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1. Development, feeding, and sex shape the relative quantity of the nutritional obligatory symbiont Wolbachia in bed bugs

Author

Marius Poulain, Elodie Rosinski, Hélène Henri, Séverine Balmand, Marie-Laure Delignette-Muller, Abdelaziz Heddi, Romain Lasseur, Fabrice Vavre, Anna Zaidman-Rémy, and Natacha Kremer

Subjects
Cimex lectularius, Wolbachia, nutritional symbiosis, host-symbiont interaction, bacterial growth dynamics, development, Microbiology, QR1-502
Abstract

The common bed bug, Cimex lectularius, is a hemipteran insect that feeds only on blood, and whose bites cause public health issues. Due to globalization and resistance to insecticides, this pest has undergone a significant and global resurgence in recent decades. Blood is an unbalanced diet, lacking notably sufficient B vitamins. Like all strict hematophagous arthropods, bed bugs host a nutritional symbiont supplying B vitamins. In C. lectularius, this nutritional symbiont is the intracellular bacterium Wolbachia (wCle). It is located in specific symbiotic organs, the bacteriomes, as well as in ovaries. Experimental depletion of wCle has been shown to result in longer nymphal development and lower fecundity. These phenotypes were rescued by B vitamin supplementation. Understanding the interaction between wCle and the bed bug may help to develop new pest control methods targeting the disruption of this symbiotic interaction. The objective of this work was thus to quantify accurately the density of wCle over the life cycle of the host and to describe potential associated morphological changes in the bacteriome. We also sought to determine the impact of sex, feeding status, and aging on the bacterial population dynamics. We showed that the relative quantity of wCle continuously increases during bed bug development, while the relative size of the bacteriome remains stable. We also showed that adult females harbor more wCle than males and that wCle relative quantity decreases slightly in adults with age, except in weekly-fed males. These results are discussed in the context of bed bug ecology and will help to define critical points of the symbiotic interaction during the bed bug life cycle.

Published
2024
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2. Coordination of host and endosymbiont gene expression governs endosymbiont growth and elimination in the cereal weevil Sitophilus spp.

Author

Mariana Galvão Ferrarini, Agnès Vallier, Carole Vincent-Monégat, Elisa Dell’Aglio, Benjamin Gillet, Sandrine Hughes, Ophélie Hurtado, Guy Condemine, Anna Zaidman-Rémy, Rita Rebollo, Nicolas Parisot, and Abdelaziz Heddi

Subjects
Microbial ecology, QR100-130
Abstract

Abstract Background Insects living in nutritionally poor environments often establish long-term relationships with intracellular bacteria that supplement their diets and improve their adaptive and invasive powers. Even though these symbiotic associations have been extensively studied on physiological, ecological, and evolutionary levels, few studies have focused on the molecular dialogue between host and endosymbionts to identify genes and pathways involved in endosymbiosis control and dynamics throughout host development. Results We simultaneously analyzed host and endosymbiont gene expression during the life cycle of the cereal weevil Sitophilus oryzae, from larval stages to adults, with a particular emphasis on emerging adults where the endosymbiont Sodalis pierantonius experiences a contrasted growth-climax-elimination dynamics. We unraveled a constant arms race in which different biological functions are intertwined and coregulated across both partners. These include immunity, metabolism, metal control, apoptosis, and bacterial stress response. Conclusions The study of these tightly regulated functions, which are at the center of symbiotic regulations, provides evidence on how hosts and bacteria finely tune their gene expression and respond to different physiological challenges constrained by insect development in a nutritionally limited ecological niche. Graphical Abstract Video Abstract

Published
2023
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4. Efficient compartmentalization in insect bacteriomes protects symbiotic bacteria from host immune system

Author

Mariana Galvão Ferrarini, Elisa Dell’Aglio, Agnès Vallier, Séverine Balmand, Carole Vincent-Monégat, Sandrine Hughes, Benjamin Gillet, Nicolas Parisot, Anna Zaidman-Rémy, Cristina Vieira, Abdelaziz Heddi, and Rita Rebollo

Subjects
Symbiosis, Immunity, Bacteria, Antimicrobial peptides, Coleoptera, TCT, Microbial ecology, QR100-130
Abstract

Abstract Background Many insects house symbiotic intracellular bacteria (endosymbionts) that provide them with essential nutrients, thus promoting the usage of nutrient-poor habitats. Endosymbiont seclusion within host specialized cells, called bacteriocytes, often organized in a dedicated organ, the bacteriome, is crucial in protecting them from host immune defenses while avoiding chronic host immune activation. Previous evidence obtained in the cereal weevil Sitophilus oryzae has shown that bacteriome immunity is activated against invading pathogens, suggesting endosymbionts might be targeted and impacted by immune effectors during an immune challenge. To pinpoint any molecular determinants associated with such challenges, we conducted a dual transcriptomic analysis of S. oryzae’s bacteriome subjected to immunogenic peptidoglycan fragments. Results We show that upon immune challenge, the bacteriome actively participates in the innate immune response via induction of antimicrobial peptides (AMPs). Surprisingly, endosymbionts do not undergo any transcriptomic changes, indicating that this potential threat goes unnoticed. Immunohistochemistry showed that TCT-induced AMPs are located outside the bacteriome, excluding direct contact with the endosymbionts. Conclusions This work demonstrates that endosymbiont protection during an immune challenge is mainly achieved by efficient confinement within bacteriomes, which provides physical separation between host systemic response and endosymbionts. Video Abstract

Published
2022
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6. Transcriptomic-based selection of reference genes for quantitative real-time PCR in an insect endosymbiotic model

Author

Agnès Vallier, Elisa Dell’Aglio, Mariana Galvão Ferrarini, Ophélie Hurtado, Carole Vincent-Monégat, Abdelaziz Heddi, Rita Rebollo, and Anna Zaidman-Rémy

Subjects
real-time PCR, insect, symbiosis, transcriptomic, normalization, Evolution, QH359-425, Ecology, QH540-549.5
Abstract

Reference genes are a fundamental tool for analyses of gene expression by real-time quantitative PCR (qRT-PCR), in that they ensure the correct comparison between conditions, stages, or treatments. Because of this, selection of appropriate genes to use as references is crucial for proper application of the technique. Nevertheless, efforts to find appropriate, stably expressed transcripts are still lacking, in particular in the field of insect science. Here, we took advantage of a massive transcriptomic high-throughput analysis of various developmental stages of the gut and associated-bacteriomes of the cereal weevil Sitophilus oryzae and identified a subset of stably expressed genes with the potential to be used as housekeeping genes from the larva to the adult stage. We employed several normalization techniques to select the most suitable genes among our subset. Our final selection includes two genes–TAO, and YTH3–which can also be used to compare transcript abundance at various developmental stages in symbiotic insects, and in insects devoid of endosymbionts (aposymbiotic). Since they are well conserved, these genes have the potential to be useful for many other insect species. This work confirms the interest in using large-scale, unbiased methods for reference gene selection.

Published
2023
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7. Endosymbiont-containing germarium transcriptional survey in a cereal weevil depicts downregulation of immune effectors at the onset of sexual maturity

Author

Mariana Galvão Ferrarini, Agnès Vallier, Elisa Dell’Aglio, Séverine Balmand, Carole Vincent-Monégat, Mériem Debbache, Justin Maire, Nicolas Parisot, Anna Zaidman-Rémy, Abdelaziz Heddi, and Rita Rebollo

Subjects
coleoptera, symbiosis, bacteriome, bacteria, interaction, Physiology, QP1-981
Abstract

Insects often establish long-term relationships with intracellular symbiotic bacteria, i.e., endosymbionts, that provide them with essential nutrients such as amino acids and vitamins. Endosymbionts are typically confined within specialized host cells called bacteriocytes that may form an organ, the bacteriome. Compartmentalization within host cells is paramount for protecting the endosymbionts and also avoiding chronic activation of the host immune system. In the cereal weevil Sitophilus oryzae, bacteriomes are present as a single organ at the larval foregut-midgut junction, and in adults, at the apex of midgut mesenteric caeca and at the apex of the four ovarioles. While the adult midgut endosymbionts experience a drastic proliferation during early adulthood followed by complete elimination through apoptosis and autophagy, ovarian endosymbionts are maintained throughout the weevil lifetime by unknown mechanisms. Bacteria present in ovarian bacteriomes are thought to be involved in the maternal transmission of endosymbionts through infection of the female germline, but the exact mode of transmission is not fully understood. Here, we show that endosymbionts are able to colonize the germarium in one-week-old females, pinpointing a potential infection route of oocytes. To identify potential immune regulators of ovarian endosymbionts, we have analyzed the transcriptomes of the ovarian bacteriomes through young adult development, from one-day-old adults to sexually mature ones. In contrast with midgut bacteriomes, immune effectors are downregulated in ovarian bacteriomes at the onset of sexual maturation. We hypothesize that relaxation of endosymbiont control by antimicrobial peptides might allow bacterial migration and potential oocyte infection, ensuring endosymbiont transmission.

