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1. MatP local enrichment delays segregation independently of tetramer formation and septal anchoring in Vibrio cholerae

Author: Elena Espinosa, Jihane Challita, Jean-Michel Desfontaines, Christophe Possoz, Marie-Eve Val, Didier Mazel, Martial Marbouty, Romain Koszul, Elisa Galli, and François-Xavier Barre
Subjects: Science
Abstract: Abstract Vibrio cholerae harbours a primary chromosome derived from the monochromosomal ancestor of the Vibrionales (ChrI) and a secondary chromosome derived from a megaplasmid (ChrII). The coordinated segregation of the replication terminus of both chromosomes (TerI and TerII) determines when and where cell division occurs. ChrI encodes a homologue of Escherichia coli MatP, a protein that binds to a DNA motif (matS) that is overrepresented in replication termini. Here, we use a combination of deep sequencing and fluorescence microscopy techniques to show that V. cholerae MatP structures TerI and TerII into macrodomains, targets them to mid-cell during replication, and delays their segregation, thus supporting that ChrII behaves as a bona fide chromosome. We further show that the extent of the segregation delay mediated by MatP depends on the number and local density of matS sites, and is independent of its assembly into tetramers and any interaction with the divisome, in contrast to what has been previously observed in E. coli.
Published: 2024
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2. Insights into early animal evolution from the genome of the xenacoelomorph worm Xenoturbella bocki

Author: Philipp H Schiffer, Paschalis Natsidis, Daniel J Leite, Helen E Robertson, François Lapraz, Ferdinand Marlétaz, Bastian Fromm, Liam Baudry, Fraser Simpson, Eirik Høye, Anne C Zakrzewski, Paschalia Kapli, Katharina J Hoff, Steven Müller, Martial Marbouty, Heather Marlow, Richard R Copley, Romain Koszul, Peter Sarkies, and Maximilian J Telford
Subjects: Xenoturbella, Deuterostomia, animal evolution, Xenacoelomorpha, genome analysis, Medicine, Science, Biology (General), QH301-705.5
Abstract: The evolutionary origins of Bilateria remain enigmatic. One of the more enduring proposals highlights similarities between a cnidarian-like planula larva and simple acoel-like flatworms. This idea is based in part on the view of the Xenacoelomorpha as an outgroup to all other bilaterians which are themselves designated the Nephrozoa (protostomes and deuterostomes). Genome data can provide important comparative data and help understand the evolution and biology of enigmatic species better. Here, we assemble and analyze the genome of the simple, marine xenacoelomorph Xenoturbella bocki, a key species for our understanding of early bilaterian evolution. Our highly contiguous genome assembly of X. bocki has a size of ~111 Mbp in 18 chromosome-like scaffolds, with repeat content and intron, exon, and intergenic space comparable to other bilaterian invertebrates. We find X. bocki to have a similar number of genes to other bilaterians and to have retained ancestral metazoan synteny. Key bilaterian signaling pathways are also largely complete and most bilaterian miRNAs are present. Overall, we conclude that X. bocki has a complex genome typical of bilaterians, which does not reflect the apparent simplicity of its body plan that has been so important to proposals that the Xenacoelomorpha are the simple sister group of the rest of the Bilateria.
Published: 2024
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3. Phage-inducible chromosomal minimalist islands (PICMIs), a novel family of small marine satellites of virulent phages

Author: Rubén Barcia-Cruz, David Goudenège, Jorge A. Moura de Sousa, Damien Piel, Martial Marbouty, Eduardo P. C. Rocha, and Frédérique Le Roux
Subjects: Science
Abstract: Abstract Phage satellites are bacterial genetic elements that co-opt phage machinery for their own dissemination. Here we identify a family of satellites, named Phage-Inducible Chromosomal Minimalist Islands (PICMIs), that are broadly distributed in marine bacteria of the family Vibrionaceae. A typical PICMI is characterized by reduced gene content, does not encode genes for capsid remodelling, and packages its DNA as a concatemer. PICMIs integrate in the bacterial host genome next to the fis regulator, and encode three core proteins necessary for excision and replication. PICMIs are dependent on virulent phage particles to spread to other bacteria, and protect their hosts from other competitive phages without interfering with their helper phage. Thus, our work broadens our understanding of phage satellites and narrows down the minimal number of functions necessary to hijack a tailed phage.
Published: 2024
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4. Chromosome folding and prophage activation reveal specific genomic architecture for intestinal bacteria

