne pathogens, microbiome, microbial interactions, Microbiology, QR1-502
Abstract

Ticks are among the most important vectors of pathogens affecting humans and other animals worldwide. They do not only carry pathogens however, as a diverse group of commensal and symbiotic microorganisms are also present in ticks. Unlike pathogens, their biology and their effect on ticks remain largely unexplored, and are in fact often neglected. Nonetheless, they can confer multiple detrimental, neutral, or beneficial effects to their tick hosts, and can play various roles in fitness, nutritional adaptation, development, reproduction, defense against environmental stress, and immunity. Non-pathogenic microorganisms may also play a role in driving transmission of tick-borne pathogens (TBP), with many potential implications for both human and animal health. In addition, the genetic proximity of some pathogens to mutualistic symbionts hosted by ticks is evident when studying phylogenies of several bacterial genera. The best examples are found within members of the Rickettsia, Francisella, and Coxiella genera: while in medical and veterinary research these bacteria are traditionally recognized as highly virulent vertebrate pathogens, it is now clear to evolutionary ecologists that many (if not most) Coxiella, Francisella, and Rickettsia bacteria are actually non-pathogenic microorganisms exhibiting alternative lifestyles as mutualistic ticks symbionts. Consequently, ticks represent a compelling yet challenging system in which to study microbiomes and microbial interactions, and to investigate the composition, functional, and ecological implications of bacterial communities. Ultimately, deciphering the relationships between tick microorganisms as well as tick symbiont interactions will garner invaluable information, which may aid in the future development of arthropod pest and vector-borne pathogen transmission control strategies.

Published
2017
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18. Dynamics of prevalence and diversity of avian malaria infections in wild Culex pipiens mosquitoes: the effects of Wolbachia, filarial nematodes and insecticide resistance

Author

Flore Zélé, Juilen Vézilier, Gregory L’Ambert, Antoine Nicot, Sylvain Gandon, Ana Rivero, and Olivier Duron

Subjects
Culex pipiens, Avian malaria, Plasmodium, Wolbachia, Filarial nematodes, Insecticide resistance, Infectious and parasitic diseases, RC109-216
Abstract

Abstract Background Identifying the parasites transmitted by a particular vector and the factors that render this vector susceptible to the parasite are key steps to understanding disease transmission. Although avian malaria has become a model system for the investigation of the ecological and evolutionary dynamics of Plasmodium parasites, little is still known about the field prevalence, diversity and distribution of avian Plasmodium species within the vectors, or about the extrinsic factors affecting Plasmodium population dynamics in the wild. Methods We examined changes in avian malaria prevalence and Plasmodium lineage composition in female Culex pipiens caught throughout one field season in 2006, across four sampling sites in southern France. Using site occupancy models, we correct the naive estimates of Plasmodium prevalence to account for PCR-based imperfect detection. To establish the importance of different factors that may bear on the prevalence and diversity of avian Plasmodium in field mosquitoes, we focus on Wolbachia and filarial parasite co-infections, as well as on the insecticide resistance status of the mosquito. Results Plasmodium prevalence in Cx. pipiens increased from February (0%) to October (15.8%) and did not vary significantly among the four sampling sites. The application of site occupancy models leads to a 4% increase in this initial (naive) estimate of prevalence. The parasite community was composed of 15 different haemosporidian lineages, 13 of which belonged to the Plasmodium genus, and 2 to the Haemoproteus genus. Neither the presence of different Wolbachia types and of filarial parasites co-infecting the mosquitoes, nor their insecticide resistance status were found to affect the Plasmodium prevalence and diversity. Conclusion We found that haemosporidian parasites are common and diverse in wild-caught Cx. pipiens mosquitoes in Southern France. The prevalence of the infection in mosquitoes is unaffected by Wolbachia and filarial co-infections as well as the insecticide resistant status of the vector. These factors may thus have a negligible impact on the transmission of avian malaria. In contrast, the steady increase in prevalence from February to October indicates that the dynamics of avian malaria is driven by seasonality and supports that infected birds are the reservoir of a diverse community of lineages in southern France.

Published
2014
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19. The Recent Evolution of a Maternally-Inherited Endosymbiont of Ticks Led to the Emergence of the Q Fever Pathogen, Coxiella burnetii.

Author

Olivier Duron, Valérie Noël, Karen D McCoy, Matteo Bonazzi, Karim Sidi-Boumedine, Olivier Morel, Fabrice Vavre, Lionel Zenner, Elsa Jourdain, Patrick Durand, Céline Arnathau, François Renaud, Jean-François Trape, Abel S Biguezoton, Julie Cremaschi, Muriel Dietrich, Elsa Léger, Anaïs Appelgren, Marlène Dupraz, Elena Gómez-Díaz, Georges Diatta, Guiguigbaza-Kossigan Dayo, Hassane Adakal, Sébastien Zoungrana, Laurence Vial, and Christine Chevillon

Subjects
Immunologic diseases. Allergy, RC581-607, Biology (General), QH301-705.5
Abstract

Q fever is a highly infectious disease with a worldwide distribution. Its causative agent, the intracellular bacterium Coxiella burnetii, infects a variety of vertebrate species, including humans. Its evolutionary origin remains almost entirely unknown and uncertainty persists regarding the identity and lifestyle of its ancestors. A few tick species were recently found to harbor maternally-inherited Coxiella-like organisms engaged in symbiotic interactions, but their relationships to the Q fever pathogen remain unclear. Here, we extensively sampled ticks, identifying new and atypical Coxiella strains from 40 of 58 examined species, and used this data to infer the evolutionary processes leading to the emergence of C. burnetii. Phylogenetic analyses of multi-locus typing and whole-genome sequencing data revealed that Coxiella-like organisms represent an ancient and monophyletic group allied to ticks. Remarkably, all known C. burnetii strains originate within this group and are the descendants of a Coxiella-like progenitor hosted by ticks. Using both colony-reared and field-collected gravid females, we further establish the presence of highly efficient maternal transmission of these Coxiella-like organisms in four examined tick species, a pattern coherent with an endosymbiotic lifestyle. Our laboratory culture assays also showed that these Coxiella-like organisms were not amenable to culture in the vertebrate cell environment, suggesting different metabolic requirements compared to C. burnetii. Altogether, this corpus of data demonstrates that C. burnetii recently evolved from an inherited symbiont of ticks which succeeded in infecting vertebrate cells, likely by the acquisition of novel virulence factors.

Published
2015
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20. Distribution of endosymbiotic reproductive manipulators reflects invasion process and not reproductive system polymorphism in the little fire ant Wasmannia auropunctata.

Author

Olivier Rey, Arnaud Estoup, Benoit Facon, Anne Loiseau, Alexandre Aebi, Olivier Duron, Fabrice Vavre, and Julien Foucaud

Subjects
Medicine, Science
Abstract

Endosymbiotic reproductive manipulators may have drastic effects on the ecological and evolutionary dynamics of their hosts. The prevalence of these endosymbionts reflects both their ability to manipulate their hosts and the history of the host populations. The little fire ant Wasmannia auropunctata displays a polymorphism in both its reproductive system (sexual versus clonal populations) and the invasive status of its populations (associated to a habitat shift). We first screened for the presence of a diverse array of reproductive parasites in sexual and clonal populations of W. auropunctata, as a means to investigate the role of endosymbionts in reproductive phenotypes. Wolbachia was the only symbiont found and we then focused on its worldwide distribution and diversity in natural populations of W. auropunctata. Using a multilocus scheme, we further characterized the Wolbachia strains present in these populations. We found that almost all the native sexual populations and only a few clonal populations are infected by Wolbachia. The presence of similar Wolbachia strains in both sexual and clonal populations indicates that they are probably not the cause of the reproductive system polymorphism. The observed pattern seems rather associated to the invasion process of W. auropunctata. In particular, the observed loss of Wolbachia in clonal populations, that recurrently emerged from sexual populations, likely resulted from natural heat treatment and/or relaxed selection during the shift in habitat associated to the invasion process.

Published
2013
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21. Cytoplasmic incompatibility as a means of controlling Culex pipiens quinquefasciatus mosquito in the islands of the south-western Indian Ocean.

Author

Célestine M Atyame, Nicole Pasteur, Emilie Dumas, Pablo Tortosa, Michaël Luciano Tantely, Nicolas Pocquet, Séverine Licciardi, Ambicadutt Bheecarry, Betty Zumbo, Mylène Weill, and Olivier Duron

Subjects
Arctic medicine. Tropical medicine, RC955-962, Public aspects of medicine, RA1-1270
Abstract

The use of the bacterium Wolbachia is an attractive alternative method to control vector populations. In mosquitoes, as in members of the Culex pipiens complex, Wolbachia induces a form of embryonic lethality called cytoplasmic incompatibility, a sperm-egg incompatibility occurring when infected males mate either with uninfected females or with females infected with incompatible Wolbachia strain(s). Here we explore the feasibility of the Incompatible Insect Technique (IIT), a species-specific control approach in which field females are sterilized by inundative releases of incompatible males. We show that the Wolbachia wPip(Is) strain, naturally infecting Cx. p. pipiens mosquitoes from Turkey, is a good candidate to control Cx. p. quinquefasciatus populations on four islands of the south-western Indian Ocean (La Réunion, Mauritius, Grande Glorieuse and Mayotte). The wPip(Is) strain was introduced into the nuclear background of Cx. p. quinquefasciatus mosquitoes from La Réunion, leading to the LR[wPip(Is)] line. Total embryonic lethality was observed in crosses between LR[wPip(Is)] males and all tested field females from the four islands. Interestingly, most crosses involving LR[wPip(Is)] females and field males were also incompatible, which is expected to reduce the impact of any accidental release of LR[wPip(Is)] females. Cage experiments demonstrate that LR[wPip(Is)] males are equally competitive with La Réunion males resulting in demographic crash when LR[wPip(Is)] males were introduced into La Réunion laboratory cages. These results, together with the geographic isolation of the four south-western Indian Ocean islands and their limited land area, support the feasibility of an IIT program using LR[wPip(Is)] males and stimulate the implementation of field tests for a Cx. p. quinquefasciatus control strategy on these islands.

Published
2011
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22. NoWolbachiaprotection againstPlasmodium falciparuminfection in the major malaria mosquitoAnopheles moucheti

Author

Théo Mouillaud, Audric Berger, Marie Buysse, Nil Rahola, Josquin Daron, Jean-Pierre Agbor, Sandrine N. Sango, Daniel E. Neafsey, Olivier Duron, and Diego Ayala

Abstract

Since the discovery of natural malaria vector populations infected by the endosymbiont bacteriumWolbachia, a renewed interest has arisen for using this bacterium as an alternative for malaria control. Among naturally infected mosquitoes,Anopheles moucheti, a major malaria mosquito in Central Africa, exhibits one of the highest prevalences ofWolbachiainfection. To better understand whether this maternally inherited bacterium could be used for malaria control, we investigatedWolbachiainfluence inAn. mouchetipopulations naturally infected by the malaria parasitePlasmodium falciparum. To this end, we collected mosquitoes in a village from Cameroon, Central Africa, where this mosquito is the main malaria vector. We found that the prevalence ofWolbachiabacterium was almost fixed in the studied mosquito population, and was higher than previously recorded. We also quantifiedWolbachiain whole mosquitoes and dissected abdomens, confirming that the bacterium is also elsewhere than in the abdomen, but at lower density. Finally, we analyzed the impact ofWolbachiapresence and density onP. falciparuminfection.Wolbachiadensity was slightly higher in mosquitoes infected with the malaria parasite than in uninfected mosquitoes. However, we observed no correlation between theP. falciparumandWolbachiadensities. In conclusion, our study indicates that naturally occurringWolbachiainfection does not affectP. falciparumdevelopment withinAn. mouchetimosquitoes.