Published
2023
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9. The transposable element-rich genome of the cereal pest Sitophilus oryzae

Author

Nicolas Parisot, Carlos Vargas-Chávez, Clément Goubert, Patrice Baa-Puyoulet, Séverine Balmand, Louis Beranger, Caroline Blanc, Aymeric Bonnamour, Matthieu Boulesteix, Nelly Burlet, Federica Calevro, Patrick Callaerts, Théo Chancy, Hubert Charles, Stefano Colella, André Da Silva Barbosa, Elisa Dell’Aglio, Alex Di Genova, Gérard Febvay, Toni Gabaldón, Mariana Galvão Ferrarini, Alexandra Gerber, Benjamin Gillet, Robert Hubley, Sandrine Hughes, Emmanuelle Jacquin-Joly, Justin Maire, Marina Marcet-Houben, Florent Masson, Camille Meslin, Nicolas Montagné, Andrés Moya, Ana Tereza Ribeiro de Vasconcelos, Gautier Richard, Jeb Rosen, Marie-France Sagot, Arian F. A. Smit, Jessica M. Storer, Carole Vincent-Monegat, Agnès Vallier, Aurélien Vigneron, Anna Zaidman-Rémy, Waël Zamoum, Cristina Vieira, Rita Rebollo, Amparo Latorre, and Abdelaziz Heddi

Subjects
Coleoptera, Weevil, Sitophilus oryzae, Genome, Transposable elements, Endosymbiosis, Biology (General), QH301-705.5
Abstract

Abstract Background The rice weevil Sitophilus oryzae is one of the most important agricultural pests, causing extensive damage to cereal in fields and to stored grains. S. oryzae has an intracellular symbiotic relationship (endosymbiosis) with the Gram-negative bacterium Sodalis pierantonius and is a valuable model to decipher host-symbiont molecular interactions. Results We sequenced the Sitophilus oryzae genome using a combination of short and long reads to produce the best assembly for a Curculionidae species to date. We show that S. oryzae has undergone successive bursts of transposable element (TE) amplification, representing 72% of the genome. In addition, we show that many TE families are transcriptionally active, and changes in their expression are associated with insect endosymbiotic state. S. oryzae has undergone a high gene expansion rate, when compared to other beetles. Reconstruction of host-symbiont metabolic networks revealed that, despite its recent association with cereal weevils (30 kyear), S. pierantonius relies on the host for several amino acids and nucleotides to survive and to produce vitamins and essential amino acids required for insect development and cuticle biosynthesis. Conclusions Here we present the genome of an agricultural pest beetle, which may act as a foundation for pest control. In addition, S. oryzae may be a useful model for endosymbiosis, and studying TE evolution and regulation, along with the impact of TEs on eukaryotic genomes.

Published
2021
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13. Endosymbiosis morphological reorganization during metamorphosis diverges in weevils

Author

Justin Maire, Bessem Chouaia, Anna Zaidman-Rémy, and Abdelaziz Heddi

Subjects
symbiosis, bacteriome, metamorphosis, weevil, dryophthoridae, evolution, insect, rhynchophorus, nardonella, sitophilus, Biology (General), QH301-705.5
Abstract

Virtually all animals associate with beneficial symbiotic bacteria. Whether and how these associations are modulated across a host’s lifecycle is an important question in disentangling animal-bacteria interactions. We recently reported a case of complete morphological reorganization of symbiosis during metamorphosis of the cereal weevil, Sitophilus oryzae. In this model, the bacteriome, a specialized organ that houses the intracellular bacterium Sodalis pierantonius, undergoes a two-phase remodeling program synchronously driven by host and endosymbiont, resulting in a localization shift and the formation of multiple new bacteriomes. Here, we provide comparative data in a closely-related coleopteran, the red palm weevil Rhynchophorus ferrugineus, which is associated with the ancestral endosymbiont Nardonella. Using cell imaging experiments, we show that the red pal weevil bacteriome remains unchanged during metamorphosis, hence contrasting with what we reported in the cereal weevil S. oryzae. These findings highlight the complexity and divergence of host-symbiont interactions and their intertwining with host development, even in closely-related species. Abbreviations: DAPI: 4′,6-diamidino-2-phenylindole; FISH: Fluorescence in situ hybridization; T3SS: Type III secretion system.

Published
2020
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14. The transposable element-rich genome of the cereal pest Sitophilus oryzae

Author

Parisot, Nicolas, Vargas-Chávez, Carlos, Goubert, Clément, Baa-Puyoulet, Patrice, Balmand, Séverine, Beranger, Louis, Blanc, Caroline, Bonnamour, Aymeric, Boulesteix, Matthieu, Burlet, Nelly, Calevro, Federica, Callaerts, Patrick, Chancy, Théo, Charles, Hubert, Colella, Stefano, Da Silva Barbosa, André, Dell’Aglio, Elisa, Di Genova, Alex, Febvay, Gérard, Gabaldón, Toni, Galvão Ferrarini, Mariana, Gerber, Alexandra, Gillet, Benjamin, Hubley, Robert, Hughes, Sandrine, Jacquin-Joly, Emmanuelle, Maire, Justin, Marcet-Houben, Marina, Masson, Florent, Meslin, Camille, Montagné, Nicolas, Moya, Andrés, Ribeiro de Vasconcelos, Ana Tereza, Richard, Gautier, Rosen, Jeb, Sagot, Marie-France, Smit, Arian F. A., Storer, Jessica M., Vincent-Monegat, Carole, Vallier, Agnès, Vigneron, Aurélien, Zaidman-Rémy, Anna, Zamoum, Waël, Vieira, Cristina, Rebollo, Rita, Latorre, Amparo, and Heddi, Abdelaziz

Published
2021
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15. What can a weevil teach a fly, and reciprocally? Interaction of host immune systems with endosymbionts in Glossina and Sitophilus

Author

Anna Zaidman-Rémy, Aurélien Vigneron, Brian L Weiss, and Abdelaziz Heddi

Subjects
Cereal weevil, Tsetse fly, Endosymbiosis, Immunity, Evolution, Insects, Microbiology, QR1-502
Abstract

Abstract The tsetse fly (Glossina genus) is the main vector of African trypanosomes, which are protozoan parasites that cause human and animal African trypanosomiases in Sub-Saharan Africa. In the frame of the IAEA/FAO program ‘Enhancing Vector Refractoriness to Trypanosome Infection’, in addition to the tsetse, the cereal weevil Sitophilus has been introduced as a comparative system with regards to immune interactions with endosymbionts. The cereal weevil is an agricultural pest that destroys a significant proportion of cereal stocks worldwide. Tsetse flies are associated with three symbiotic bacteria, the multifunctional obligate Wigglesworthia glossinidia, the facultative commensal Sodalis glossinidius and the parasitic Wolbachia. Cereal weevils house an obligatory nutritional symbiosis with the bacterium Sodalis pierantonius, and occasionally Wolbachia. Studying insect host-symbiont interactions is highly relevant both for understanding the evolution of symbiosis and for envisioning novel pest control strategies. In both insects, the long co-evolution between host and endosymbiont has led to a stringent integration of the host-bacteria partnership. These associations were facilitated by the development of specialized host traits, including symbiont-housing cells called bacteriocytes and specific immune features that enable both tolerance and control of the bacteria. In this review, we compare the tsetse and weevil model systems and compile the latest research findings regarding their biological and ecological similarities, how the immune system controls endosymbiont load and location, and how host-symbiont interactions impact developmental features including cuticle synthesis and immune system maturation. We focus mainly on the interactions between the obligate symbionts and their host’s immune systems, a central theme in both model systems. Finally, we highlight how parallel studies on cereal weevils and tsetse flies led to mutual discoveries and stimulated research on each model, creating a pivotal example of scientific improvement through comparison between relatively distant models.

Published
2018
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16. An IMD-like pathway mediates both endosymbiont control and host immunity in the cereal weevil Sitophilus spp.

Author

Justin Maire, Carole Vincent-Monégat, Florent Masson, Anna Zaidman-Rémy, and Abdelaziz Heddi

Subjects
Endosymbiosis, Bacteriocyte, Antimicrobial peptide, Sitophilus, Innate immunity, Compartmentalization, Microbial ecology, QR100-130
Abstract

Abstract Many insects developing on nutritionally unbalanced diets have evolved symbiotic associations with vertically transmitted intracellular bacteria (endosymbionts) that provide them with metabolic components, thereby improving the host’s abilities to thrive on such poor ecological niches. While host-endosymbiont coevolutionary constraints are known to entail massive genomic changes in the microbial partner, host’s genomic evolution remains elusive, particularly with regard to the immune system. In the cereal weevil Sitophilus spp., which houses Sodalis pierantonius, endosymbionts are secluded in specialized host cells, the bacteriocytes that group together as an organ, the bacteriome. We previously reported that at standard conditions, the bacteriome highly expresses the coleoptericin A (colA) antimicrobial peptide (AMP), which was shown to prevent endosymbiont escape from the bacteriocytes. However, following the insect systemic infection by pathogens, the bacteriome upregulates a cocktail of AMP encoding genes, including colA. The regulations that allow these contrasted immune responses remain unknown. In this short report, we provide evidence that an IMD-like pathway is conserved in two sibling species of cereal weevils, Sitophilus oryzae and Sitophilus zeamais. RNA interference (RNAi) experiments showed that imd and relish genes are essential for (i) colA expression in the bacteriome under standard conditions, (ii) AMP up-regulation in the bacteriome following a systemic immune challenge, and (iii) AMP systemic induction following an immune challenge. Histological analyses also showed that relish inhibition by RNAi resulted in endosymbiont escape from the bacteriome, strengthening the involvement of an IMD-like pathway in endosymbiont control. We conclude that Sitophilus’ IMD-like pathway mediates both the bacteriome immune program involved in endosymbiont seclusion within the bacteriocytes and the systemic and local immune responses to exogenous challenges. This work provides a striking example of how a conserved immune pathway, initially described as essential in pathogen clearance, also functions in the control of mutualistic associations.