Author: Quentin Lamy-Besnier, Amaury Bignaud, Julian R. Garneau, Marie Titecat, Devon E. Conti, Alexandra Von Strempel, Marc Monot, Bärbel Stecher, Romain Koszul, Laurent Debarbieux, and Martial Marbouty
Subjects: Phages, Gut, HiC, Virome, OMM12, 3D signatures, Microbial ecology, QR100-130
Abstract: Abstract Background Bacteria and their viruses, bacteriophages, are the most abundant entities of the gut microbiota, a complex community of microorganisms associated with human health and disease. In this ecosystem, the interactions between these two key components are still largely unknown. In particular, the impact of the gut environment on bacteria and their associated prophages is yet to be deciphered. Results To gain insight into the activity of lysogenic bacteriophages within the context of their host genomes, we performed proximity ligation-based sequencing (Hi-C) in both in vitro and in vivo conditions on the 12 bacterial strains of the OMM12 synthetic bacterial community stably associated within mice gut (gnotobiotic mouse line OMM12). High-resolution contact maps of the chromosome 3D organization of the bacterial genomes revealed a wide diversity of architectures, differences between environments, and an overall stability over time in the gut of mice. The DNA contacts pointed at 3D signatures of prophages leading to 16 of them being predicted as functional. We also identified circularization signals and observed different 3D patterns between in vitro and in vivo conditions. Concurrent virome analysis showed that 11 of these prophages produced viral particles and that OMM12 mice do not carry other intestinal viruses. Conclusions The precise identification by Hi-C of functional and active prophages within bacterial communities will unlock the study of interactions between bacteriophages and bacteria across conditions (healthy vs disease). Video Abstract
Published: 2023
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5. Chromosomal assembly of the flat oyster (Ostrea edulis L.) genome as a new genetic resource for aquaculture

Author: Isabelle Boutet, Homère J. Alves Monteiro, Lyam Baudry, Takeshi Takeuchi, Eric Bonnivard, Bernard Billoud, Sarah Farhat, Ricardo Gonzales‐Araya, Benoit Salaun, Ann C. Andersen, Jean‐Yves Toullec, François H. Lallier, Jean‐François Flot, Nadège Guiglielmoni, Ximing Guo, Cui Li, Bassem Allam, Emmanuelle Pales‐Espinosa, Jakob Hemmer‐Hansen, Pierrick Moreau, Martial Marbouty, Romain Koszul, and Arnaud Tanguy
Subjects: aquaculture, flat oyster, genome, Martelia, transposable elements, Evolution, QH359-425
Abstract: Abstract The European flat oyster (Ostrea edulis L.) is a native bivalve of the European coasts. Harvest of this species has declined during the last decades because of the appearance of two parasites that have led to the collapse of the stocks and the loss of the natural oyster beds. O. edulis has been the subject of numerous studies in population genetics and on the detection of the parasites Bonamia ostreae and Marteilia refringens. These studies investigated immune responses to these parasites at the molecular and cellular levels. Several genetic improvement programs have been initiated especially for parasite resistance. Within the framework of a European project (PERLE 2) that aims to produce genetic lines of O. edulis with hardiness traits (growth, survival, resistance) for the purpose of repopulating natural oyster beds in Brittany and reviving the culture of this species in the foreshore, obtaining a reference genome becomes essential as done recently in many bivalve species of aquaculture interest. Here, we present a chromosome‐level genome assembly and annotation for the European flat oyster, generated by combining PacBio, Illumina, 10X linked, and Hi‐C sequencing. The finished assembly is 887.2 Mb with a scaffold‐N50 of 97.1 Mb scaffolded on the expected 10 pseudochromosomes. Annotation of the genome revealed the presence of 35,962 protein‐coding genes. We analyzed in detail the transposable element (TE) diversity in the flat oyster genome, highlighted some specificities in tRNA and miRNA composition, and provided the first insight into the molecular response of O. edulis to M. refringens. This genome provides a reference for genomic studies on O. edulis to better understand its basic physiology and as a useful resource for genetic breeding in support of aquaculture and natural reef restoration.
Published: 2022
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6. Bacterial Membrane Vesicles as a Novel Strategy for Extrusion of Antimicrobial Bismuth Drug in Helicobacter pylori