Published
2023

23. Diversity and phylogeny of the tick-borne bacterial genus Candidatus Allocryptoplasma (Anaplasmataceae)

Author

Sofian Ouass, Nathalie Boulanger, Benjamin Lelouvier, Jean-Louis-Marie Insonere, Camille Lacroux, Sabrina Krief, Edward Asalu, Nil Rahola, Olivier Duron, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM), Université de Strasbourg (UNISTRA), Vaiomer, Éco-Anthropologie (EA), and Muséum national d'Histoire naturelle (MNHN)-Centre National de la Recherche Scientifique (CNRS)

Subjects
Anaplasmataceae, Infectious Diseases, Anaplasma, Veterinary (miscellaneous), Insect Science, [SDV]Life Sciences [q-bio], Ehrlichia, Allocryptoplasma, Tick-borne diseases, Animal Science and Zoology, Parasitology, Tick
Abstract

The family Anaplasmataceae includes tick-borne bacteria of major public and veterinary health interest, as best illustrated by members of the genera Anaplasma and Ehrlichia. Recent epidemiological surveys have also reported on the presence of a novel putative genus in the Anaplasmataceae, Candidatus Allocryptoplasma, previously described as Candidatus Cryptoplasma in the western black-legged tick, Ixodes pacificus. However, the genetic diversity of Ca. Allocryptoplasma and its phylogenetic relationship with other Anaplasmataceae remain unclear. In this study, we developed a multi-locus sequence typing approach, examining the DNA sequence variation at five genes of Ca. Allocryptoplasma found in ticks. Combining this multi-locus sequence typing and genetic data available on public databases, we found that substantial genetic diversity of Ca. Allocryptoplasma is present in Ixodes, Amblyomma and Haemaphysalis spp. ticks on most continents. Further analyses confirmed that the Ca. Allocryptoplasma of ticks, the Ca. Allocryptoplasma of lizards and some Anaplasma-like bacteria of wild mice cluster into a monophyletic genus, divergent from all other genera of the family Anaplasmataceae. Candidatus Allocryptoplasma appears as a sister genus of Anaplasma and, with the genera Ehrlichia and Neoehrlichia, they form a monophyletic subgroup of Anaplasmataceae associated with tick-borne diseases. The detection of genetically distinct Ca. Allocryptoplasma in ticks of significant medical or veterinary interest supports the hypothesis that it is an emergent genus of tick-borne pathogens of general concern.

Published
2023

24. Genomic Changes During the Evolution of theCoxiellaGenus Along the Parasitism-Mutualism Continuum

Author

Diego Santos-Garcia, Olivier Morel, Hélène Henri, Adil El Filali, Marie Buysse, Valérie Noël, Karen D. McCoy, Yuval Gottlieb, Lisa Klasson, Lionel Zenner, Olivier Duron, and Fabrice Vavre

Abstract

The Coxiellaceae family is composed of five genera showing lifestyles ranging from free-living to symbiosis. Among them,Coxiella burnetiiis a well-known pathogen causing Q fever in humans. This bacterium presents both intracellular (parasitic) and environmental (resistant) forms. Recently, several environmentalCoxiellagenomes have been reported, among which several have come from intracellular mutualistic symbionts of ticks, termedCoxiella-like endosymbionts. We sequenced two newCoxiella-LE genomes fromDermacentor marginatus(CLEDm) andOrnithodoros maritimus(CLEOmar) ticks, the latter belonging to theC. burnetiilineage. Using these newly sequencedCoxiella-LEs and 43 Coxiellaceae genomes, we conducted comparative genomic and phylogenomic analyses to increase our knowledge ofC. burnetiipathogenicity and the emergence ofCoxiella-LEs. Results highlight the probably parasitic nature of the common ancestor of the Coxiellaceae. Indeed, the virulence factor Dot/Icm T4 Secretion System is present in most, but not all, Coxiellaceae. Whereas it is part of a putative pathogenic island inC. burnetii, it has been entirely lost or inactivated inCoxiella-LEs, suggesting its importance in pathogenesis. Additionally, we found that a Sha/Mrp antiporter was laterally acquired in theC. burnetiilineage. This antiporter might be involved in alkali resistance and the development of the resistant form that is able to persist in the environment for long periods of time. The Sha operon is eroded or absent inCoxiella-LEs. Finally, we found that allCoxiellarepresentatives produce B vitamins and co-factors indicating a pre-adaptation ofCoxiellato mutualism with hematophagous arthropods. Accordingly, the ancestor ofC. burnetiiandCoxiella-LEs was likely a parasitic bacterium able to manipulate its host cell and to produce vitamins and co-factors for its own use.

Published
2022

25. Multiple Wolbachia subpopulations co-occur in single Culex pipiens mosquitoes

Author

Hans Schrieke, Olivier Duron, A Eren, and Julie Reveillaud

Abstract

Background Wolbachia is a maternally inherited intracellular bacterium that infects a wide range of arthropods including mosquitoes. The endosymbiont is widely used in biocontrol strategies due to its capacity to modulate the arthropod reproduction and to limit pathogen transmission. Results While most studies assume that Wolbachia infections are mono-clonal within individual hosts, we show here that an ancestral Wolbachia can evolve to a set of closely related, but genetically distinct, subpopulations which coexist within the same hosts and are maternally transmitted to host progeny. To this aim, we reconstructed Wolbachia Metagenome-Assembled Genomes in naturally-infected single individual Culex pipiens mosquitoes from both ovary and midgut metagenomes for the first time and afforded Wolbachia population genomic analyses within and between single individuals. We observed consistent single nucleotide and amnio acid variations across samples that we also confirmed in egg metagenomes from geographical distant locations. Conclusion This study reveals the presence of multiple Wolbachia subpopulations co-existing in individual mosquitoes that could have critical importance for the good use of Wolbachia in basic and applied research.

Published
2022

27. Ecological Contacts and Host Specificity Promote Replacement of Nutritional Endosymbionts in Ticks

Author

Florian Binetruy, Raz Leibson, Olivier Duron, Yuval Gottlieb, and Marie Buysse

Subjects
Ecology, Phylogenetic tree, Ecology (disciplines), Soil Science, Biology, Tick, bacterial infections and mycoses, biology.organism_classification, Host Specificity, Ecological network, Ticks, Microbial ecology, Symbiosis, Horizontal gene transfer, Animals, bacteria, Francisella, Phylogeny, Ecology, Evolution, Behavior and Systematics, Coevolution
Abstract

Symbiosis with vitamin-provisioning microbes is essential for the nutrition of animals with specialized feeding habits. While coevolution stabilizes the interactions between symbiotic partners, their associations are not necessarily permanent: Recently acquired symbionts can replace ancestral symbionts. In this study, we demonstrate successful replacement dynamics of Francisella-Like Endosymbionts (-LE), a group of invasive B-vitamin-provisioning endosymbionts, across tick communities driven by a complex web of horizontal transfers. Using a broad collection of Francisella-LE-infected tick species, we determined the diversity of Francisella-LE haplotypes through a multi-locus strain typing approach, and further characterized their phylogenetic relationships and their association with biological traits of their tick hosts. The patterns observed showed that Francisella-LE commonly transfer through similar ecological networks and geographic distributions shared among different tick species, and, in certain cases, through preferential shuffling across congeneric tick species. Altogether, these findings reveal the importance of both routes in shaping the invasive pattern in which new nutritional symbioses are initiated.

Published
2021

28. The origin and evolution of mitochondrial tropism inMidichloriabacteria

Author

Anna Maria Floriano, Gherard Batisti Biffignandi, Michele Castelli, Emanuela Olivieri, Emanuela Clementi, Francesco Comandatore, Laura Rinaldi, Maxwell Opara, Olivier Plantard, Ana M. Palomar, Valérie Noël, Amrita Vijay, Nathan Lo, Benjamin L. Makepeace, Olivier Duron, Aaron Jex, Lionel Guy, and Davide Sassera

Abstract

Midichloriaare intracellular bacterial symbionts of ticks. Some representatives of this genus have the unique capability to colonize mitochondria in the cells of their hosts. Hypotheses on the nature of this interaction have proven difficult to test, partly due to a lack of data. Indeed, until now, mitochondrial tropism information and genomes were available only for symbionts of three and two tick host species, respectively. Here we analyzed the mitochondrial tropism of three additionalMidichloriaand sequenced nine novel genomes, showing that the tropism is pnon-monophyletic, either due to losses of the trait or multiple parallel acquisitions. Comparative genome analyses support the first hypothesis, as the genomes of non-mitochondrial symbionts appear to be reduced subsets of those capable of colonizing the organelles. We detect genomic signatures of mitochondrial tropism, showing a set of candidate genes characteristic of the strains capable of mitochondrial colonization. These include the type IV secretion system and the flagellum, which could allow the secretion of unique effectors, direct interaction with, or invasion of the mitochondria. Other genes, including putative adhesion molecules, proteins possibly involved in actin polymerization, cell wall and outer membrane proteins, are only present in mitochondrial symbionts. The bacteria could use these to manipulate host structures, including mitochondrial membranes, in order to fuse with the organelles or manipulate the mitochondrial network.

Published
2022

29. Habitat fragmentation differentially shapes neutral and immune gene variation in a tropical bird species

Author

Anthony Ollivier, Aurélie Khimoun, Olivier Duron, Franck Theron, Nyls de Pracontal, Bruno Faivre, Gilles Leblond, Maxime Loubon, Antoine Perrin, Stéphane Garnier, Biogéosciences [UMR 6282] [Dijon] (BGS), Université de Bourgogne (UB)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Centre National de la Recherche Scientifique (CNRS), Groupe d’Etude et de Protection des Oiseaux en Guyane (GEPOG), SARL BIOS, Evolution of host-microbe communities (MIVEGEC-EVCO), Processus Écologiques et Évolutifs au sein des Communautés (PEEC), Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Institut de Recherche pour le Développement (IRD [France-Sud])-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Institut de Recherche pour le Développement (IRD [France-Sud])-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Institut de Recherche pour le Développement (IRD [France-Sud])-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Institut de Recherche pour le Développement (IRD [France-Sud])-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), and Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])

Subjects
0106 biological sciences, 0301 basic medicine, Population, Biodiversity, Context (language use), Biology, 010603 evolutionary biology, 01 natural sciences, Article, Birds, 03 medical and health sciences, Genetic drift, Genetic variation, Genetics, Animals, education, Ecosystem, Genetics (clinical), Selection (genetic algorithm), education.field_of_study, Genetic diversity, Habitat fragmentation, 15. Life on land, 030104 developmental biology, Evolutionary biology, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, human activities
Abstract

International audience; Habitat fragmentation is a major cause of biodiversity loss, responsible for an alteration of intraspecific patterns of neutral genetic diversity and structure. Although neutral genetic variation can be informative for demographic inferences, it may be a poor predictor of adaptive genetic diversity and thus of the consequences of habitat fragmentation on selective evolutionary processes. In this context, we contrasted patterns of genetic diversity and structure of neutral loci (microsatellites) and immune genes (i.e., toll-like receptors) in an understorey bird species, the wedge-billed woodcreeper Glyphorynchus spirurus. The objectives were (1) to investigate forest fragmentation effects on population genetic diversity, (2) to disentangle the relative role of demography (genetic drift and migration) and selection, and (3) to assess whether immunogenetic patterns could be associated with variation of ectoparasite (i.e., ticks) pressures. Our results revealed an erosion of neutral genetic diversity and a substantial genetic differentiation among fragmented populations, resulting from a decrease in landscape connectivity and leading to the divergence of distinct genetic pools at a small spatial scale. Patterns of genetic diversity observed for TLR4 and TLR5 were concordant with neutral genetic patterns, whereas those observed for TLR3 and TLR21 were discordant. This result underlines that the dominant evolutionary force shaping immunogenetic diversity (genetic drift vs. selection) may be different depending on loci considered. Finally, tick prevalence was higher in fragmented environments. We discussed the hypothesis that pathogen selective pressures may contribute to maintain adaptive genetic diversity despite the negative demographic effect of habitat fragmentation on neutral genetic diversity.