Published
2018
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18. Coordination of host and endosymbiont gene expression governs endosymbiont growth and elimination in the cereal weevilSitophilusspp

Author

Ferrarini, Mariana Galvão, primary, Vallier, Agnès, additional, Vincent-Monégat, Carole, additional, Dell’Aglio, Elisa, additional, Gillet, Benjamin, additional, Hughes, Sandrine, additional, Hurtado, Ophélie, additional, Condemine, Guy, additional, Zaidman-Rémy, Anna, additional, Rebollo, Rita, additional, Parisot, Nicolas, additional, and Heddi, Abdelaziz, additional

Published
2023
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19. Coordination of host and endosymbiont gene expression governs endosymbiont growth and elimination in the cereal weevilSitophilusspp

Author

Mariana Galvão Ferrarini, Agnès Vallier, Carole Vincent-Monégat, Elisa Dell’Aglio, Benjamin Gillet, Sandrine Hughes, Ophélie Hurtado, Guy Condemine, Anna Zaidman-Rémy, Rita Rebollo, Nicolas Parisot, and Abdelaziz Heddi

Abstract

Insects living in nutritionally poor environments often establish long-term relationships with intracellular bacteria that supplement their diets and improve their adaptive and invasive powers. Even though these symbiotic associations have been extensively studied on physiological, ecological and evolutionary levels, few studies have focused on the molecular dialogue between host and endosymbionts to identify genes and pathways involved in endosymbiosis control and dynamics. We simultaneously analyzed host and endosymbiont gene expression during the life cycle of the cereal weevilSitophilus oryzae, from larval stages to adults, with a particular emphasis on emerging adults where the endosymbiontSodalis pierantoniusexperiences a contrasted growth-climax-elimination dynamics. We unraveled a constant arms race in which different biological functions are intertwined and coregulated across both partners. These include immunity, metabolism, metal control, apoptosis, and bacterial stress response. Particularly, genes from the Hippo regulatory pathway are specifically induced by endosymbiont growth, while the regulation of metal ions constitutes the basis of the arms race between the two partners at the onset of the bacterial load climax. The study of these tightly regulated functions, which are at the center of symbiotic regulations, provides evidence on how hosts and bacteria finely tune their gene expression and respond to different physiological challenges constrained by insect development in a nutritionally limited ecological niche.Graphical Abstract

Published
2023

20. Endosymbiont-containing germarium transcriptional survey in a cereal weevil depicts downregulation of immune effectors at the onset of sexual maturity

Author

Ferrarini, Mariana Galvão, primary, Vallier, Agnès, additional, Dell’Aglio, Elisa, additional, Balmand, Séverine, additional, Vincent-Monégat, Carole, additional, Debbache, Mériem, additional, Maire, Justin, additional, Parisot, Nicolas, additional, Zaidman-Rémy, Anna, additional, Heddi, Abdelaziz, additional, and Rebollo, Rita, additional

Published
2023
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21. Transcriptional survey of ovarian bacteriomes in the cereal weevil,Sitophilus oryzae, shows down-regulation of immune effectors at the onset of sexual maturity

Author

Ferrarini, Mariana Galvão, primary, Vallier, Agnès, additional, Dell’Aglio, Elisa, additional, Balmand, Séverine, additional, Vincent-Monégat, Carole, additional, Debbache, Mériem, additional, Maire, Justin, additional, Parisot, Nicolas, additional, Zaidman-Rémy, Anna, additional, Heddi, Abdelaziz, additional, and Rebollo, Rita, additional

Published
2023
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23. Transcriptional survey of ovarian bacteriomes in the cereal weevil,Sitophilus oryzae, shows down-regulation of immune effectors at the onset of sexual maturity

Author

Mariana Galvão Ferrarini, Agnès Vallier, Elisa Dell’Aglio, Séverine Balmand, Carole Vincent-Monégat, Mériem Debbache, Justin Maire, Nicolas Parisot, Anna Zaidman-Rémy, Abdelaziz Heddi, and Rita Rebollo

Abstract

Insects often establish long-term relationships with intracellular symbiotic bacteria,i.e. endosymbionts, that provide them with essential nutrients such as amino acids and vitamins. Endosymbionts are typically confined within specialized host cells called bacteriocytes that may form an organ, the bacteriome. Compartmentalization within host cells is paramount for protecting the endosymbionts and also avoiding chronic activation of the host immune system. In the cereal weevilSitophilus oryzae, bacteriomes are present as a single organ at the larval foregut-midgut junction, and in adults, at the apex of midgut mesenteric caeca and at the apex of the four ovarioles. While the adult midgut endosymbionts experience a drastic proliferation during early adulthood followed by complete elimination through apoptosis and autophagy, ovarian endosymbionts are maintained throughout the weevil lifetime by unknown mechanisms. Bacteria present in ovarian bacteriomes are thought to be involved in the maternal transmission of endosymbionts through infection of the female germline, but the exact mode of transmission is not fully understood. Here, we show that endosymbionts are able to colonize the germarium in one-week-old females, pinpointing a potential infection route of oocytes. To identify potential immune regulators of ovarian endosymbionts, we have analyzed the transcriptomes of the ovarian bacteriomes through young adult development, from one-day-old adults to sexually mature ones. In contrast with midgut bacteriomes, immune effectors are downregulated in ovarian bacteriomes at the onset of sexual maturation. We hypothesize that relaxation of endosymbiont control by antimicrobial peptides might allow bacterial migration and potential oocyte infection, ensuring endosymbiont transmission.

Published
2023

26. Additional file 2 of Efficient compartmentalization in insect bacteriomes protects symbiotic bacteria from host immune system

Author

Ferrarini, Mariana Galvão, Dell’Aglio, Elisa, Vallier, Agnès, Balmand, Séverine, Vincent-Monégat, Carole, Hughes, Sandrine, Gillet, Benjamin, Parisot, Nicolas, Zaidman-Rémy, Anna, Vieira, Cristina, Heddi, Abdelaziz, and Rebollo, Rita

Abstract

Additional file 2: Text S1. Description of genes highly expressed from S. pierantonius.

Published
2022
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27. Endosymbiont-containing germarium transcriptional survey in a cereal weevil depicts downregulation of immune effectors at the onset of sexual maturity.

Author

Galvão Ferrarini, Mariana, Vallier, Agnès, Dell’Aglio, Elisa, Balmand, Séverine, Vincent-Monégat, Carole, Debbache, Mériem, Maire, Justin, Parisot, Nicolas, Zaidman-Rémy, Anna, Heddi, Abdelaziz, and Rebollo, Rita

Subjects
CURCULIONIDAE, YOUNG adults, ESSENTIAL amino acids, RICE weevil, ANTIMICROBIAL peptides, PYRICULARIA oryzae
Abstract

Insects often establish long-term relationships with intracellular symbiotic bacteria, i.e., endosymbionts, that provide them with essential nutrients such as amino acids and vitamins. Endosymbionts are typically confined within specialized host cells called bacteriocytes that may form an organ, the bacteriome. Compartmentalization within host cells is paramount for protecting the endosymbionts and also avoiding chronic activation of the host immune system. In the cereal weevil Sitophilus oryzae, bacteriomes are present as a single organ at the larval foregut-midgut junction, and in adults, at the apex of midgut mesenteric caeca and at the apex of the four ovarioles. While the adult midgut endosymbionts experience a drastic proliferation during early adulthood followed by complete elimination through apoptosis and autophagy, ovarian endosymbionts are maintained throughout the weevil lifetime by unknown mechanisms. Bacteria present in ovarian bacteriomes are thought to be involved in the maternal transmission of endosymbionts through infection of the female germline, but the exact mode of transmission is not fully understood. Here, we show that endosymbionts are able to colonize the germarium in oneweek-old females, pinpointing a potential infection route of oocytes. To identify potential immune regulators of ovarian endosymbionts, we have analyzed the transcriptomes of the ovarian bacteriomes through young adult development, from one-day-old adults to sexually mature ones. In contrast with midgut bacteriomes, immune effectors are downregulated in ovarian bacteriomes at the onset of sexual maturation. We hypothesize that relaxation of endosymbiont control by antimicrobial peptides might allow bacterial migration and potential oocyte infection, ensuring endosymbiont transmission. [ABSTRACT FROM AUTHOR]

Published
2023
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28. Efficient compartmentalization in insect bacteriomes protects symbiotic bacteria from host immune system

Author

Ferrarini, Mariana Galvão, primary, Dell’Aglio, Elisa, additional, Vallier, Agnès, additional, Balmand, Séverine, additional, Vincent-Monégat, Carole, additional, Hughes, Sandrine, additional, Gillet, Benjamin, additional, Parisot, Nicolas, additional, Zaidman-Rémy, Anna, additional, Vieira, Cristina, additional, Heddi, Abdelaziz, additional, and Rebollo, Rita, additional

Published
2022
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29. Spatial and morphological reorganization of endosymbiosis during metamorphosis accommodates adult metabolic requirements in a weevil

Author

Sandrine Hughes, Anna Zaidman-Rémy, Séverine Balmand, Agnès Vallier, Nicolas Parisot, Mariana Galvão Ferrarini, Justin Maire, Benjamin Gillet, Abdelaziz Heddi, Carole Vincent-Monégat, Biologie Fonctionnelle, Insectes et Interactions (BF2I), Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Institut de Génomique Fonctionnelle de Lyon (IGFL), École normale supérieure - Lyon (ENS Lyon)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), École normale supérieure de Lyon (ENS de Lyon)-Université Claude Bernard Lyon 1 (UCBL), and ANR-13-BSV7-0016,IMetSym,Contrôles immunitaire et métabolique dans les symbioses intracellulaires d'insectes(2013)