Author: Sumith Kumar, Christine Schmitt, Olivier Gorgette, Martial Marbouty, Magalie Duchateau, Quentin Giai Gianetto, Mariette Matondo, Jean-Michel Guigner, and Hilde De Reuse
Subjects: Helicobacter pylori, bismuth, membrane vesicles, antibiotic resistance, polyphosphate granules, chromosome conformation capture, Microbiology, QR1-502
Abstract: ABSTRACT Bacterial antibiotic resistance is a major threat to human health. A combination of antibiotics with metals is among the proposed alternative treatments. Only one such combination is successfully used in clinics; it associates antibiotics with the metal bismuth to treat infections by Helicobacter pylori. This bacterial pathogen colonizes the human stomach and is associated with gastric cancer, killing 800,000 individuals yearly. The effect of bismuth in H. pylori treatment is not well understood in particular for sublethal doses such as those measured in the plasma of treated patients. We addressed this question and observed that bismuth induces the formation of homogeneously sized membrane vesicles (MVs) with unique protein cargo content enriched in bismuth-binding proteins, as shown by quantitative proteomics. Purified MVs of bismuth-exposed bacteria were strongly enriched in bismuth as measured by inductively coupled plasma optical emission spectrometry (ICP-OES), unlike bacterial cells from which they originate. Thus, our results revealed a novel function of MVs in bismuth detoxification, where secreted MVs act as tool to discard bismuth from the bacteria. Bismuth also induces the formation of intracellular polyphosphate granules that are associated with changes in nucleoid structure. Nucleoid compaction in response to bismuth was established by immunogold electron microscopy and refined by the first chromosome conformation capture (Hi-C) analysis of H. pylori. Our results reveal that even low doses of bismuth induce profound changes in H. pylori physiology and highlight a novel defense mechanism that involves MV-mediated bismuth extrusion from the bacteria and a probable local DNA protective response where polyphosphate granules are associated with nucleoid compaction. IMPORTANCE Bacterial resistance to antibiotics is a major threat to human health. Treatments combining antibiotics with metals were proposed to circumvent this hurdle. Only one such combination is successfully used in clinics associating antibiotics with the metal bismuth to treat infections by the human pathogen Helicobacter pylori. H. pylori causes 800,000 deaths by gastric cancer yearly. How bismuth impacts H. pylori and its response to this toxic metal were ill defined. We discovered that upon bismuth exposure, H. pylori secretes membrane vesicles that are enriched in bismuth. Bismuth also induces the formation of intracellular polyphosphate granules associated with compaction of the chromosome. Upon bismuth exposure, H. pylori displays both defense and protection mechanisms, with bismuth extrusion by vesicles and shielding of the chromosome.
Published: 2022
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7. High-throughput identification of viral termini and packaging mechanisms in virome datasets using PhageTermVirome

Author: Julian R. Garneau, Véronique Legrand, Martial Marbouty, Maximilian O. Press, Dean R. Vik, Louis-Charles Fortier, Matthew B. Sullivan, David Bikard, and Marc Monot
Subjects: Medicine, Science
Abstract: Abstract Viruses that infect bacteria (phages) are increasingly recognized for their importance in diverse ecosystems but identifying and annotating them in large-scale sequence datasets is still challenging. Although efficient scalable virus identification tools are emerging, defining the exact ends (termini) of phage genomes is still particularly difficult. The proper identification of termini is crucial, as it helps in characterizing the packaging mechanism of bacteriophages and provides information on various aspects of phage biology. Here, we introduce PhageTermVirome (PTV) as a tool for the easy and rapid high-throughput determination of phage termini and packaging mechanisms using modern large-scale metagenomics datasets. We successfully tested the PTV algorithm on a mock virome dataset and then used it on two real virome datasets to achieve the rapid identification of more than 100 phage termini and packaging mechanisms, with just a few hours of computing time. Because PTV allows the identification of free fully formed viral particles (by recognition of termini present only in encapsidated DNA), it can also complement other virus identification softwares to predict the true viral origin of contigs in viral metagenomics datasets. PTV is a novel and unique tool for high-throughput characterization of phage genomes, including phage termini identification and characterization of genome packaging mechanisms. This software should help researchers better visualize, map and study the virosphere. PTV is freely available for downloading and installation at https://gitlab.pasteur.fr/vlegrand/ptv .
Published: 2021
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8. Chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization

Author: Jérémy Gauthier, Hélène Boulain, Joke J. F. A. van Vugt, Lyam Baudry, Emma Persyn, Jean-Marc Aury, Benjamin Noel, Anthony Bretaudeau, Fabrice Legeai, Sven Warris, Mohamed A. Chebbi, Géraldine Dubreuil, Bernard Duvic, Natacha Kremer, Philippe Gayral, Karine Musset, Thibaut Josse, Diane Bigot, Christophe Bressac, Sébastien Moreau, Georges Periquet, Myriam Harry, Nicolas Montagné, Isabelle Boulogne, Mahnaz Sabeti-Azad, Martine Maïbèche, Thomas Chertemps, Frédérique Hilliou, David Siaussat, Joëlle Amselem, Isabelle Luyten, Claire Capdevielle-Dulac, Karine Labadie, Bruna Laís Merlin, Valérie Barbe, Jetske G. de Boer, Martial Marbouty, Fernando Luis Cônsoli, Stéphane Dupas, Aurélie Hua-Van, Gaelle Le Goff, Annie Bézier, Emmanuelle Jacquin-Joly, James B. Whitfield, Louise E. M. Vet, Hans M. Smid, Laure Kaiser, Romain Koszul, Elisabeth Huguet, Elisabeth A. Herniou, and Jean-Michel Drezen
Subjects: Biology (General), QH301-705.5
Abstract: Jeremy Gauthier et al. present the chromosome scale assembly of the genome of the parasitic wasp C. congregata and show that bracovirus genes have colonized all ten chromosomes. Comparison with genome scaffolds of another wasp reveals a striking stability of these regions over ~53 million years, suggesting strong evolutionary constraints.
Published: 2021
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9. instaGRAAL: chromosome-level quality scaffolding of genomes using a proximity ligation-based scaffolder