Published
2020

30. Microbial community structure reveals instability of nutritional symbiosis during the evolutionary radiation of Amblyomma ticks

Author

Nil Rahola, Florian Binetruy, Roxanne Barosi, Manon Villa, Olivier Duron, Marie Buysse, Diego Ayala, Christophe Paupy, Quentin Lejarre, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Centre International de Recherches Médicales de Franceville (CIRMF), Diversity, ecology, evolution & Adaptation of arthropod vectors (MIVEGEC-DEEVA), Evolution des Systèmes Vectoriels (ESV), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Evolution of host-microbe communities (MIVEGEC-EVCO), and Processus Écologiques et Évolutifs au sein des Communautés (PEEC)

Subjects
0106 biological sciences, 0301 basic medicine, maternally inherited bacteria, Zoology, Tick, 010603 evolutionary biology, 01 natural sciences, ticks, 03 medical and health sciences, Coxiella, Amblyomma, Symbiosis, Phylogenetics, parasitic diseases, Genetics, Animals, Francisella, Rickettsia, Phylogeny, Ecology, Evolution, Behavior and Systematics, Coevolution, Bacteria, biology, Obligate, Microbiota, bacterial infections and mycoses, biology.organism_classification, Biological Evolution, [SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology, symbiosis, [SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology, endosymbiont replacement, B vitamins, 030104 developmental biology, coevolution, bacteria, microbial community, Adaptation, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Abstract

International audience; Mutualistic interactions with microbes have facilitated the adaptation of major eukaryotic lineages to restricted diet niches. Hence, ticks with their strictly blood‐feeding lifestyle are associated with intracellular bacterial symbionts through an essential B vitamin supplementation. In this study, examination of bacterial diversity in 25 tick species of the genus Amblyomma showed that three intracellular bacteria, Coxiella‐like endosymbionts (LE), Francisella‐LE and Rickettsia, are remarkably common. No other bacterium is as uniformly present in Amblyomma ticks. Almost all Amblyomma species were found to harbour a nutritive obligate symbiont, Coxiella‐LE or Francisella‐LE, that is able to synthesize B vitamins. However, despite the co‐evolved and obligate nature of these mutualistic interactions, the structure of microbiomes does not mirror the Amblyomma phylogeny, with a clear exclusion pattern between Coxiella‐LE and Francisella‐LE across tick species. Coxiella‐LE, but not Francisella‐LE, form evolutionarily stable associations with ticks, commonly leading to co‐cladogenesis. We further found evidence for symbiont replacements during the radiation of Amblyomma, with recent, and probably ongoing, invasions by Francisella‐LE and subsequent replacements of ancestral Coxiella‐LE through transient co‐infections. Nutritional symbiosis in Amblyomma ticks is thus not a stable evolutionary state, but instead arises from conflicting origins between unrelated but competing symbionts with similar metabolic capabilities.

Published
2020

31. Novel Rickettsia genotypes in ticks in French Guiana, South America

Author

Florian Binetruy, Marie Buysse, Roxanne Barosi, Olivier Duron, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Evolution of host-microbe communities (MIVEGEC-EVCO), Processus Écologiques et Évolutifs au sein des Communautés (PEEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), and Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])

Subjects
0301 basic medicine, Rainforest, animal structures, Transovarial transmission, Genotype, 030231 tropical medicine, Zoology, lcsh:Medicine, Tick, Article, 03 medical and health sciences, 0302 clinical medicine, Ticks, Phylogenetics, parasitic diseases, medicine, Animals, Humans, Typing, Rickettsia, lcsh:Science, Phylogeny, Infectious-disease epidemiology, Multidisciplinary, biology, Phylogenetic tree, lcsh:R, Rickettsia Infections, biology.organism_classification, medicine.disease, bacterial infections and mycoses, 3. Good health, Spotted fever, French Guiana, 030104 developmental biology, Rickettsiosis, [SDE]Environmental Sciences, bacteria, lcsh:Q, Bacterial infection
Abstract

Rickettsia are obligate intracellular bacteria often associated with ticks and best known for causing human diseases (rickettsiosis), including typhus fever and sporadic cases of serious infection. In this study, we conducted a large survey of ticks in French Guiana to understand the overall diversity of Rickettsia in this remote area largely covered by dense rainforests. Out of 819 individuals (22 tick species in six genera), 252 (30.8%) samples were positive for Rickettsia infection. Multilocus typing and phylogenetic analysis identified 19 Rickettsia genotypes, but none was 100% identical to already known Rickettsia species or strains. Among these 19 genotypes, we identified two validated Rickettsia species, Rickettsia amblyommatis (spotted fever group) and Rickettsia bellii (bellii group), and characterized a novel and divergent Rickettsia phylogenetic group, the guiana group. While some tick hosts of these Rickettsia genotypes are among the most common ticks to bite humans in French Guiana, their potential pathogenicity remains entirely unknown. However, we found a strong association between Rickettsia genotypes and their host tick species, suggesting that most of these Rickettsia genotypes may be nonpathogenic forms maintained through transovarial transmission.

Published
2020

32. MIxS-SA: a MIxS extension defining the minimum information standard for sequence data from symbiont-associated micro-organisms

Author

Fátima Jorge, Jaelle C. Brealey, Paul J. Brindley, Marie Buysse, Cinzia Cantacessi, Olivier Duron, Raina Fichorova, Connor R. Fitzpatrick, Megan Hahn, Christopher Hunter, Vincent Hervé, Laura J. Knoll, Kevin D. Kohl, Marco Lalle, Julius Lukeš, Joaquín Martínez Martínez, Susan L. Perkins, Robert Poulin, Karyna Rosario, Adam C. Schneider, Lynn M. Schriml, Luke R. Thompson, Ramona L. Walls, Nolwenn M. Dheilly, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM), Centre de Recherche en Ecologie et Evolution de la Santé (CREES), Institut de Recherche pour le Développement (IRD)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), Institut de recherche sur la biologie de l'insecte UMR7261 (IRBI), Université de Tours (UT)-Centre National de la Recherche Scientifique (CNRS), Unité de virologie, Agence nationale de sécurité sanitaire de l'alimentation, de l'environnement et du travail (ANSES), Laboratoire de Ploufragan-Plouzané-Niort [ANSES], University of Otago [Dunedin, Nouvelle-Zélande], NTNU University Museum [Trondheim], Norwegian University of Science and Technology [Trondheim] (NTNU), Norwegian University of Science and Technology (NTNU)-Norwegian University of Science and Technology (NTNU), The George Washington University (GW), Department of Veterinary Medicine, University of Cambridge [UK] (CAM), Harvard Medical School [Boston] (HMS), University of North Carolina [Chapel Hill] (UNC), University of North Carolina System (UNC), NYC Department of Health and Mental Hygiene (NYC Health), University of Wisconsin-Madison, University of Pittsburgh (PITT), Pennsylvania Commonwealth System of Higher Education (PCSHE), Istituto Superiore di Sanità (ISS), Institute of Parasitology [České Budějovice] (BIOLOGY CENTRE CAS), Biology Centre of the Czech Academy of Sciences (BIOLOGY CENTRE CAS), Czech Academy of Sciences [Prague] (CAS)-Czech Academy of Sciences [Prague] (CAS), Bigelow Laboratory for Ocean Sciences, The City College of New York (CCNY), City University of New York [New York] (CUNY), University of South Florida [Tampa] (USF), Hendrix College, University of Maryland School of Medicine, University of Maryland System, Mississippi State University [Mississippi], National Oceanic and Atmospheric Administration (NOAA), Critical Path Institute [Tucson, AZ], Virologie UMR1161 (VIRO), École nationale vétérinaire - Alfort (ENVA)-Agence nationale de sécurité sanitaire de l'alimentation, de l'environnement et du travail (ANSES)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Cantacessi, Cinzia [0000-0001-6863-2950], and Apollo - University of Cambridge Repository

Subjects
3107 Microbiology, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, FOS: Biological sciences, Human Genome, Genetics, General Medicine, Infection, 31 Biological Sciences, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Abstract

The symbiont-associated (SA) environmental package is a new extension to the minimum information about any (x) sequence (MIxS) standards, established by the Parasite Microbiome Project (PMP) consortium, in collaboration with the Genomics Standard Consortium. The SA was built upon the host-associated MIxS standard, but reflects the nestedness of symbiont-associated microbiota within and across host-symbiont-microbe interactions. This package is designed to facilitate the collection and reporting of a broad range of metadata information that apply to symbionts such as life history traits, association with one or multiple host organisms, or the nature of host-symbiont interactions along the mutualism-parasitism continuum. To better reflect the inherent nestedness of all biological systems, we present a novel feature that allows users to co-localize samples, to nest a package within another package, and to identify replicates. Adoption of the MIxS-SA and of the new terms will facilitate reports of complex sampling design from a myriad of environments.

Published
2022

33. A dual endosymbiosis supports nutritional adaptation to hematophagy in the invasive tick Hyalomma marginatum

Author

Anna Maria Floriano, Marie Buysse, Yuval Gottlieb, Tiago Nardi, Francesco Comandatore, Emanuela Olivieri, Alessia Giannetto, Ana M Palomar, Benjamin L Makepeace, Chiara Bazzocchi, Alessandra Cafiso, Davide Sassera, Olivier Duron, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Centre de Recherche en Ecologie et Evolution de la Santé (CREES), and Institut de Recherche pour le Développement (IRD)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)

Subjects
endosymbiosis, General Immunology and Microbiology, hematophagy, QH301-705.5, General Neuroscience, Midichloria, Science, Francisella, Hyalomma, Other, General Medicine, General Biochemistry, Genetics and Molecular Biology, [SDE]Environmental Sciences, Medicine, Biology (General)
Abstract

Many animals are dependent on microbial partners that provide essential nutrients lacking from their diet. Ticks, whose diet consists exclusively on vertebrate blood, rely on maternally inherited bacterial symbionts to supply B vitamins. While previously studied tick species consistently harbor a single lineage of those nutritional symbionts, we evidence here that the invasive tick Hyalomma marginatum harbors a unique dual-partner nutritional system between an ancestral symbiont, Francisella, and a more recently acquired symbiont, Midichloria. Using metagenomics, we show that Francisella exhibits extensive genome erosion that endangers the nutritional symbiotic interactions. Its genome includes folate and riboflavin biosynthesis pathways but deprived functional biotin biosynthesis on account of massive pseudogenization. Co-symbiosis compensates this deficiency since the Midichloria genome encompasses an intact biotin operon, which was primarily acquired via lateral gene transfer from unrelated intracellular bacteria commonly infecting arthropods. Thus, in H. marginatum, a mosaic of co-evolved symbionts incorporating gene combinations of distant phylogenetic origins emerged to prevent the collapse of an ancestral nutritional symbiosis. Such dual endosymbiosis was never reported in other blood feeders but was recently documented in agricultural pests feeding on plant sap, suggesting that it may be a key mechanism for advanced adaptation of arthropods to specialized diets.