Subjects
Insecta, Sodalis, food.ingredient, Cytoskeleton organization, [SDV]Life Sciences [q-bio], media_common.quotation_subject, Insect, Flagellum, Biology, 03 medical and health sciences, 0302 clinical medicine, food, Animals, Metamorphosis, Symbiosis, ComputingMilieux_MISCELLANEOUS, 030304 developmental biology, media_common, 0303 health sciences, Multidisciplinary, Endosymbiosis, fungi, Metamorphosis, Biological, Bacteriome, Midgut, Biological Sciences, Cell biology, Weevils, 030217 neurology & neurosurgery, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Abstract

Bacterial intracellular symbiosis (endosymbiosis) is widespread in nature and impacts many biological processes. In holometabolous symbiotic insects, metamorphosis entails a complete and abrupt internal reorganization that creates a constraint for endosymbiont transmission from larvae to adults. To assess how endosymbiosis copes—and potentially evolves—throughout this major host-tissue reorganization, we used the association between the cereal weevil Sitophilus oryzae and the bacterium Sodalis pierantonius as a model system. S. pierantonius are contained inside specialized host cells, the bacteriocytes, that group into an organ, the bacteriome. Cereal weevils require metabolic inputs from their endosymbiont, particularly during adult cuticle synthesis, when endosymbiont load increases dramatically. By combining dual RNA-sequencing analyses and cell imaging, we show that the larval bacteriome dissociates at the onset of metamorphosis and releases bacteriocytes that undergo endosymbiosis-dependent transcriptomic changes affecting cell motility, cell adhesion, and cytoskeleton organization. Remarkably, bacteriocytes turn into spindle cells and migrate along the midgut epithelium, thereby conveying endosymbionts to midgut sites where future mesenteric caeca will develop. Concomitantly, endosymbiont genes encoding a type III secretion system and a flagellum apparatus are transiently up-regulated while endosymbionts infect putative stem cells and enter their nuclei. Infected cells then turn into new differentiated bacteriocytes and form multiple new bacteriomes in adults. These findings show that endosymbiosis reorganization in a holometabolous insect relies on a synchronized host–symbiont molecular and cellular “choreography” and illustrates an adaptive feature that promotes bacteriome multiplication to match increased metabolic requirements in emerging adults.

Published
2020

30. The transposable element-rich genome of the cereal pest Sitophilus oryzae

Author

Arian F.A. Smit, Séverine Balmand, Stefano Colella, Nicolas Montagné, Amparo Latorre, Jessica M. Storer, Nelly Burlet, Jeb Rosen, Caroline Blanc, Federica Calevro, Marina Marcet-Houben, Marie-France Sagot, Patrick Callaerts, Waël Zamoum, Patrice Baa-Puyoulet, Anna Zaidman-Rémy, Clément Goubert, Rita Rebollo, Louis Beranger, Carlos Vargas-Chávez, Gautier Richard, Ana Tereza Ribeiro de Vasconcelos, Justin Maire, Agnès Vallier, Elisa Dell’Aglio, Florent Masson, Robert Hubley, Sandrine Hughes, Camille Meslin, Gérard Febvay, Aurélien Vigneron, Nicolas Parisot, Théo Chancy, Cristina Vieira, Abdelaziz Heddi, Alex Di Genova, Benjamin Gillet, André Da Silva Barbosa, Carole Vincent-Monégat, Emmanuelle Jacquin-Joly, Hubert Charles, Mariana Galvão Ferrarini, Matthieu Boulesteix, Toni Gabaldón, Alexandra L. Gerber, Andrés Moya, Aymeric Bonnamour, Biologie Fonctionnelle, Insectes et Interactions (BF2I), Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), 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), Catholic University of Leuven - Katholieke Universiteit Leuven (KU Leuven), 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), Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Laboratorio Nacional de Computação Cientifica [Rio de Janeiro] (LNCC / MCT), Institut de Génomique Fonctionnelle de Lyon (IGFL), École normale supérieure - Lyon (ENS Lyon)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Institute for Systems Biology [Seattle] (ISB), Barcelona Supercomputing Center - Centro Nacional de Supercomputacion (BSC - CNS), Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana [Espagne] (FISABIO), Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Université de Rennes (UR)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-INSTITUT AGRO Agrocampus Ouest, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Eléments transposables, évolution, populations, Département génétique, interactions et évolution des génomes [LBBE] (GINSENG), 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), Institut d'écologie et des sciences de l'environnement de Paris (iEES Paris ), Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), École normale supérieure de Lyon (ENS de Lyon)-Université Claude Bernard Lyon 1 (UCBL), Université de Rennes (UR)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut Agro Rennes Angers, Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, Région Auvergne-Rhône-Alpes, European Regional Development Fund, PGC2018-099344-B-I00, Ministerio de Ciencia, Innovación y Universidades, PROMETEO/2018/133, Conselleria d’Educació, Generalitat Valenciana, Institut National des Sciences Appliquées de Lyon, ANR-10-BLAN-1701, Agence Nationale de la Recherche, IDEX-Lyon PALSE IMPULSION, Ministerio de Economía y Competitividad, ANR-17-CE20-0031,GREEN,Comprendre les mécanismes de régulation et la fonction des gènes de la réponse immunitaire de l'hôte pour perturber la symbiose et le contrôle des endosymbiotes chez les insectes nuisibles(2017), ANR-17-CE20-0015,Unleash,Découverte de la relation entre épigénétique et symbiose chez l'insecte(2017), Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Barcelona Supercomputing Center, Agence Nationale de la Recherche (France), European Commission, Agencia Estatal de Investigación (España), Ministerio de Ciencia, Innovación y Universidades (España), Generalitat Valenciana, and Ministerio de Economía y Competitividad (España)

Subjects
Life Sciences & Biomedicine - Other Topics, Weevil, ALPHA-AMYLASE INHIBITORS, Physiology, Cell Communication, Plant Science, drosophila immune-response, Genome, HORIZONTAL GENE-TRANSFER, MULTIPLE SEQUENCE ALIGNMENT, 0302 clinical medicine, Structural Biology, Biology (General), Sitophilus oryzae Genome, 2. Zero hunger, Genetics, 0303 health sciences, Endosymbiosis Immunity, biology, Endosymbiosis, horizontal gene-transfer, Sitophilus, Sitophilus oryzae, food and beverages, wide analysis, Coleoptera, RED FLOUR BEETLE, Horizontal gene transfer, multiple sequence alignment, Agricultural pests, stored-product insects, phosphine resistance, General Agricultural and Biological Sciences, Life Sciences & Biomedicine, Research Article, DIGESTIVE PROTEINASES, Biotechnology, Informàtica::Aplicacions de la informàtica::Bioinformàtica [Àrees temàtiques de la UPC], Transposable element, Sodalis, food.ingredient, QH301-705.5, PRIMARY ENDOSYMBIONT, Evolution, alpha-amylase inhibitors, General Biochemistry, Genetics and Molecular Biology, 03 medical and health sciences, Rice weevil, food, STORED-PRODUCT INSECTS, [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], PHOSPHINE RESISTANCE, Animals, Humans, DROSOPHILA IMMUNE-RESPONSE, Red flour beetle, Biology, Ecology, Evolution, Behavior and Systematics, 030304 developmental biology, [SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE], Science & Technology, Immunity, Cell Biology, primary endosymbiont, biology.organism_classification, digestive proteinases, Genòmica, [SDV.GEN.GA]Life Sciences [q-bio]/Genetics/Animal genetics, red flour beetle, DNA Transposable Elements, Weevils, Edible Grain, WIDE ANALYSIS, Transposable elements, 030217 neurology & neurosurgery, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis, Developmental Biology
Abstract

Parisot et al., [Background]: The rice weevil Sitophilus oryzae is one of the most important agricultural pests, causing extensive damage to cereal in fields and to stored grains. S. oryzae has an intracellular symbiotic relationship (endosymbiosis) with the Gram-negative bacterium Sodalis pierantonius and is a valuable model to decipher host-symbiont molecular interactions., [Results]: We sequenced the Sitophilus oryzae genome using a combination of short and long reads to produce the best assembly for a Curculionidae species to date. We show that S. oryzae has undergone successive bursts of transposable element (TE) amplification, representing 72% of the genome. In addition, we show that many TE families are transcriptionally active, and changes in their expression are associated with insect endosymbiotic state. S. oryzae has undergone a high gene expansion rate, when compared to other beetles. Reconstruction of host-symbiont metabolic networks revealed that, despite its recent association with cereal weevils (30 kyear), S. pierantonius relies on the host for several amino acids and nucleotides to survive and to produce vitamins and essential amino acids required for insect development and cuticle biosynthesis., [Conclusions]: Here we present the genome of an agricultural pest beetle, which may act as a foundation for pest control. In addition, S. oryzae may be a useful model for endosymbiosis, and studying TE evolution and regulation, along with the impact of TEs on eukaryotic genomes., Funding for this project was provided by the Fondation de l’Institut National des Sciences Appliquées-Lyon (INSA-Lyon), the research direction of INSA-Lyon, the Santé des Plantes et Environnement (SPE) department at the Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (INRAE), the French ANR-10-BLAN-1701 (ImmunSymbArt), the French ANR-13-BSV7-0016-01 (IMetSym), the French ANR-17_CE20_0031_01 (GREEN), and a grant from la Région Rhône-Alpes (France) to AH. RR received funding from the French ANR-17-CE20-0015 (UNLEASH) and the IDEX-Lyon PALSE IMPULSION initiative. The project was also funded by European Regional Development Fund (ERDF) and Ministerio de Ciencia, Innovación y Universidades (Spain) PGC2018-099344-B-I00 to AL, and PID2019-105969GB-I00 to AM and Conselleria d’Educació, Generalitat Valenciana (Spain), grant number PROMETEO/2018/133 to AM. CV-C was a recipient of a fellowship from the Ministerio de Economía y Competitividad (Spain) and a grant from la Région Rhône-Alpes (France).