Published
2021

35. Infection with Borrelia afzelii and manipulation of the egg surface microbiota have no effect on the fitness of immature Ixodes ricinus ticks

Author

Maarten J. Voordouw, Elodie Maluenda, Alessandro Belli, Olivier Duron, Georgia Hurry, Anouk Sarr, Phineas T. Hamilton, Olivier Plantard, University of Saskatchewan [Saskatoon] (U of S), Institute of Biology of the University of Neuchâtel, Université de Neuchâtel (UNINE), Deeley Research Centre, BC Cancer Agency (BCCRC), Centre de Recherche en Ecologie et Evolution de la Santé (CREES), Institut de Recherche pour le Développement (IRD)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Biologie, Epidémiologie et analyse de risque en Santé Animale (BIOEPAR), Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), This work was supported by a Swiss National Science Foundation grant (FN 31003A_141153) and a Discovery Grant from the Natural Sciences and Engineering Research Council (NSERC) of Canada (RGPIN-2019-04483) awarded to Maarten J. Voordouw and an NSERC undergraduate summer research award (USRA) to Georgia Hurry. Phineas T. Hamilton is supported by a Canadian Institutes of Health Research (CIHR) post-doctoral fellowship., and École nationale vétérinaire, agroalimentaire et de l'alimentation Nantes-Atlantique (ONIRIS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)

Subjects
0301 basic medicine, Ixodes ricinus, Science, [SDV]Life Sciences [q-bio], 030231 tropical medicine, Zoology, Tick, Borrelia afzelii, medicine.disease_cause, Article, Microbial ecology, 03 medical and health sciences, 0302 clinical medicine, parasitic diseases, medicine, Nymph, Symbiosis, Larva, Infectious-disease epidemiology, Multidisciplinary, biology, Ricinus, fungi, biology.organism_classification, bacterial infections and mycoses, 3. Good health, 030104 developmental biology, Medicine, Pathogens, Moulting, Entomology, Arthropod Vector
Abstract

Arthropod vectors carry vector-borne pathogens that cause infectious disease in vertebrate hosts, and arthropod-associated microbiota, which consists of non-pathogenic microorganisms. Vector-borne pathogens and the microbiota can both influence the fitness of their arthropod vectors, and hence the epidemiology of vector-borne diseases. The bacterium Borrelia afzelii, which causes Lyme borreliosis in Europe, is transmitted among vertebrate reservoir hosts by Ixodes ricinus ticks, which also harbour a diverse microbiota of non-pathogenic bacteria. The purpose of this controlled study was to test whether B. afzelii and the tick-associated microbiota influence the fitness of I. ricinus. Eggs obtained from field-collected adult female ticks were surface sterilized (with bleach and ethanol), which reduced the abundance of the bacterial microbiota in the hatched I. ricinus larvae by 28-fold compared to larvae that hatched from control eggs washed with water. The dysbiosed and control larvae were subsequently fed on B. afzelii-infected or uninfected control mice, and the engorged larvae were left to moult into nymphs under laboratory conditions. I. ricinus larvae that fed on B. afzelii-infected mice had a significantly faster larva-to-nymph moulting time compared to larvae that fed on uninfected control mice, but the effect was small (2.4% reduction) and unlikely to be biologically significant. We found no evidence that B. afzelii infection or reduction of the larval microbiota influenced the four other life history traits of the immature I. ricinus ticks, which included engorged larval weight, unfed nymphal weight, larva-to-nymph moulting success, and immature tick survival. A retrospective power analysis found that our sampling effort had sufficient power (> 80%) to detect small effects (differences of 5% to 10%) of our treatments. Under the environmental conditions of this study, we conclude that B. afzelii and the egg surface microbiota had no meaningful effects on tick fitness and hence on the R0 of Lyme borreliosis.

Published
2021

36. A dual endosymbiosis drives nutritional adaptation to hematophagy in the invasive tick Hyalomma marginatum

Author

Chiara Bazzocchi, Alessia Giannetto, Ben Makepeace, Anna Maria Floriano, Ana Maria Palomar Urbina, Yuval Gottlieb, Marie Buysse, Alessandra Cafiso, Emanuela Olivieri, Olivier Duron, Tiago Nardi, Francesco Comandatore, and Davide Sassera

Subjects
Genetics, B vitamins, biology, Endosymbiosis, Hematophagy, Hyalomma marginatum, Midichloria, Francisella, Tick, biology.organism_classification, Genome
Abstract

Many animals are dependent on microbial partners that provide essential nutrients lacking from their diet. Ticks, whose diet consists exclusively on vertebrate blood, rely on maternally inherited bacterial symbionts to supply B vitamins. While previously studied tick species consistently harbor a single lineage of those nutritional symbionts, we evidence here that the invasive tick Hyalomma marginatum harbors a unique dual-partner nutritional system between an ancestral symbiont, Francisella, and a more recently acquired symbiont, Midichloria. Using metagenomics, we show that Francisella exhibits extensive genome erosion that endangers the nutritional symbiotic interactions: Its genome includes folate and riboflavin biosynthesis pathways but deprived functional biotin biosynthesis on account of massive pseudogenization. Co-symbiosis compensates this deficiency since the Midichloria genome encompasses an intact biotin operon, which was primarily acquired via lateral gene transfer from unrelated intracellular bacteria commonly infecting arthropods. Thus, in H. marginatum, a mosaic of co-evolved symbionts incorporating gene combinations of distant phylogenetic origins emerged to prevent the collapse of an ancestral nutritional symbiosis. Such dual endosymbiosis was never reported in other blood feeders but was recently documented in agricultural pests feeding on plant sap, suggesting that it may be a key mechanism for advanced adaptation of arthropods to specialized diets.

Published
2021

37. Ecology, evolution, and epidemiology of zoonotic and vector-borne infectious diseases in French Guiana: Transdisciplinarity does matter to tackle new emerging threats