Published
2021

31. PGRP-LB: An Inside View into the Mechanism of the Amidase Reaction

Author

Anna Zaidman-Rémy, Carole Vincent-Monégat, Pierre Aller, Allen M. Orville, Abdelaziz Heddi, A. Butryn, Pedro Da Silva, Laurent Soulère, Julien Orlans, Catherine Sivignon, Isabelle Rahioui, Biologie Fonctionnelle, Insectes et Interactions (BF2I), Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), DIAMOND Light source, Research Complex at Harwell, Institut de Chimie et Biochimie Moléculaires et Supramoléculaires (ICBMS), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Institut de Chimie du CNRS (INC)-École Supérieure Chimie Physique Électronique de Lyon-Centre National de la Recherche Scientifique (CNRS), and ANR-17-CE20-0031,GREEN,Comprendre les mécanismes de régulation et la fonction des gènes de la réponse immunitaire de l'hôte pour perturber la symbiose et le contrôle des endosymbiotes chez les insectes nuisibles(2017)

Subjects
Models, Molecular, 0301 basic medicine, QH301-705.5, Mutant, Peptidoglycan, Article, Protein Structure, Secondary, Catalysis, Amidohydrolases, Amidase, Inorganic Chemistry, 03 medical and health sciences, chemistry.chemical_compound, Tracheal cytotoxin, Amidase activity, Animals, Protein Isoforms, peptidoglycan recognition protein, Amino Acid Sequence, Virulence Factors, Bordetella, Biology (General), Physical and Theoretical Chemistry, Site-directed mutagenesis, QD1-999, Drosophila melanogaster, Molecular Biology, innate immunity, Spectroscopy, X-ray crystallography, Innate immune system, 030102 biochemistry & molecular biology, Organic Chemistry, Pattern recognition receptor, General Medicine, Computer Science Applications, PGRP-LB, Zinc, Chemistry, 030104 developmental biology, chemistry, Biochemistry, Mutant Proteins, Carrier Proteins, Sugars, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Abstract

Peptidoglycan recognition proteins (PGRPs) are ubiquitous among animals and play pivotal functions in insect immunity. Non-catalytic PGRPs are involved in the activation of immune pathways by binding to the peptidoglycan (PGN), whereas amidase PGRPs are capable of cleaving the PGN into non-immunogenic compounds. Drosophila PGRP-LB belongs to the amidase PGRPs and downregulates the immune deficiency (IMD) pathway by cleaving meso-2,6-diaminopimelic (meso-DAP or DAP)-type PGN. While the recognition process is well analyzed for the non-catalytic PGRPs, little is known about the enzymatic mechanism for the amidase PGRPs, despite their essential function in immune homeostasis. Here, we analyzed the specific activity of different isoforms of Drosophila PGRP-LB towards various PGN substrates to understand their specificity and role in Drosophila immunity. We show that these isoforms have similar activity towards the different compounds. To analyze the mechanism of the amidase activity, we performed site directed mutagenesis and solved the X-ray structures of wild-type Drosophila PGRP-LB and its mutants, with one of these structures presenting a protein complexed with the tracheal cytotoxin (TCT), a muropeptide derived from the PGN. Only the Y78F mutation abolished the PGN cleavage while other mutations reduced the activity solely. Together, our findings suggest the dynamic role of the residue Y78 in the amidase mechanism by nucleophilic attack through a water molecule to the carbonyl group of the amide function destabilized by Zn2+.

Published
2021

32. The transposable element-rich genome of the cereal pest Sitophilus oryzae

Author

Sandrine Hughes, Abdelaziz Heddi, Alex Di Genova, Federica Calevro, Benjamin Gillet, Amparo Latorre, Hubert Charles, Ana Tereza Ribeiro de Vasconcelos, Cristina Vieira, Séverine Balmand, Marina Marcet-Houben, Matthieu Boulesteix, Stefano Colella, Jeb Rosen, Agnès Vallier, Jessica M. Storer, André Da Silva Barbosa, Carole Vincent-Monégat, Camille Meslin, Justin Maire, Mariana Galvão Ferrarini, Aurélien Vigneron, Arian F.A. Smit, Nicolas Parisot, Patrick Callaerts, Waël Zamoum, Rita Rebollo, Robert Hubley, Nicolas Montagné, Nelly Burlet, Caroline Blanc, Andrés Moya, Aymeric Bonnamour, Anna Zaidman-Rémy, Carlos Vargas-Chávez, Emmanuelle Jacquin-Joly, Clément Goubert, Florent Masson, Marie-France Sagot, Louis Beranger, Toni Gabaldón, Gérard Febvay, Théo Chancy, Alexandra L. Gerber, Patrice Baa-Puyoulet, Gautier Richard, and Elisa Dell’Aglio

Subjects
2. Zero hunger, Genetics, Transposable element, 0303 health sciences, Sodalis, food.ingredient, Endosymbiosis, business.industry, Sitophilus, Pest control, food and beverages, Biology, biology.organism_classification, Genome, 03 medical and health sciences, 0302 clinical medicine, Rice weevil, food, PEST analysis, business, 030217 neurology & neurosurgery, 030304 developmental biology
Abstract

BackgroundThe rice weevil Sitophilus oryzae is one of the most important agricultural pests, causing extensive damage to cereal in fields and to stored grains. S. oryzae has an intracellular symbiotic relationship (endosymbiosis) with the Gram-negative bacterium Sodalis pierantonius and is a valuable model to decipher host-symbiont molecular interactions.ResultsWe sequenced the Sitophilus oryzae genome using a combination of short and long reads to produce the best assembly for a Curculionidae species to date. We show that S. oryzae has undergone successive bursts of transposable element (TE) amplification, representing 72% of the genome. In addition, we show that many TE families are transcriptionally active, and changes in their expression are associated with insect endosymbiotic state. S. oryzae has undergone a high gene expansion rate, when compared to other beetles. Reconstruction of host-symbiont metabolic networks revealed that, despite its recent association with cereal weevils (30 Kyear), S. pierantonius relies on the host for several amino acids and nucleotides to survive and to produce vitamins and essential amino-acids required for insect development and cuticle biosynthesis.ConclusionsHere we present the genome of an agricultural pest beetle, which may act as a foundation for pest control. In addition, S. oryzae may be a useful model for endosymbiosis, and studying TE evolution and regulation, along with the impact of TEs on eukaryotic genomes.

Published
2021

33. Steroid hormone signaling is essential to regulate innate immune cells and fight bacterial infection in Drosophila.

Author

Jennifer C Regan, Ana S Brandão, Alexandre B Leitão, Angela Raquel Mantas Dias, Elio Sucena, António Jacinto, and Anna Zaidman-Rémy

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

Coupling immunity and development is essential to ensure survival despite changing internal conditions in the organism. Drosophila metamorphosis represents a striking example of drastic and systemic physiological changes that need to be integrated with the innate immune system. However, nothing is known about the mechanisms that coordinate development and immune cell activity in the transition from larva to adult. Here, we reveal that regulation of macrophage-like cells (hemocytes) by the steroid hormone ecdysone is essential for an effective innate immune response over metamorphosis. Although it is generally accepted that steroid hormones impact immunity in mammals, their action on monocytes (e.g. macrophages and neutrophils) is still not well understood. Here in a simpler model system, we used an approach that allows in vivo, cell autonomous analysis of hormonal regulation of innate immune cells, by combining genetic manipulation with flow cytometry, high-resolution time-lapse imaging and tissue-specific transcriptomic analysis. We show that in response to ecdysone, hemocytes rapidly upregulate actin dynamics, motility and phagocytosis of apoptotic corpses, and acquire the ability to chemotax to damaged epithelia. Most importantly, individuals lacking ecdysone-activated hemocytes are defective in bacterial phagocytosis and are fatally susceptible to infection by bacteria ingested at larval stages, despite the normal systemic and local production of antimicrobial peptides. This decrease in survival is comparable to the one observed in pupae lacking immune cells altogether, indicating that ecdysone-regulation is essential for hemocyte immune functions and survival after infection. Microarray analysis of hemocytes revealed a large set of genes regulated at metamorphosis by EcR signaling, among which many are known to function in cell motility, cell shape or phagocytosis. This study demonstrates an important role for steroid hormone regulation of immunity in vivo in Drosophila, and paves the way for genetic dissection of the mechanisms at work behind steroid regulation of innate immune cells.

Published
2013
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34. Functional analysis of PGRP-LA in Drosophila immunity.

Author

Mathilde Gendrin, Anna Zaidman-Rémy, Nichole A Broderick, Juan Paredes, Mickaël Poidevin, Alain Roussel, and Bruno Lemaitre

Subjects
Medicine, Science
Abstract

PeptidoGlycan Recognition Proteins (PGRPs) are key regulators of the insect innate antibacterial response. Even if they have been intensively studied, some of them have yet unknown functions. Here, we present a functional analysis of PGRP-LA, an as yet uncharacterized Drosophila PGRP. The PGRP-LA gene is located in cluster with PGRP-LC and PGRP-LF, which encode a receptor and a negative regulator of the Imd pathway, respectively. Structure predictions indicate that PGRP-LA would not bind to peptidoglycan, pointing to a regulatory role of this PGRP. PGRP-LA expression was enriched in barrier epithelia, but low in the fat body. Use of a newly generated PGRP-LA deficient mutant indicates that PGRP-LA is not required for the production of antimicrobial peptides by the fat body in response to a systemic infection. Focusing on the respiratory tract, where PGRP-LA is strongly expressed, we conducted a genome-wide microarray analysis of the tracheal immune response of wild-type, Relish, and PGRP-LA mutant larvae. Comparing our data to previous microarray studies, we report that a majority of genes regulated in the trachea upon infection differ from those induced in the gut or the fat body. Importantly, antimicrobial peptide gene expression was reduced in the tracheae of larvae and in the adult gut of PGRP-LA-deficient Drosophila upon oral bacterial infection. Together, our results suggest that PGRP-LA positively regulates the Imd pathway in barrier epithelia.

Published
2013
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35. Endosymbiosis morphological reorganization during metamorphosis diverges in weevils.

Author

Maire, J, Chouaia, B, Zaidman-Rémy, A, Heddi, A, Maire, J, Chouaia, B, Zaidman-Rémy, A, and Heddi, A

Abstract

Virtually all animals associate with beneficial symbiotic bacteria. Whether and how these associations are modulated across a host's lifecycle is an important question in disentangling animal-bacteria interactions. We recently reported a case of complete morphological reorganization of symbiosis during metamorphosis of the cereal weevil, Sitophilus oryzae. In this model, the bacteriome, a specialized organ that houses the intracellular bacterium Sodalis pierantonius, undergoes a two-phase remodeling program synchronously driven by host and endosymbiont, resulting in a localization shift and the formation of multiple new bacteriomes. Here, we provide comparative data in a closely-related coleopteran, the red palm weevil Rhynchophorus ferrugineus, which is associated with the ancestral endosymbiont Nardonella. Using cell imaging experiments, we show that the red pal weevil bacteriome remains unchanged during metamorphosis, hence contrasting with what we reported in the cereal weevil S. oryzae. These findings highlight the complexity and divergence of host-symbiont interactions and their intertwining with host development, even in closely-related species. Abbreviations: DAPI: 4',6-diamidino-2-phenylindole; FISH: Fluorescence in situ hybridization; T3SS: Type III secretion system.

Published
2020

36. Drosophila immunity: analysis of PGRP-SB1 expression, enzymatic activity and function.

Author

Anna Zaidman-Rémy, Mickael Poidevin, Mireille Hervé, David P Welchman, Juan C Paredes, Carina Fahlander, Hakan Steiner, Dominique Mengin-Lecreulx, and Bruno Lemaitre

Subjects
Medicine, Science
Abstract

Peptidoglycan is an essential and specific component of the bacterial cell wall and therefore is an ideal recognition signature for the immune system. Peptidoglycan recognition proteins (PGRPs) are conserved from insects to mammals and able to bind PGN (non-catalytic PGRPs) and, in some cases, to efficiently degrade it (catalytic PGRPs). In Drosophila, several non-catalytic PGRPs function as selective peptidoglycan receptors upstream of the Toll and Imd pathways, the two major signalling cascades regulating the systemic production of antimicrobial peptides. Recognition PGRPs specifically activate the Toll pathway in response to Lys-type peptidoglycan found in most Gram-positive bacteria and the Imd pathway in response to DAP-type peptidoglycan encountered in Gram-positive bacilli-type bacteria and in Gram-negative bacteria. Catalytic PGRPs on the other hand can potentially reduce the level of immune activation by scavenging peptidoglycan. In accordance with this, PGRP-LB and PGRP-SC1A/B/2 have been shown to act as negative regulators of the Imd pathway. In this study, we report a biochemical and genetic analysis of PGRP-SB1, a catalytic PGRP. Our data show that PGRP-SB1 is abundantly secreted into the hemolymph following Imd pathway activation in the fat body, and exhibits an enzymatic activity towards DAP-type polymeric peptidoglycan. We have generated a PGRP-SB1/2 null mutant by homologous recombination, but its thorough phenotypic analysis did not reveal any immune function, suggesting a subtle role or redundancy of PGRP-SB1/2 with other molecules. Possible immune functions of PGRP-SB1 are discussed.

Published
2011
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40. Weevil pgrp-lb prevents endosymbiont TCT dissemination and chronic host systemic immune activation

Author

Anna Zaidman-Rémy, Séverine Balmand, Mireille Hervé, Isabelle Rahioui, Florent Masson, Julien Orlans, Marie-Odile Fauvarque, Aurélien Vigneron, Nicolas Parisot, Pedro Da Silva, Justin Maire, Carole Vincent-Monégat, Caroline Anselme, Dominique Mengin-Lecreulx, Abdelaziz Heddi, Jackie Perrin, Agnès Vallier, Biologie Fonctionnelle, Insectes et Interactions (BF2I), Institut National de la Recherche Agronomique (INRA)-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA), Institut de Biologie Intégrative de la Cellule (I2BC), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Institut National de la Recherche Agronomique, Institut National des Sciences Appliquees-Lyon, French (IMetSym) [ANR-13-BSV7-0016-01], French (GREEN) [ANR-17-CE20-0031-01], La Region Rhone-Alpes, ANR-17-CE20-0031,GREEN,Comprendre les mécanismes de régulation et la fonction des gènes de la réponse immunitaire de l'hôte pour perturber la symbiose et le contrôle des endosymbiotes chez les insectes nuisibles(2017), Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), and Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)-Université Paris-Saclay

Subjects
[SDV.IMM.II]Life Sciences [q-bio]/Immunology/Innate immunity, chemistry.chemical_compound, nod1, RNA interference, Tracheal cytotoxin, Protein Isoforms, bacteria, sitophilus-oryzae, innate immunity, 0303 health sciences, Multidisciplinary, Endosymbiosis, Cytotoxins, Biological Sciences, drosophila, mitochondrial, symbiosis, Cell biology, PNAS Plus, Larva, coevolution, Insect Proteins, Evolution, Context (language use), PGRP, Peptidoglycan, Biology, 03 medical and health sciences, Immune system, Animals, 030304 developmental biology, Innate immune system, endosymbiosis, Host Microbial Interactions, 030306 microbiology, fungi, Bacteriome, mutualist wigglesworthia, biochemical phenomena, metabolism, and nutrition, peptidoglycan recognition proteins, infection, [SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology, chemistry, neisseria-gonorrhoeae, Weevils, insect, Carrier Proteins, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Abstract

Significance Permanent infections with beneficial bacteria are widespread in nature and are believed to play a pivotal role in evolution. How hosts’ immune functions are regulated to maintain cooperative bacteria while preventing them from constantly activating the host immune system is a key question in understanding host–bacterial associations’ sustainability. In insects, beneficial bacteria are often confined within specialized host cells, the bacteriocytes, which avoid direct contact between the host’s immune system and bacteria. Here, we report an additional mechanism that prevents bacteria-released immunogenic molecules (i.e., peptidoglycan fragments) from escaping the bacteriocytes. We show that two peptidoglycan-cleaving enzymes are specifically produced in the bacteriocytes, where they cleave bacterial peptidoglycan into nonimmunogenic fragments, thereby preventing continuous and damageable host systemic immune activation., Long-term intracellular symbiosis (or endosymbiosis) is widely distributed across invertebrates and is recognized as a major driving force in evolution. However, the maintenance of immune homeostasis in organisms chronically infected with mutualistic bacteria is a challenging task, and little is known about the molecular processes that limit endosymbiont immunogenicity and host inflammation. Here, we investigated peptidoglycan recognition protein (PGRP)-encoding genes in the cereal weevil Sitophilus zeamais’s association with Sodalis pierantonius endosymbiont. We discovered that weevil pgrp-lb generates three transcripts via alternative splicing and differential regulation. A secreted isoform is expressed in insect tissues under pathogenic conditions through activation of the PGRP-LC receptor of the immune deficiency pathway. In addition, cytosolic and transmembrane isoforms are permanently produced within endosymbiont-bearing organ, the bacteriome, in a PGRP-LC–independent manner. Bacteriome isoforms specifically cleave the tracheal cytotoxin (TCT), a peptidoglycan monomer released by endosymbionts. pgrp-lb silencing by RNAi results in TCT escape from the bacteriome to other insect tissues, where it chronically activates the host systemic immunity through PGRP-LC. While such immune deregulations did not impact endosymbiont load, they did negatively affect host physiology, as attested by a diminished sexual maturation of adult weevils. Whereas pgrp-lb was first described in pathogenic interactions, this work shows that, in an endosymbiosis context, specific bacteriome isoforms have evolved, allowing endosymbiont TCT scavenging and preventing chronic endosymbiont-induced immune responses, thus promoting host homeostasis.