Author

Anne Lavergne, Marine Ginouves, Florian Binetruy, Claude Flamand, Mathieu Nacher, Emmanuel Roux, Roxane Schaub, Sébastien Gourbière, Benoit de Thoisy, Pierre Couppié, Arthur Kocher, Lise Musset, Philippe Quénel, Sourakhata Tirera, Luisiane Carvalho, Jérôme Murienne, Sébastien Briolant, Magalie Demar, Yanouk Epelboin, Ghislaine Prévot, Olivier Duron, Isabelle Dusfour, Benjamin Roche, Maylis Douine, Stéphane Pelleau, Luana Mathieu, Agathe Chavy, Loïc Epelboin, Alain Franc, Paul Le Turnier, Pauline Thill, Jean-François Guégan, Emeline Houël, Dominique Rousset, Stanislas Talaga, Laboratoire des Interactions Virus-Hôtes [Cayenne, Guyane Française], Institut Pasteur de la Guyane, Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP), Réseau International des Instituts Pasteur (RIIP), Centre de Recherche en Ecologie et Evolution de la Santé (CREES), Institut de Recherche pour le Développement (IRD)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Centre Hospitalier Andrée Rosemon [Cayenne, Guyane Française], Centre National de Référence du Paludisme [Cayenne, Guyane française] (CNR - laboratoire associé), Centre Collaborateur OMS pour la surveillance de la résistance aux antipaludiques [Cayenne, Guyane française] (CCOMS), Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)-Organisation Mondiale de la Santé / World Health Organization Office (OMS / WHO), Laboratoire de Parasitologie [Cayenne, Guyane française], Institut de recherche en santé, environnement et travail (Irset), Université d'Angers (UA)-Université de Rennes (UR)-École des Hautes Études en Santé Publique [EHESP] (EHESP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique ), École des Hautes Études en Santé Publique [EHESP] (EHESP), Centre de Recherches Ecologiques et Evolutives sur le Cancer (MIVEGEC-CREEC), Processus Écologiques et Évolutifs au sein des Communautés (PEEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Vecteurs - Infections tropicales et méditerranéennes (VITROME), Institut de Recherche pour le Développement (IRD)-Aix Marseille Université (AMU)-Institut de Recherche Biomédicale des Armées [Brétigny-sur-Orge] (IRBA), Institut de Recherche Biomédicale des Armées [Antenne Marseille] (IRBA), Santé publique France Guyane, Santé publique France - French National Public Health Agency [Saint-Maurice, France], Université de Guyane (UG), Centre d’Infection et d’Immunité de Lille - INSERM U 1019 - UMR 9017 - UMR 8204 (CIIL), Institut Pasteur de Lille, Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Lille-Centre Hospitalier Régional Universitaire [Lille] (CHRU Lille)-Centre National de la Recherche Scientifique (CNRS), Centre d'investigation clinique Antilles-Guyane (CIC - Antilles Guyane), Institut National de la Santé et de la Recherche Médicale (INSERM)-CHU Pointe-à-Pitre/Abymes [Guadeloupe] -CHU de la Martinique [Fort de France]-Centre Hospitalier Andrée Rosemon [Cayenne, Guyane Française], Département de Santé Globale - Department Global Health, Institut Pasteur [Paris] (IP)-Université Paris Cité (UPCité), Laboratoire Génome et développement des plantes (LGDP), Université de Perpignan Via Domitia (UPVD)-Centre National de la Recherche Scientifique (CNRS), Vectopôle Amazonien Emile Abonnenc [Cayenne, Guyane française], Unité d'Epidémiologie [Cayenne, Guyane française], Modélisation mathématique des maladies infectieuses - Mathematical modelling of Infectious Diseases, Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité), Biodiversité, Gènes & Communautés (BioGeCo), Université de Bordeaux (UB)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), from patterns to models in computational biodiversity and biotechnology (PLEIADE), Laboratoire Bordelais de Recherche en Informatique (LaBRI), Université de Bordeaux (UB)-École Nationale Supérieure d'Électronique, Informatique et Radiocommunications de Bordeaux (ENSEIRB)-Centre National de la Recherche Scientifique (CNRS)-Université de Bordeaux (UB)-École Nationale Supérieure d'Électronique, Informatique et Radiocommunications de Bordeaux (ENSEIRB)-Centre National de la Recherche Scientifique (CNRS)-Inria Bordeaux - Sud-Ouest, Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)-Biodiversité, Gènes & Communautés (BioGeCo), Université de Bordeaux (UB)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Biome Tropical et Immuno-Pathophysiologie = Tropical Biome and ImmunoPhysiopathology [Lille] (TBIP), Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Lille-Centre Hospitalier Régional Universitaire [Lille] (CHRU Lille)-Centre National de la Recherche Scientifique (CNRS)-Institut Pasteur de Lille, Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Lille-Centre Hospitalier Régional Universitaire [Lille] (CHRU Lille)-Centre National de la Recherche Scientifique (CNRS)-Université de Guyane (UG), Ecologie des forêts de Guyane (UMR ECOFOG), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-AgroParisTech-Université de Guyane (UG)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Max Planck Institute for the Science of Human History (MPI-SHH), Max-Planck-Gesellschaft, Evolution et Diversité Biologique (EDB), Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS), Centre d’Investigation Clinique de Nantes (CIC Nantes), Université de Nantes (UN)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre hospitalier universitaire de Nantes (CHU Nantes), Centre hospitalier universitaire de Nantes (CHU Nantes), Malaria : parasites et hôtes - Malaria : parasites and hosts, Institut Pasteur [Paris] (IP), UMR 228 Espace-Dev, Espace pour le développement, Institut de Recherche pour le Développement (IRD)-Université de Perpignan Via Domitia (UPVD)-Avignon Université (AU)-Université de La Réunion (UR)-Université de Montpellier (UM)-Université de Guyane (UG)-Université des Antilles (UA), LMI Sentinela [Rio de Janeiro], Institut de Recherche pour le Développement (IRD)-Universidade de Brasilia [Brasília] (UnB)-Fundação Oswaldo Cruz / Oswaldo Cruz Foundation (FIOCRUZ), Service Universitaire des Maladies Infectieuses et du Voyageur [Tourcoing], Centre Hospitalier Tourcoing, Centre Hospitalier Gustave Dron [Tourcoing], Animal, Santé, Territoires, Risques et Ecosystèmes (UMR ASTRE), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), This work has benefited from three 'Investissement d’Avenir' grants managed by Agence Nationale de la Recherche (CEBA: ANR-10-LABX-25-01, TULIP: ANR-10-LABX-0041, DRIIHM: ANR-11-LABX-0010). The two lead coauthors received European funding through the European Regional Development Fund Operational Program FEDER RESERVOIRS Project (BdT) and a US NSF-NIH (NSF#1911457) Ecology of infectious diseases award (J-FG). J-FG is also supported by IRD, INRAE, and Université of Montpellier. OD thanks l’Office français de la biodiversité, le Groupe d'Étude et de Protection des Oiseaux en Guyane (GEPOG), la Direction de l'Alimentation, de l'Agriculture et de la Forêt de Guyane (DAAF). AL acknowledges European funding through the European Regional Development Fund Operational Program FEDER RESERVOIRS, CAROLLIA, EFAG and VIRUSES projects. LM is supported by European funding through the European Regional Development Fund Operational Program FEDER ELIMALAR project and Santé publique France as the National Reference Center for Malaria. PQ thanks Publique France/Cire Guyane, CNR sur les arboviroses, CNR du paludisme. EH and ID acknowledge European funding through the European Regional Development Fund Operational Program FEDER CONTROLE Projet, the French Guiana Regional Council and the Air Liquide Foundation. SB is supported by the French Army (Grant LR607e). ER is grateful for European funding through the European Regional Development Fund Operational Program FEDER OSE-Guyamapa project, the French Embassy in Brazil, the Guyamazon program ('GAPAM-Sentinela' project), CNES, and the Bill and Melinda Gates Foundation., ANR-10-LABX-0025,CEBA,CEnter of the study of Biodiversity in Amazonia(2010), ANR-10-LABX-0041,TULIP,Towards a Unified theory of biotic Interactions: the roLe of environmental(2010), ANR-11-LABX-0010,DRIIHM / IRDHEI,Dispositif de recherche interdisciplinaire sur les Interactions Hommes-Milieux(2011), Génétique et évolution des maladies infectieuses (GEMI), Centre National de Référence du Paludisme [Cayenne, Guyane française] (CNR), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Génétique et évolution des maladies infectieuses (GEMI), Institut de Recherche pour le Développement (IRD)-Aix Marseille Université (AMU)-Institut de Recherche Biomédicale des Armées (IRBA), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS), Institut de Recherche pour le Développement (IRD)-Universidade de Brasilia [Brasília] (UnB)-Fundação Oswaldo Cruz (FIOCRUZ), Dusfour, Isabelle, Laboratoires d'excellence - CEnter of the study of Biodiversity in Amazonia - - CEBA2010 - ANR-10-LABX-0025 - LABX - VALID, Towards a Unified theory of biotic Interactions: the roLe of environmental - - TULIP2010 - ANR-10-LABX-0041 - LABX - VALID, Dispositif de recherche interdisciplinaire sur les Interactions Hommes-Milieux - - DRIIHM / IRDHEI2011 - ANR-11-LABX-0010 - LABX - VALID, Université d'Angers (UA)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-École des Hautes Études en Santé Publique [EHESP] (EHESP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique ), Centre National de la Recherche Scientifique (CNRS)-Centre Hospitalier Régional Universitaire [Lille] (CHRU Lille)-Université de Lille-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut Pasteur de Lille, Institut National de la Santé et de la Recherche Médicale (INSERM)-CHU de la Martinique [Fort de France]-CHU Pointe-à-Pitre/Abymes [Guadeloupe] -Centre Hospitalier Andrée Rosemon [Cayenne, Guyane Française], Institut Pasteur [Paris], Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)-Centre National de la Recherche Scientifique (CNRS)-Centre Hospitalier Régional Universitaire [Lille] (CHRU Lille)-Université de Lille-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut Pasteur de Lille, Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)-Université de Guyane (UG), Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, Université de Guyane (UG)-Université des Antilles (UA)-Institut de Recherche pour le Développement (IRD)-Université de Perpignan Via Domitia (UPVD)-Avignon Université (AU)-Université de La Réunion (UR)-Université de Montpellier (UM), Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique )-Institut National de la Santé et de la Recherche Médicale (INSERM)-École des Hautes Études en Santé Publique [EHESP] (EHESP)-Université de Rennes 1 (UR1), and Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Université d'Angers (UA)

Subjects
0301 basic medicine, Microbiology (medical), Emerging and reemerging infectious diseases, Ecology (disciplines), media_common.quotation_subject, [SDV]Life Sciences [q-bio], [SDE.MCG]Environmental Sciences/Global Changes, 030106 microbiology, Immigration, Interdisciplinary Research, Wildlife, Vector Borne Diseases, Animals, Wild, Anthropogenic pressures, Biology, Microbiology, 03 medical and health sciences, [SDV.MHEP.MI]Life Sciences [q-bio]/Human health and pathology/Infectious diseases, Zoonoses, Genetics, Prevalence, Animals, Humans, Human Activities, Molecular Biology, Epidemiologic transition, Global change, Ecology, Evolution, Behavior and Systematics, Ecosystem, media_common, Demography, [SDV.MHEP.ME] Life Sciences [q-bio]/Human health and pathology/Emerging diseases, [SDV.MHEP.ME]Life Sciences [q-bio]/Human health and pathology/Emerging diseases, Resistance (ecology), Ecology, Incidence, Outbreak, 15. Life on land, French Guiana, [SDV] Life Sciences [q-bio], Epidemiological transition, [SDE.MCG] Environmental Sciences/Global Changes, 030104 developmental biology, Infectious Diseases, Promiscuity, Vector (epidemiology), [SDV.MHEP.MI] Life Sciences [q-bio]/Human health and pathology/Infectious diseases
Abstract

International audience; French Guiana is a European ultraperipheric region located on the northern Atlantic coast of South America. It constitutes an important forested region for biological conservation in the Neotropics. Although very sparsely populated, with its inhabitants mainly concentrated on the Atlantic coastal strip and along the two main rivers, it is marked by the presence and development of old and new epidemic disease outbreaks, both research and health priorities. In this review paper, we synthetize 15 years of multidisciplinary and integrative research at the interface between wildlife, ecosystem modification, human activities and sociodemographic development, and human health. This study reveals a complex epidemiological landscape marked by important transitional changes, facilitated by increased interconnections between wildlife, land-use change and human occupation and activity, human and trade transportation, demography with substantial immigration, and identified vector and parasite pharmacological resistance. Among other French Guianese characteristics, we demonstrate herein the existence of more complex multi-host disease life cycles than previously described for several disease systems in Central and South America, which clearly indicates that today the greater promiscuity between wildlife and humans due to demographic and economic pressures may offer novel settings for microbes and their hosts to circulate and spread. French Guiana is a microcosm that crystallizes all the current global environmental, demographic and socioeconomic change conditions, which may favor the development of ancient and future infectious diseases.

Published
2021

38. Publisher Correction: Infection with Borrelia afzelii and manipulation of the egg surface microbiota have no effect on the fitness of immature Ixodes ricinus ticks

Author

Maarten J. Voordouw, Georgia Hurry, Anouk Sarr, Phineas T. Hamilton, Elodie Maluenda, Alessandro Belli, Olivier Duron, and Olivier Plantard

Subjects
Ixodes ricinus, Science, Zoology, Biology, Borrelia afzelii, medicine.disease_cause, Mice, Borrelia burgdorferi Group, medicine, Prevalence, Animals, Disease Reservoirs, Life Cycle Stages, Lyme Disease, Multidisciplinary, Tick Bites, Ixodes, biology.organism_classification, Publisher Correction, Antibodies, Bacterial, Insect Vectors, Disease Models, Animal, Physical Fitness, Immunoglobulin G, Larva, Host-Pathogen Interactions, Medicine
Abstract

Arthropod vectors carry vector-borne pathogens that cause infectious disease in vertebrate hosts, and arthropod-associated microbiota, which consists of non-pathogenic microorganisms. Vector-borne pathogens and the microbiota can both influence the fitness of their arthropod vectors, and hence the epidemiology of vector-borne diseases. The bacterium Borrelia afzelii, which causes Lyme borreliosis in Europe, is transmitted among vertebrate reservoir hosts by Ixodes ricinus ticks, which also harbour a diverse microbiota of non-pathogenic bacteria. The purpose of this controlled study was to test whether B. afzelii and the tick-associated microbiota influence the fitness of I. ricinus. Eggs obtained from field-collected adult female ticks were surface sterilized (with bleach and ethanol), which reduced the abundance of the bacterial microbiota in the hatched I. ricinus larvae by 28-fold compared to larvae that hatched from control eggs washed with water. The dysbiosed and control larvae were subsequently fed on B. afzelii-infected or uninfected control mice, and the engorged larvae were left to moult into nymphs under laboratory conditions. I. ricinus larvae that fed on B. afzelii-infected mice had a significantly faster larva-to-nymph moulting time compared to larvae that fed on uninfected control mice, but the effect was small (2.4% reduction) and unlikely to be biologically significant. We found no evidence that B. afzelii infection or reduction of the larval microbiota influenced the four other life history traits of the immature I. ricinus ticks, which included engorged larval weight, unfed nymphal weight, larva-to-nymph moulting success, and immature tick survival. A retrospective power analysis found that our sampling effort had sufficient power ( 80%) to detect small effects (differences of 5% to 10%) of our treatments. Under the environmental conditions of this study, we conclude that B. afzelii and the egg surface microbiota had no meaningful effects on tick fitness and hence on the R