Published
2019

41. What can a weevil teach a fly, and reciprocally? Interaction of host immune systems with endosymbionts in Glossina and Sitophilus

Author

Brian L. Weiss, Abdelaziz Heddi, Anna Zaidman-Rémy, Aurélien Vigneron, Biologie Fonctionnelle, Insectes et Interactions (BF2I), Institut National de la Recherche Agronomique (INRA)-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA), French ANR-13-BSV7–0016-01 (IMetSym), NIH/NIAID (AI051584), Ambrose Monell Foundation, International Atomic Energy Agency (IAEA), Zaidman-Remy, Anna, and Heddi, Abdelaziz

Subjects
0301 basic medicine, Biodiversité et Ecologie, [SDV]Life Sciences [q-bio], lcsh:QR1-502, Review, Wigglesworthia glossinidia, Cereal weevil, lcsh:Microbiology, Homeostasis, 2. Zero hunger, Tsetse fly, endosymbiosis, immunity, evolution, insects, homeostasis, biology, Sitophilus, Sodalis glossinidius, food and beverages, Biological Evolution, Insects, espèce modèle, Wolbachia, symbiose, Microbiology (medical), Sodalis, food.ingredient, Tsetse Flies, Evolution, 030106 microbiology, Zoology, Microbiology, Biodiversity and Ecology, 03 medical and health sciences, food, Enterobacteriaceae, Animals, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, Symbiosis, Wigglesworthia, Host Microbial Interactions, Obligate, Endosymbiosis, Host (biology), fungi, Immunity, mouche tsé tsé, 15. Life on land, biochemical phenomena, metabolism, and nutrition, biology.organism_classification, 030104 developmental biology, Weevils, bacteria, Pest Control, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Abstract

International audience; The tsetse fly (Glossina genus) is the main vector of African trypanosomes, which are protozoan parasites that cause human and animal African trypanosomiases in Sub-Saharan Africa. In the frame of the IAEA/FAO program 'Enhancing Vector Refractoriness to Trypanosome Infection', in addition to the tsetse, the cereal weevil Sitophilus has been introduced as a comparative system with regards to immune interactions with endosymbionts. The cereal weevil is an agricultural pest that destroys a significant proportion of cereal stocks worldwide. Tsetse flies are associated with three symbiotic bacteria, the multifunctional obligate Wigglesworthia glossinidia, the facultative commensal Sodalis glossinidius and the parasitic Wolbachia. Cereal weevils house an obligatory nutritional symbiosis with the bacterium Sodalis pierantonius, and occasionally Wolbachia. Studying insect host-symbiont interactions is highly relevant both for understanding the evolution of symbiosis and for envisioning novel pest control strategies. In both insects, the long co-evolution between host and endosymbiont has led to a stringent integration of the host-bacteria partnership. These associations were facilitated by the development of specialized host traits, including symbiont-housing cells called bacteriocytes and specific immune features that enable both tolerance and control of the bacteria. In this review, we compare the tsetse and weevil model systems and compile the latest research findings regarding their biological and ecological similarities, how the immune system controls endosymbiont load and location, and how host-symbiont interactions impact developmental features including cuticle synthesis and immune system maturation. We focus mainly on the interactions between the obligate symbionts and their host's immune systems, a central theme in both model systems. Finally, we highlight how parallel studies on cereal weevils and tsetse flies led to mutual discoveries and stimulated research on each model, creating a pivotal example of scientific improvement through comparison between relatively distant models.

Published
2018

43. An IMD-like pathway mediates both endosymbiont control and host immunity in the cereal weevil Sitophilus spp

Author

Carole Vincent-Monégat, Anna Zaidman-Rémy, Justin Maire, Abdelaziz Heddi, Florent Masson, Biologie Fonctionnelle, Insectes et Interactions (BF2I), Institut National de la Recherche Agronomique (INRA)-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA), Ecole Polytechnique Fédérale de Lausanne (EPFL), ANR-13-BSV7-0016,IMetSym,Contrôles immunitaire et métabolique dans les symbioses intracellulaires d'insectes(2013), INRA, INSA-Lyon, French (IMetSym) [ANR-13-BSV7-0016-01], and French Ministry of Higher Education and Research

Subjects
0301 basic medicine, Innate immunity, Compartmentalization, endosymbiosis, bacteriocyte, antimicrobial peptide, sitophilus, Genetics, Endosymbiosis, Cytotoxins, Sitophilus, Microbiology and Parasitology, Microbiologie et Parasitologie, Host-Pathogen Interactions, Insect Proteins, [SDV.IMM]Life Sciences [q-bio]/Immunology, lcsh:QR100-130, Antimicrobial peptide, Microbiology (medical), Sodalis, food.ingredient, charancon, Short Report, Biology, Microbiology, Host Specificity, lcsh:Microbial ecology, 03 medical and health sciences, Immune system, food, Bacterial Proteins, Enterobacteriaceae, endosymbiote, Bacteriocyte, Animals, Symbiosis, Innate immune system, Intracellular parasite, fungi, endosymbiose, Bacteriome, biochemical phenomena, metabolism, and nutrition, biology.organism_classification, Immunity, Innate, [SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology, 030104 developmental biology, Gene Expression Regulation, Weevils, bacteria, Edible Grain, Antimicrobial Cationic Peptides, Transcription Factors, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Abstract

Many insects developing on nutritionally unbalanced diets have evolved symbiotic associations with vertically transmitted intracellular bacteria (endosymbionts) that provide them with metabolic components, thereby improving the host’s abilities to thrive on such poor ecological niches. While host-endosymbiont coevolutionary constraints are known to entail massive genomic changes in the microbial partner, host’s genomic evolution remains elusive, particularly with regard to the immune system. In the cereal weevil Sitophilus spp., which houses Sodalis pierantonius, endosymbionts are secluded in specialized host cells, the bacteriocytes that group together as an organ, the bacteriome. We previously reported that at standard conditions, the bacteriome highly expresses the coleoptericin A (colA) antimicrobial peptide (AMP), which was shown to prevent endosymbiont escape from the bacteriocytes. However, following the insect systemic infection by pathogens, the bacteriome upregulates a cocktail of AMP encoding genes, including colA. The regulations that allow these contrasted immune responses remain unknown. In this short report, we provide evidence that an IMD-like pathway is conserved in two sibling species of cereal weevils, Sitophilus oryzae and Sitophilus zeamais. RNA interference (RNAi) experiments showed that imd and relish genes are essential for (i) colA expression in the bacteriome under standard conditions, (ii) AMP up-regulation in the bacteriome following a systemic immune challenge, and (iii) AMP systemic induction following an immune challenge. Histological analyses also showed that relish inhibition by RNAi resulted in endosymbiont escape from the bacteriome, strengthening the involvement of an IMD-like pathway in endosymbiont control. We conclude that Sitophilus’ IMD-like pathway mediates both the bacteriome immune program involved in endosymbiont seclusion within the bacteriocytes and the systemic and local immune responses to exogenous challenges. This work provides a striking example of how a conserved immune pathway, initially described as essential in pathogen clearance, also functions in the control of mutualistic associations. Electronic supplementary material The online version of this article (10.1186/s40168-017-0397-9) contains supplementary material, which is available to authorized users.

Published
2018

44. Evaluating the essentiality of the primary endosymbiont of the rice weevil Sitophilus oryzae through genome analysis

Author

Vargas-Chavez, Carlos, Parisot, Nicolas, Goubert, C., Baa-Puyoulet, Patrice, Balmand, Severine, Boulesteix, M., Burlet, Nelly, Callaerts, Patrick, Charles, Hubert, Colella, Stefano, Febvay, Gérard, Gabaldon, Toni, Jacquin-Joly, Emmanuelle, Loska, Damian, Maire, Justin, MASSON, Florent, Meslin, Camille, montagné, N, Moya, Andres, Vincent-Monégat, Carole, Rebollo, Rita, Vallier, Agnès, Vigneron, Aurélien, Zaidman-Rémy, A., Calevro, Federica, Vieira, Cristina, Latorre, Amparo, Heddi, Abdelaziz, Charles, Hubert, Biologie Fonctionnelle, Insectes et Interactions (BF2I), Institut National de la Recherche Agronomique (INRA)-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA), Eléments transposables, évolution, populations, 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), Catholic University of Leuven - Katholieke Universiteit Leuven (KU Leuven), Laboratoire des symbioses tropicales et méditerranéennes (UMR LSTM), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Université Montpellier 1 (UM1)-Institut de Recherche pour le Développement (IRD)-Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Unité de recherche Productions végétales (CRAG ANT PROD V), Institut National de la Recherche Agronomique (INRA), Barcelona Supercomputing Center - Centro Nacional de Supercomputacion (BSC - CNS), Institut d'écologie et des sciences de l'environnement de Paris (iEES), Institut National de la Recherche Agronomique (INRA)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12)-Centre National de la Recherche Scientifique (CNRS), Barcelona Institute of Science and Technology (BIST), Department ofComputationaland Systems Biology, University of Pittsburgh (PITT), Pennsylvania Commonwealth System of Higher Education (PCSHE)-Pennsylvania Commonwealth System of Higher Education (PCSHE), Institut Cavanilles de Biodiversitat i Biologia Evolutiva (ICBiBE), Universitat de València (UV), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Institut d'Ecologie et des Sciences de l'Environnement de Paris, Institut National de la Recherche Agronomique (INRA)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut de Recherche pour le Développement (IRD [France-Ouest])-Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12)-Centre National de la Recherche Scientifique (CNRS)-Ecole Normale Supérieure Paris-Saclay (ENS Paris Saclay), Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut de Recherche pour le Développement (IRD)-Université de Montpellier (UM)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), and Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)

Subjects
[SDV.BIBS] Life Sciences [q-bio]/Quantitative Methods [q-bio.QM], fungi, bacteria, food and beverages, biochemical phenomena, metabolism, and nutrition, [SDV.BIBS]Life Sciences [q-bio]/Quantitative Methods [q-bio.QM], Sitophilus oryzae L, symbiosis
Abstract

International audience; The rice weevil Sitophilus oryzae is a pest insect responsible for great economic losses to the agriculture, particularly in developing countries where the damage can exceed 40% of the cereal production. This pest harbors an endosymbiont, “Candidatus Sodalis pierantonius” (cited Sodalis hereafter) that improves its fitness and invasive power. It has been demonstrated that Sodalis recently replaced the ancestral endosymbiont “Candidatus Nardonella” (cited Nardonella hereafter), which is still conserved in other members of the Dryophthoridae family. This recent acquisition raises several challenges for the host, given that the genome of Sodalis has not experienced a drastic genome size shrinkage when compared to other old-lasting insect’s endosymbionts. While the genomes of Sodalis and several strains of Nardonella are available, the insect’s genome is still needed to perform a full study of the system. To this end, we have sequenced and assembled the full genome of the weevil S. oryzae using a combination of Next Generation Sequencing data. Additionally, we have compared this genome with other available insect genomes. We found that the genome of S. oryzae encodes immune elements similar to those of other holometabolous insects, including those living without endosymbionts. Remarkably, an impressive amount of repeated elements was identified, similar to what was previously described in the Sodalis endosymbiont, suggesting the occurrence of gene rearrangement processes at this early phase of symbiogenesis. We concluded that while Sodalis is completely dependent on its host, the insect can survive without its endosymbiont.

Published
2018

45. Exploring host-symbiont interactions through whole genome sequencing of the rice weevil Sitophilus oryzae

Author

Carlos Vargas-Chavez, Nicolas Parisot, Clément Goubert, Patrice Baa-Puyoulet, Severine Balmand, Boulesteix, M., Nelly Burlet, Callaerts, A., Hubert CHARLES, Stefano Colella, Gérard Febvay, Toni Gabaldon, Emmanuelle Jacquin-Joly, Damian Loska, Justin Maire, Florent Masson, Camille Meslin, Nicolas Montagne, Andres Moya, Carole Vincent-Monégat, Rita Rebollo, Agnès Vallier, Aurélien Vigneron, Zaidman-Rémy, A., Federica Calevro, Cristina Vieira, Amparo Latorre, Abdelaziz Heddi, Biologie Fonctionnelle, Insectes et Interactions (BF2I), Institut National de la Recherche Agronomique (INRA)-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA), Eléments transposables, évolution, populations, 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), Unité de recherche Productions végétales (CRAG ANT PROD V), Institut National de la Recherche Agronomique (INRA), Barcelona Supercomputing Center - Centro Nacional de Supercomputacion (BSC - CNS), Institut d'écologie et des sciences de l'environnement de Paris (iEES Paris), Institut National de la Recherche Agronomique (INRA)-Sorbonne Université (SU)-Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12)-Centre National de la Recherche Scientifique (CNRS), Barcelona Institute of Science and Technology (BIST), Department ofComputationaland Systems Biology, University of Pittsburgh (PITT), Pennsylvania Commonwealth System of Higher Education (PCSHE)-Pennsylvania Commonwealth System of Higher Education (PCSHE), Institut Cavanilles de Biodiversitat i Biologia Evolutiva (ICBiBE), and Universitat de València (UV)

Subjects
Sitophilus oryzae, genome, [SDV.BIBS]Life Sciences [q-bio]/Quantitative Methods [q-bio.QM], ComputingMilieux_MISCELLANEOUS
Abstract

International audience

Published
2017

46. Endosymbiosis as a source of immune innovation

Author

Anna Zaidman-Rémy, Abdelaziz Heddi, Biologie Fonctionnelle, Insectes et Interactions (BF2I), Institut National de la Recherche Agronomique (INRA)-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA), INRA, INSA Lyon, ANR-10 BSV7-170101-545 03, ANR-13-BSV7-0016-01, ANR-10-BLAN-1701,ImmunSymbArt,Immunité et Symbiose chez les Arthropodes(2010), ANR-13-BSV7-0016,IMetSym,Contrôles immunitaire et métabolique dans les symbioses intracellulaires d'insectes(2013), and Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon

Subjects
0301 basic medicine, Insecta, General Immunology and Microbiology, Endosymbiosis, [SDV]Life Sciences [q-bio], 030106 microbiology, Context (language use), General Medicine, Biological evolution, Biology, Biological Evolution, immunity, General Biochemistry, Genetics and Molecular Biology, symbiosis, 03 medical and health sciences, 030104 developmental biology, Symbiosis, Evolutionary biology, evolution, [SDE]Environmental Sciences, Animals, General Agricultural and Biological Sciences, Coevolution, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Abstract

National audience; Some years ago, Lynn Margulis proposed to envision symbiosis as a source of evolutionary innovation. Here we revisit this concept in the context of insect nutritional endosymbiosis, and discuss recent data suggesting that host-endosymbiont coevolution has led to the selection of innovative strategies towards endosymbiont maintenance and control by the host immune system. (C) 2018 Published by Elsevier Masson SAS on behalf of Academie des sciences.

Published
2017

47. Effects of symbiotic status on cellular immunity dynamics in Sitophilus oryzae

Author

Séverine Balmand, Abdelaziz Heddi, Sergio López-Madrigal, Justin Maire, Anna Zaidman-Rémy, Biologie Fonctionnelle, Insectes et Interactions (BF2I), Institut National de la Recherche Agronomique (INRA)-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA), INRA Département Santé des Plantes et Environnement, INSA de Lyon [Grant number BQR2015], and ANR [ANR-13- BSV7-0016-01] (IMetSym)

Subjects
0301 basic medicine, Cellular immunity, immunité cellulaire, Sodalis, food.ingredient, lymphocyte proliferation blastogenesis (lymphocytes), [SDV]Life Sciences [q-bio], 030106 microbiology, Immunology, Zoology, cellular immunity, Biology, 03 medical and health sciences, food, Immune system, Enterobacteriaceae, Symbiosis, Animals, innate immunity, Mutualism (biology), Immunity, Cellular, Innate immune system, endosymbiosis, Ecology, charancon du riz, Sitophilus, fungi, Enterobacteriaceae Infections, Gene Expression Regulation, Developmental, food and beverages, endosymbiose, biology.organism_classification, immunité innée, Immunity, Humoral, hemocytes, rice weevil, 030104 developmental biology, haemocytes, Larva, Weevils, Developmental Biology, Symbiotic bacteria
Abstract

Many insects maintain intracellular symbiosis with mutualistic bacteria that improve their adaptive capabilities in nutritionally poor habitats. Adaptation of insect immune systems to such associations has been shown in several symbiotic consortia, including that of the rice weevil Sitophilus oryzae with the gammaproteobacterium Sodalis pierantonius. Although authors have mostly focused on the role of humoral immunity in host-symbiont interactions, recent studies suggest that symbiotic bacteria may also interfere with the cellular, hemocyte-based, immunity. Here, we have explored hemocyte dynamics in S. oryzae in the presence or absence of S. pierantonius, and in response to bacterial challenges. We have identified five morphotypes within larval hemocytes, whose abundance and morphometry drastically change along insect development. We show that hemocytes make part of the weevil immune system by responding to pathogenic infections. In contrast with previous results on other insect species, however, our analyses did not reveal any symbiotic-dependent modulation of the hemocyte global population.

Published
2017

50. Antimicrobial peptides and cell processes tracking endosymbiont dynamics

Author

Abdelaziz Heddi, Anna Zaidman-Rémy, Florent Masson, Biologie Fonctionnelle, Insectes et Interactions (BF2I), Institut National de la Recherche Agronomique (INRA)-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA), ANR (ImmunSymbArt) [ANR-10 BSV7-170101-545 03], ANR (IMetSym) [ANR-13-BSV7-0016-01], and French Ministry of Higher Education and Research

Subjects
0301 basic medicine, antimicrobial peptide, Cell, Antimicrobial peptides, Coleoptericin, Apoptosis, bacteriocyte, Biology, Bacterial Physiological Phenomena, General Biochemistry, Genetics and Molecular Biology, 03 medical and health sciences, Botany, [SDV.BA.ZV]Life Sciences [q-bio]/Animal biology/Vertebrate Zoology, medicine, Autophagy, Animals, Symbiosis, 2. Zero hunger, endosymbiosis, Endosymbiosis, Bacteriocyte, fungi, Articles, biochemical phenomena, metabolism, and nutrition, Cell biology, Sitophilus, 030104 developmental biology, medicine.anatomical_structure, bacteria, Insect Proteins, Weevils, General Agricultural and Biological Sciences, Intracellular, Symbiotic bacteria, Antimicrobial Cationic Peptides
Abstract

Many insects sustain long-term relationships with intracellular symbiotic bacteria that provide them with essential nutrients. Such endosymbiotic relationships likely emerged from ancestral infections of the host by free-living bacteria, the genomes of which experience drastic gene losses and rearrangements during the host–symbiont coevolution. While it is well documented that endosymbiont genome shrinkage results in the loss of bacterial virulence genes, whether and how the host immune system evolves towards the tolerance and control of bacterial partners remains elusive. Remarkably, many insects rely on a ‘compartmentalization strategy’ that consists in secluding endosymbionts within specialized host cells, the bacteriocytes, thus preventing direct symbiont contact with the host systemic immune system. In this review, we compile recent advances in the understanding of the bacteriocyte immune and cellular regulators involved in endosymbiont maintenance and control. We focus on the cereal weevils Sitophilus spp., in which bacteriocytes form bacteriome organs that strikingly evolve in structure and number according to insect development and physiological needs. We discuss how weevils track endosymbiont dynamics through at least two mechanisms: (i) a bacteriome local antimicrobial peptide synthesis that regulates endosymbiont cell cytokinesis and helps to maintain a homeostatic state within bacteriocytes and (ii) some cellular processes such as apoptosis and autophagy which adjust endosymbiont load to the host developmental requirements, hence ensuring a fine-tuned integration of symbiosis costs and benefits. This article is part of the themed issue ‘Evolutionary ecology of arthropod antimicrobial peptides’.

Published
2016

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