Published
2021

39. Borrelia afzelii Infection in the Rodent Host Has Dramatic Effects on the Bacterial Microbiome of Ixodes ricinus Ticks

Author

Georgia Hurry, Anouk Sarr, Elodie Maluenda, Alessandro Belli, Olivier Duron, Phineas T. Hamilton, Olivier Plantard, Maarten J. Voordouw, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Centre de Recherche en Ecologie et Evolution de la Santé (CREES), Institut de Recherche pour le Développement (IRD)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), Deeley Research Centre, BC Cancer Agency (BCCRC), Institute of Biology of the University of Neuchâtel, Université de Neuchâtel (UNINE), University of Saskatchewan [Saskatoon] (U of S), Biologie, Epidémiologie et analyse de risque en Santé Animale (BIOEPAR), and Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)

Subjects
Nymph, Ixodes ricinus, Sodium Hypochlorite, Tick, Borrelia afzelii, medicine.disease_cause, Applied Microbiology and Biotechnology, Microbiology, 03 medical and health sciences, Lyme disease, stomatognathic system, Borrelia burgdorferi Group, parasitic diseases, medicine, Invertebrate Microbiology, Animals, Microbiome, 030304 developmental biology, Ovum, 0303 health sciences, Tick-borne disease, Lyme Disease, Mice, Inbred BALB C, Ecology, biology, Ethanol, Ixodes, 030306 microbiology, Microbiota, Ricinus, fungi, Sterilization, biology.organism_classification, medicine.disease, bacterial infections and mycoses, 3. Good health, Larva, [SDE]Environmental Sciences, Female, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, Food Science, Biotechnology
Abstract

The microbiome of blood-sucking arthropods can shape their competence to acquire and maintain infections with vector-borne pathogens. We used a controlled study to investigate the interactions between Borrelia afzelii, which causes Lyme borreliosis in Europe, and the bacterial microbiome of Ixodes ricinus, its primary tick vector. We applied a surface sterilization treatment to I. ricinus eggs to produce dysbiosed tick larvae that had a low bacterial abundance and a changed bacterial microbiome compared to those of the control larvae. Dysbiosed and control larvae fed on B. afzelii-infected mice and uninfected control mice, and the engorged larvae were left to molt into nymphs. The nymphs were tested for B. afzelii infection, and their bacterial microbiome underwent 16S rRNA amplicon sequencing. Surprisingly, larval dysbiosis had no effect on the vector competence of I. ricinus for B. afzelii, as the nymphal infection prevalence and the nymphal spirochete load were the same between the dysbiosed group and the control group. The strong effect of egg surface sterilization on the tick bacterial microbiome largely disappeared once the larvae molted into nymphs. The most important determinant of the bacterial microbiome of I. ricinus nymphs was the B. afzelii infection status of the mouse on which the nymphs had fed as larvae. Nymphs that had taken their larval blood meal from an infected mouse had a less abundant but more diverse bacterial microbiome than the control nymphs. Our study demonstrates that vector-borne infections in the vertebrate host shape the microbiome of the arthropod vector. IMPORTANCE Many blood-sucking arthropods transmit pathogens that cause infectious disease. For example, Ixodes ricinus ticks transmit the bacterium Borrelia afzelii, which causes Lyme disease in humans. Ticks also have a microbiome, which can influence their ability to acquire and transmit tick-borne pathogens such as B. afzelii. We sterilized I. ricinus eggs with bleach, and the tick larvae that hatched from these eggs had a dramatically reduced and changed bacterial microbiome compared to that of control larvae. These larvae fed on B. afzelii-infected mice, and the resultant nymphs were tested for B. afzelii and for their bacterial microbiome. We found that our manipulation of the bacterial microbiome had no effect on the ability of the tick larvae to acquire and maintain populations of B. afzelii. In contrast, we found that B. afzelii infection had dramatic effects on the bacterial microbiome of I. ricinus nymphs. Our study demonstrates that infections in the vertebrate host can shape the tick microbiome.

Published
2021

40. Tissue localization of Coxiella-like endosymbionts in three European tick species through fluorescence in situ hybridization

Author

Claudine Menard, Marie Buysse, Olivier Plantard, Olivier Duron, Karen D. McCoy, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Institut de Recherche pour le Développement (IRD [France-Sud])-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), UMR 1300 Biologie, Epidémiologie et Analyse du Risque, Institut National de la Recherche Agronomique (INRA)-Ecole Nationale Vétérinaire, Agroalimentaire et de l'alimentation Nantes-Atlantique (ONIRIS)-Biologie, Epidémiologie et Analyse du Risque (BioEpAR)-Santé animale (S.A.), Institut des Biomolécules Max Mousseron [Pôle Chimie Balard] (IBMM), Ecole Nationale Supérieure de Chimie de Montpellier (ENSCM)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), Evolution of host-microbe communities (MIVEGEC-EVCO), Processus Écologiques et Évolutifs au sein des Communautés (PEEC), Institut de Recherche pour le Développement (IRD [France-Sud])-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Institut de Recherche pour le Développement (IRD [France-Sud])-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Institut de Recherche pour le Développement (IRD [France-Sud])-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Institut de Recherche pour le Développement (IRD [France-Sud])-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Biologie, Epidémiologie et analyse de risque en Santé Animale (BIOEPAR), Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Ecole Nationale Supérieure de Chimie de Montpellier (ENSCM)-Institut de Chimie du CNRS (INC)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), and Institut National de la Recherche Agronomique (INRA)-École nationale vétérinaire, agroalimentaire et de l'alimentation Nantes-Atlantique (ONIRIS)

Subjects
DNA, Bacterial, 0301 basic medicine, Malpighian tubule system, Ixodidae, Transovarial transmission, Ixodes hexagonus, 030231 tropical medicine, In situ hybridization, Tick, Microbiology, Salivary Glands, 03 medical and health sciences, Ticks, Coxiella, 0302 clinical medicine, parasitic diseases, medicine, Animals, Symbiosis, In Situ Hybridization, Fluorescence, Phylogeny, ComputingMilieux_MISCELLANEOUS, Dermacentor, biology, medicine.diagnostic_test, Ovary, Malpighian tubules, bacterial infections and mycoses, biology.organism_classification, 3. Good health, Europe, B vitamins, 030104 developmental biology, Infectious Diseases, Tissue tropism, Insect Science, bacteria, Female, Parasitology, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, Fluorescence in situ hybridization
Abstract

International audience; Ticks are commonly infected by Coxiella-like endosymbionts (Coxiella-LE) which are thought to supply missing B vitamin nutrients required for blood digestion.While this nutritional symbiosis is essential for the survival and reproduction of infected tick species, our knowledge of where Coxiella-LE is localized in tick tissues is partial at best since previous studies have focused on a limited number of Asian or American tick species. To fill this gap, we investigated the tissue localization of Coxiella-LE in three European tick species, Ornithodoros maritimus, Dermacentor marginatus and Ixodes hexagonus, using a diagnostic fluorescence in situ hybridization (FISH) assay, combined with PCR-based detection. Specific fluorescent foci were observed in several tick tissues. We visualized a pronounced tissue tropism of Coxiella-LE for tick ovaries and Malpighian tubules, a pattern suggestive of a high degree of lifestyle specialization toward mutualism: infection of the ovaries is indicative of transovarial transmission, whereas infection of the Malpighian tubules suggests a nutritional function. We postulate that Malpighian tubules are key organs for the nutritional symbiosis, notably the synthesis of B vitamins by Coxiella-LE, whereas the infection of the ovaries ensures vertical transmission of the symbionts to future generations. We also detected occasional infections in other organs, such as salivary glands and the midgut. Finally, we discuss the potential significance of the different tissue tropism for tick biology.

Published
2019

41. Surface sterilization methods impact measures of internal microbial diversity in ticks

Author

Marlène Dupraz, Florian Binetruy, Olivier Duron, Marie Buysse, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Evolution of host-microbe communities (MIVEGEC-EVCO), Processus Écologiques et Évolutifs au sein des Communautés (PEEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), and Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])

Subjects
0301 basic medicine, Sodium Hypochlorite, Amblyomma cajennense, Ticks, 0302 clinical medicine, Amblyomma, RNA, Ribosomal, 16S, biology, Gastrointestinal Microbiome, Biodiversity, Tick microbiome, Éthanol, Bacterial communities, 3. Good health, Infectious Diseases, Vecteur de maladie, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, [SDE]Environmental Sciences, Female, L72 - Organismes nuisibles des animaux, 030231 tropical medicine, Zoology, [SDV.BID]Life Sciences [q-bio]/Biodiversity, Tick, Agent pathogène, Specimen Handling, lcsh:Infectious and parasitic diseases, 03 medical and health sciences, parasitic diseases, Animals, DNA Barcoding, Taxonomic, lcsh:RC109-216, Microbiome, 16S rRNA, Symbiosis, Maladie transmissible par tiques, Bacteria, Ethanol, Obligate, Research, Évaluation de l'impact, Stérilisation, biology.organism_classification, bacterial infections and mycoses, 030104 developmental biology, Parasitology, Metabarcoding, Disinfectants
Abstract

Background Ticks are obligate blood feeders transmitting major pathogens worldwide. Over the past few years, considerable research efforts have focused on the diversity, distribution and impact of gut and intracellular bacterial symbionts on tick development and tick-borne pathogen transmission. The study of this internal microbiome requires the use of a sterilization method to remove external (i.e. cuticular) microbes present on the tick’s surface and to avoid any further contamination. Several sterilization methods exist, including ethanol- or bleach-based treatments that are both effective in killing microbes but with different potential effects on DNA denaturation. Methods We examined how these different sterilization methods impact the measure of internal microbial diversity hosted by the Cayenne tick Amblyomma cajennense (sensu stricto). Bacterial barcoding investigations based on 16S rRNA gene sequences were conducted on two batches of 50 individuals each: Ticks of the first batch were sterilized with bleach diluted at 1% and the second batch with 70% ethanol. Tick external microbiome was also determined from cuticle smearing and water samples used for tick washing. Results Bacterial barcoding investigations showed major differences between ethanol- and bleach-treated specimens. Both methods led to the detection of major intracellular bacteria associated with A. cajennense (s.s.) but ethanol-treated ticks always harbored a higher bacterial diversity than bleach-treated ticks. Further examinations of tick gut and tick external microbiome revealed that ethanol-based surface sterilization method is inefficient to eliminate the DNA of external bacteria. Conclusions We herein provide evidence that studies investigating the internal microbiome of ticks should consider bleach as the gold standard to efficiently remove cuticular bacterial DNA. Indeed, this method does not impact the internal bacterial diversity hosted by ticks and is thus a better method than the ethanol-based one for studying the internal microbiome. Electronic supplementary material The online version of this article (10.1186/s13071-019-3517-5) contains supplementary material, which is available to authorized users.

Published
2019

42. Phylogenetics of the Spiroplasma ixodetis endosymbiont reveals past transfers between ticks and other arthropods

Author

Oliver Martin, Christine Chevillon, Xavier Bailly, Olivier Duron, Marco V. Bernasconi, Florian Binetruy, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Unité Mixte de Recherche d'Épidémiologie des maladies Animales et zoonotiques (UMR EPIA), Institut National de la Recherche Agronomique (INRA)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS), Evolution of host-microbe communities (MIVEGEC-EVCO), Processus Écologiques et Évolutifs au sein des Communautés (PEEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Institute for Integrative Biology [Zürich] (IBZ), Eidgenössische Technische Hochschule - Swiss Federal Institute of Technology [Zürich] (ETH Zürich), Dipartimento di Scienza dei Materiali, Università degli Studi di Milano-Bicocca = University of Milano-Bicocca (UNIMIB), CNRS IRD, Università degli Studi di Milano-Bicocca [Milano] (UNIMIB), Institut de Recherche pour le Développement (IRD [France-Sud])-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), Unité de recherche d'Épidémiologie Animale (UEA), Institut National de la Recherche Agronomique (INRA), and Università di Milano-Bicocca

Subjects
Male, 0301 basic medicine, Non-Mendelian inheritance, Spiroplasma, [SDV]Life Sciences [q-bio], media_common.quotation_subject, 030231 tropical medicine, Horizontal transfer, Zoology, Insect, Tick, Microbiology, 03 medical and health sciences, Ticks, 0302 clinical medicine, Phylogenetics, parasitic diseases, Disease Transmission, Infectious, Animals, Symbiosis, Arthropods, Phylogeny, ComputingMilieux_MISCELLANEOUS, media_common, Endosymbiosis, biology, Phylogenetic tree, Spiroplasma ixodetis, [SDV.BA]Life Sciences [q-bio]/Animal biology, Genetic Variation, bacterial infections and mycoses, biology.organism_classification, Infectious Disease Transmission, Vertical, Bacterial Typing Techniques, 030104 developmental biology, Infectious Diseases, Insect Science, Horizontal gene transfer, Female, Parasitology, Maternally Inherited bacteria, Arthropod, Gram-Negative Bacterial Infections, Multilocus Sequence Typing
Abstract

International audience; The bacterium Spiroplasma ixodetis is a maternally inherited endosymbiont primarily described from ticks but also found widespread across other arthropods. While it has been identified as a male-killing agent in some insect species, the consequences of infection with S. ixodetis in ticks are entirely unknown, and it is unclear how this endosymbiont spreads across tick species. Here, we have investigated this aspect through the examination of the diversity and evolutionary history of S. ixodetis infections in 12 tick species and 12 other arthropod species. Using a multi-locus typing approach, we identified that ticks harbor a substantial diversity of divergent S. ixodetis strains. Phylogenetic investigations revealed that these S. ixodetis strains do not cluster within a tick-specific subclade but rather exhibit distinct evolutionary origins. In their past, these strains have undergone repeated horizontal transfers between ticks and other arthropods, including aphids and flies. This diversity pattern strongly suggests that maternal inheritance and horizontal transfers are key drivers of S. ixodetis spread, dictating global incidence of infections across tick communities. We do not, however, detect evidence of S. ixodetis-based male-killing since we observed that infections were widely present in both males and females across populations of the African blue tick Rhipicephalus decoloratus.

Published
2019

43. The Importance of Revisiting Legionellales Diversity

Author

Fabrice Vavre, Patricia Doublet, Didier Bouchon, Olivier Duron, Evolution of host-microbe communities (MIVEGEC-EVCO), Processus Écologiques et Évolutifs au sein des Communautés (PEEC), Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Institut de Recherche pour le Développement (IRD [France-Sud]), Pathogenèse des légionelles- Legionella pathogenesis (LegioPath), Centre International de Recherche en Infectiologie - UMR (CIRI), École normale supérieure - Lyon (ENS Lyon)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Lyon (ENS Lyon)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Génétique et évolution des interactions hôtes-parasites, Département génétique, interactions et évolution des génomes [LBBE] (GINSENG), Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Equipe de recherche européenne en algorithmique et biologie formelle et expérimentale (ERABLE), Inria Grenoble - Rhône-Alpes, Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria), Ecologie et biologie des interactions (EBI), Université de Poitiers-Centre National de la Recherche Scientifique (CNRS), Centre International de Recherche en Infectiologie (CIRI), École normale supérieure de Lyon (ENS de Lyon)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Université Jean Monnet - Saint-Étienne (UJM)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure de Lyon (ENS de Lyon)-Université Claude Bernard Lyon 1 (UCBL), and Université de Lyon-Université de Lyon-Université Jean Monnet - Saint-Étienne (UJM)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)

Subjects
0301 basic medicine, Q fever, Human pathogen, Disease, Biology, Legionella pneumophila, Host Specificity, 03 medical and health sciences, Species Specificity, medicine, Animals, Humans, Mutualism (biology), [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE], Intracellular parasite, Bacterial Infections, Biodiversity, biology.organism_classification, medicine.disease, Coxiella burnetii, 030104 developmental biology, Infectious Diseases, Legionellales, Evolutionary biology, Parasitology, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, Gammaproteobacteria, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Abstract

Bacteria of the order Legionellales, such as Legionella pneumophila, the agent of Legionnaires' disease, and Coxiella burnetii, the agent of Q fever, are widely recognized as human pathogens. While our view of the Legionellales is often limited to clinical isolates, ecological surveys are continually uncovering new members of the Legionellales that do not fall into the recognized pathogenic species. Here we emphasize that most of these Legionellales are nonpathogenic forms that have evolved symbiotic lifestyles with nonvertebrate hosts. The diversity of nonpathogenic forms remains, however, largely underexplored. We conjecture that its characterization, once contrasted with the data on pathogenic species, will reveal novel highlights on the mechanisms underlying lifestyle transitions of intracellular bacteria, including the emergence of pathogenesis and mutualism, transmission routes, and host specificity.

Published
2018

44. Borrelia infection in rodent host has dramatic effects on the microbiome of ticks

Author

Phineas T. Hamilton, Anouk Sarr, Maarten J. Voordouw, Georgia Hurry, Olivier Plantard, Alessandro Belli, Elodie Maluenda, and Olivier Duron

Subjects
Ixodes ricinus, biology, Zoology, Tick, bacterial infections and mycoses, biology.organism_classification, Borrelia afzelii, medicine.disease_cause, medicine.disease, Human morbidity, Lyme disease, Vector (epidemiology), Borrelia, parasitic diseases, medicine, Microbiome
Abstract

BackgroundVector-borne diseases remain major causes of human morbidity and mortality. It is increasingly recognized that the community of microbes inhabiting arthropods can strongly affect their vector competence, but the role of the tick microbiome in Borrelia transmission – the cause of Lyme disease – remains unclear.ResultsHere, we use a large-scale experiment to clarify the reciprocal interactions between Borrelia afzelii and the microbiome of Ixodes ricinus, its primary vector. In contrast to other reports, we find that depletion of the bacterial microbiome in larval ticks has no effect on their subsequent acquisition of B. afzelii during blood feeding on infected mice. Rather, exposure to B. afzelii-infected hosts drives pervasive changes to the tick microbiome, decreasing overall bacterial abundance, shifting bacterial community composition, and increasing bacterial diversity. These effects appear to be independent of the acquisition of B. afzelii by ticks, suggesting they are mediated by physiological or immunological aspects of B. afzelii infection in the rodent host.ConclusionsManipulation of the microbiome of I. ricinus larvae had no effect on their ability to acquire B. afzelii. In contrast, B. afzelii infection in the mouse had dramatic effects on the composition of the gut microbiome in I. ricinus nymphs. Our study demonstrates that vector-borne infections in the vertebrate host shape the microbiome of the arthropod vector.

Published
2021

45. Infection with Borrelia afzelii reduces moulting time of Ixodes ricinus ticks

Author

Georgia Hurry, Elodie Maluenda, Anouk Sarr, Alessandro Belli, Phineas Hamilton, Olivier Duron, Olivier Plantard, and Maarten Voordouw

Subjects
fungi, parasitic diseases, bacterial infections and mycoses
Abstract

Arthropod vectors carry vector-borne pathogens that cause infectious disease in vertebrate hosts, and arthropod-associated non-pathogenic microorganisms. Both types of micro-organisms can influence the fitness of their arthropod vectors, and hence the epidemiology of vector-borne diseases. The bacterium Borrelia afzelii, which causes Lyme disease in Europe, is transmitted among vertebrate reservoir hosts by Ixodes ricinus ticks, which also harbour a large diversity of non-pathogenic bacteria. The purpose of this study was to test experimentally whether B. afzelii and tick-associated non-pathogenic bacteria influence the fitness of I. ricinus. Eggs obtained from field-collected adult female ticks were washed with bleach, which reduced the abundance of non-pathogenic bacteria in the hatched I. ricinus larvae by 28-fold compared to larvae that hatched from eggs washed with water. The dysbiosed and control larvae were subsequently fed on B. afzelii-infected or uninfected control mice, and the engorged larvae were allowed to moult into nymphs under laboratory conditions. I. ricinus larvae that fed on B. afzelii-infected mice had a significantly faster larva-to-nymph moulting time compared to larvae that fed on uninfected control mice. In contrast, we found no evidence that B. afzelii infection or larval dysbiosis influenced the four other life history traits of the immature I. ricinus ticks, which included engorged larval weight, unfed nymphal weight, larva-to-nymph moulting success, and immature tick survival. A power analysis found that our sampling effort had sufficient power (>80%) to detect small effects (difference of 5% – 10%) of either B. afzelii infection or larval dysbiosis. Under the laboratory conditions of our study, B. afzelii appears to be a mostly passive passenger in I. Ricinus ticks.

Published
2021

46. Vector competence of the African argasid tick Ornithodoros moubata for the Q fever agent Coxiella burnetii

Author

Maxime Duhayon, Matteo Bonazzi, Franck Cantet, Olivier Duron, Marie Buysse, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Animal, Santé, Territoires, Risques et Ecosystèmes (UMR ASTRE), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Département Systèmes Biologiques (Cirad-BIOS), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad), Institut de Recherche en Infectiologie de Montpellier (IRIM), Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), Evolution of host-microbe communities (MIVEGEC-EVCO), Processus Écologiques et Évolutifs au sein des Communautés (PEEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), and Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)

Subjects
Male, Bacterial Diseases, Life Cycles, Transovarial transmission, Physiology, [SDV]Life Sciences [q-bio], RC955-962, Disease Vectors, L73 - Maladies des animaux, Pathology and Laboratory Medicine, law.invention, Feces, Medical Conditions, Ticks, law, Arctic medicine. Tropical medicine, Medicine and Health Sciences, Polymerase chain reaction, 0303 health sciences, biology, Transmission (medicine), [SDV.BA]Life Sciences [q-bio]/Animal biology, Arthropod Vectors, Eukaryota, 3. Good health, Bacterial Pathogens, Body Fluids, Vecteur de maladie, Infectious Diseases, Blood, Intracellular Pathogens, Fièvre q, Coxiella burnetii, Medical Microbiology, Female, Public aspects of medicine, RA1-1270, Pathogens, Anatomy, Q Fever, L72 - Organismes nuisibles des animaux, Research Article, Arthropoda, Excretion, Q fever, Tick, Microbiology, 03 medical and health sciences, Ornithodoros moubata, Arachnida, parasitic diseases, medicine, Animals, Ornithodoros, Microbial Pathogens, Transmission des maladies, 030304 developmental biology, Ixodes, 030306 microbiology, Public Health, Environmental and Occupational Health, Organisms, Biology and Life Sciences, biology.organism_classification, medicine.disease, bacterial infections and mycoses, Virology, Invertebrates, Nymphs, Vector-Borne Diseases, Species Interactions, Vector (epidemiology), bacteria, Physiological Processes, Zoology, Developmental Biology
Abstract

Q fever is a widespread zoonotic disease caused by the intracellular bacterium Coxiella burnetii. While transmission is primarily but not exclusively airborne, ticks are usually thought to act as vectors on the basis of early microscopy studies. However, recent observations revealed that endosymbionts of ticks have been commonly misidentified as C. burnetii, calling the importance of tick-borne transmission into question. In this study, we re-evaluated the vector competence of the African soft tick Ornithodoros moubata for an avirulent strain of C. burnetii. To this end, we used an artificial feeding system to initiate infection of ticks, specific molecular tools to monitor further infections, and culture assays in axenic and cell media to check for the viability of C. burnetii excreted by ticks. We observed typical traits associated with vector competence: The exposure to an infected blood meal resulted in viable and persistent infections in ticks, trans-stadial transmissions of infection from nymphs to adults and the ability of adult ticks to transmit infectious C. burnetii. However, in contrast to early studies, we found that infection differed substantially between tick organs. In addition, while adult female ticks were infected, we did not observe C. burnetii in eggs, suggesting that transovarial transmission is not effective. Finally, we detected only a sporadic presence of C. burnetii DNA in tick faeces, but no living bacterium was further isolated in culture assays, suggesting that excretion in faeces is not a common mode of transmission in O. moubata., Author summary The intracellular bacterium Coxiella burnetii is the agent of Q fever, a widespread zoonotic disease. Some early detection reports and microscopy studies identified ticks as vectors of Q fever but more recent studies and molecular analyses revealed that endosymbionts of ticks have been commonly misidentified as C. burnetii: It raises questions of whether ticks play an important role in Q fever transmission. In our study, we therefore experimentally re-evaluate the vector competence of the African soft tick Ornithodoros moubata for C. burnetii. We found that O. moubata can be infected by C. burnetii after the exposure to an infected blood meal. It resulted in viable and persistent infections in ticks, a trans-stadial transmission and the ability of adult ticks to transmit infection when feeding. Infection was however not transmitted transovarially or by faeces as early reported. Overall, we conclude that O. moubata may act as a driver of the transmission and of the spatial dispersal of Q fever among vertebrates where this tick is present in Africa.

Published
2021

47. Expected transitions in ticks and their heritable endosymbionts under environmental changes

Author

Yuval Gottlieb and Olivier Duron

Subjects
fungi, sense organs, biochemical phenomena, metabolism, and nutrition, skin and connective tissue diseases
Abstract

Within arthropods, ticks harbour among the highest diversity of heritable endosymbionts reported so far, encompassing at least ten different bacterial genera. While the function of these heritable endosymbionts has not been fully determined yet, they have the potential to deeply influence the ecology of ticks impacted by climate change. This chapter focuses on the impact of heritable endosymbionts on tick growth, reproduction, survival and adaptation under environmental changes caused by climate change.

Published
2021

48. Allergy to Mammalian Meat Linked to Alpha-Gal Syndrome Potentially After Tick Bite in the Amazon: A Case Series

Author

Florent Roche, Maryvonne Dueymes, Geneviève Guillot, Angèle Soria, Mathieu Nacher, Félix Djossou, Olivier Duron, Loïc Epelboin, Centre Hospitalier Andrée Rosemon [Cayenne, Guyane Française], Ecosystemes Amazoniens et Pathologie Tropicale (EPat), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Guyane (UG), Centre d'investigation clinique Antilles-Guyane (CIC - Antilles Guyane), Institut National de la Santé et de la Recherche Médicale (INSERM)-CHU Pointe-à-Pitre/Abymes [Guadeloupe] -CHU de la Martinique [Fort de France]-Centre Hospitalier Andrée Rosemon [Cayenne, Guyane Française], Université des Antilles - UFR des sciences médicales Hyacinthe Bastaraud (UA UFR SM), Université des Antilles (UA), Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Service de dermatologie et allergologie [CHU Tenon], CHU Tenon [AP-HP], Sorbonne Université (SU)-Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Sorbonne Université (SU)-Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP), and Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Sorbonne Université (SU)

Subjects
Adult, Male, medicine.medical_specialty, Allergy, 030231 tropical medicine, Tick, Immunoglobulin E, Article, 03 medical and health sciences, 0302 clinical medicine, Food allergy, Virology, parasitic diseases, medicine, Humans, Ingestion, 030212 general & internal medicine, [SDV.IMM.ALL]Life Sciences [q-bio]/Immunology/Allergology, Tick Bites, biology, Angioedema, business.industry, Galactose, food and beverages, Middle Aged, biology.organism_classification, medicine.disease, Dermatology, French Guiana, 3. Good health, Red Meat, Infectious Diseases, biology.protein, Red meat, Female, Parasitology, medicine.symptom, Antibody, business, [SDV.AEN]Life Sciences [q-bio]/Food and Nutrition, Food Hypersensitivity
Abstract

The past decade has seen the emergence of a new type of food allergy occurring after ingestion of mammalian meat. This allergy is related to immunoglobulin (Ig)E specific for galactose-alpha-1,3 galactose (α-Gal). Originally described in the United States in 2009, other cases have subsequently been described in Australia and in Europe, but still very few in Latin America. The purpose of this study was to show the existence of this pathology in French Guiana and to describe the historical, clinical, and biological characteristics of these patients. Patients reporting an allergy to mammalian meat were included between September 2017 and August 2019. Eleven patients were included, nine of whom exhibited digestive symptoms; four, urticaria reactions; three, respiratory reactions; and five angioedema. The time between ingestion of red meat and reaction varied between 1.5 and 6 hours. The implicated meats were most often beef and pork. All patients had been regularly exposed to tick bites before the appearance of symptoms. All the samples (n = 7) were positive for anti-α-Gal anti-mammalian meats IgE. All the patients were Caucasian French expatriates. This study confirms the presence of this new entity in French Guiana and is the largest reported in Latin America. Our results do not clearly allow us to state that tick bites are the cause of this allergy, but all patients reported being exposed regularly to these arthropods.

Published
2021

49. A novel Borrelia species, intermediate between Lyme disease and relapsing fever groups, in neotropical passerine-associated ticks

Author

Florian Binetruy, Bruno Faivre, Stéphane Garnier, Marie Buysse, Valérie Noël, Nathalie Boulanger, Olivier Duron, Emilie Talagrand-Reboul, Etienne Loire, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Biogéosciences [UMR 6282] (BGS), Université de Bourgogne (UB)-Centre National de la Recherche Scientifique (CNRS), Virulence bactérienne précoce : fonctions cellulaires et contrôle de l'infection aiguë et subaiguë, Université de Strasbourg (UNISTRA), Animal, Santé, Territoires, Risques et Ecosystèmes (UMR ASTRE), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Département Systèmes Biologiques (Cirad-BIOS), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad), Evolution Théorique et Expérimentale (MIVEGEC-ETE), Perturbations, Evolution, Virulence (PEV), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Evolution of host-microbe communities (MIVEGEC-EVCO), Processus Écologiques et Évolutifs au sein des Communautés (PEEC), Biogéosciences [UMR 6282] [Dijon] (BGS), and Centre National de la Recherche Scientifique (CNRS)-Université de Bourgogne (UB)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement

Subjects
0301 basic medicine, relapsing fever, [SDV]Life Sciences [q-bio], lcsh:Medicine, L73 - Maladies des animaux, Genome, 0302 clinical medicine, Lyme disease, Ticks, Amblyomma, Genus, RNA, Ribosomal, 16S, lcsh:Science, Lyme Disease, Multidisciplinary, biology, Relapsing Fever, Passerine, 3. Good health, Vecteur de maladie, Espèce nouvelle, Pathogens, L72 - Organismes nuisibles des animaux, DNA, Bacterial, 030231 tropical medicine, Zoology, Tick, Article, Borréliose, 03 medical and health sciences, Borrelia, biology.animal, medicine, Animals, Bacteria, Whole Genome Sequencing, lcsh:R, medicine.disease, biology.organism_classification, bacterial infections and mycoses, 030104 developmental biology, Candidatus, lcsh:Q, [SDV.SPEE]Life Sciences [q-bio]/Santé publique et épidémiologie, Genome, Bacterial
Abstract

Lyme disease (LD) and relapsing fevers (RF) are vector-borne diseases caused by bacteria of the Borrelia genus. Here, we report on the widespread infection by a non-described Borrelia species in passerine-associated ticks in tropical rainforests of French Guiana, South America. This novel Borrelia species is common in two tick species, Amblyomma longirostre and A. geayi, which feed on a broad variety of neotropical mammal and bird species, including migratory species moving to North America. The novel Borrelia species is divergent from the LD and RF species, and is more closely related to the reptile- and echidna-associated Borrelia group that was recently described. Genome sequencing showed that this novel Borrelia sp. has a relatively small genome consisting of a 0.9-Mb-large chromosome and an additional 0.3 Mb dispersed on plasmids. It harbors an RF-like genomic organization but with a unique mixture of LD- and RF-specific genes, including genes used by RF Borrelia for the multiphasic antigen-switching system and a number of immune-reactive protein genes used for the diagnosis of LD. Overall, our data indicate that this novel Borrelia is an intermediate taxon between the LD and RF species that may impact a large host spectrum, including American mammals. The designation “Candidatus Borrelia mahuryensis” is proposed for this species.

Published
2020

50. Convergence of Nutritional Symbioses in Obligate Blood Feeders

Author

Olivier Duron, Yuval Gottlieb, Evolution of host-microbe communities (MIVEGEC-EVCO), Processus Écologiques et Évolutifs au sein des Communautés (PEEC), Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Centre de Recherche en Ecologie et Evolution de la Santé (CREES), Institut de Recherche pour le Développement (IRD)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), and The Hebrew University of Jerusalem (HUJ)

Subjects
0301 basic medicine, Insecta, Hematophagy, B vitamins, 030231 tropical medicine, Biotin, 03 medical and health sciences, 0302 clinical medicine, Symbiosis, Gut bacteria, Operon, Animals, 2. Zero hunger, Phylogenetic tree, biology, Obligate, food and beverages, Feeding Behavior, biology.organism_classification, Biological Evolution, 030104 developmental biology, Infectious Diseases, Evolutionary biology, Parasitology, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, [SDV.AEN]Life Sciences [q-bio]/Food and Nutrition, Bacteria, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Abstract

International audience; Symbiosis with intracellular or gut bacteria is essential for the nutrition of animals with an obligate blood-feeding habit. Divergent bacterial lineages have independently evolved functional interactions with obligate blood feeders, but all converge to an analogous biochemical feature: the provisioning of B vitamins. Although symbionts and blood feeders coevolved interdependently for millions of years we stress that their associations are not necessarily stable. Ancestral symbionts can be replaced by recently acquired bacteria with similar biochemical features, a dynamic that emerges through a combination of phylogenetic and ecological constraints. Specifically, we highlight the lateral transfer of a streamlined biotin (B7 vitamin) operon, and conjecture that its extensive spread across bacterial lineages may drive the emergence of novel nutritional symbioses with blood feeders.

Published
2020

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