Author: Lyam Baudry, Nadège Guiglielmoni, Hervé Marie-Nelly, Alexandre Cormier, Martial Marbouty, Komlan Avia, Yann Loe Mie, Olivier Godfroy, Lieven Sterck, J. Mark Cock, Christophe Zimmer, Susana M. Coelho, and Romain Koszul
Subjects: Ectocarpus, Hi-C scaffolding, Hi-C, genome assembly, MCMC, GPU, Desmarestia herbacea, Biology (General), QH301-705.5, Genetics, QH426-470
Abstract: Abstract Hi-C exploits contact frequencies between pairs of loci to bridge and order contigs during genome assembly, resulting in chromosome-level assemblies. Because few robust programs are available for this type of data, we developed instaGRAAL, a complete overhaul of the GRAAL program, which has adapted the latter to allow efficient assembly of large genomes. instaGRAAL features a number of improvements over GRAAL, including a modular correction approach that optionally integrates independent data. We validate the program using data for two brown algae, and human, to generate near-complete assemblies with minimal human intervention.
Published: 2020
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10. Chromosome organization by a conserved condensin-ParB system in the actinobacterium Corynebacterium glutamicum

Author: Kati Böhm, Giacomo Giacomelli, Andreas Schmidt, Axel Imhof, Romain Koszul, Martial Marbouty, and Marc Bramkamp
Subjects: Science
Abstract: The regulation of higher-order chromosome folding and segregation in bacteria is poorly understood. Here, Böhm et al. provide insights into the roles of DNA partitioning protein ParB and SMC condensin complexes in Corynebacterium glutamicum.
Published: 2020
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11. MetaHiC phage-bacteria infection network reveals active cycling phages of the healthy human gut

Author: Martial Marbouty, Agnès Thierry, Gaël A Millot, and Romain Koszul
Subjects: metagenomics, bacteroidetes, computational biology, proximity ligation, Hi-C, microbiome, Medicine, Science, Biology (General), QH301-705.5
Abstract: Bacteriophages play important roles in regulating the intestinal human microbiota composition, dynamics, and homeostasis, and characterizing their bacterial hosts is needed to understand their impact. We applied a metagenomic Hi-C approach on 10 healthy human gut samples to unveil a large infection network encompassing more than 6000 interactions bridging a metagenomic assembled genomes (MAGs) and a phage sequence, allowing to study in situ phage-host ratio. Whereas three-quarters of these sequences likely correspond to dormant prophages, 5% exhibit a much higher coverage than their associated MAG, representing potentially actively replicating phages. We detected 17 sequences of members of the crAss-like phage family, whose hosts diversity remained until recently relatively elusive. For each of them, a unique bacterial host was identified, all belonging to different genus of Bacteroidetes. Therefore, metaHiC deciphers infection network of microbial population with a high specificity paving the way to dynamic analysis of mobile genetic elements in complex ecosystems.
Published: 2021
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12. Author Correction: High-throughput identification of viral termini and packaging mechanisms in virome datasets using PhageTermVirome

Author: Julian R. Garneau, Véronique Legrand, Martial Marbouty, Maximilian O. Press, Dean R. Vik, Louis-Charles Fortier, Matthew B. Sullivan, David Bikard, and Marc Monot
Subjects: Medicine, Science
Published: 2022
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13. Tridimensional infiltration of DNA viruses into the host genome shows preferential contact with active chromatin

Author: Pierrick Moreau, Axel Cournac, Gianna Aurora Palumbo, Martial Marbouty, Shogofa Mortaza, Agnes Thierry, Stefano Cairo, Marc Lavigne, Romain Koszul, and Christine Neuveut
Subjects: Science
Abstract: Whether DNA viruses contact specific regions of host genomes or make random contacts is unclear. Here, the authors use Hi-C and show that HBV cccDNA and Ad5 DNA contact preferentially active chromatin at CpG islands for the former and at transcription start sites and enhancers for the latter.
Published: 2018
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14. Author Correction: Chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization

Author: Jérémy Gauthier, Hélène Boulain, Joke J. F. A. van Vugt, Lyam Baudry, Emma Persyn, Jean-Marc Aury, Benjamin Noel, Anthony Bretaudeau, Fabrice Legeai, Sven Warris, Mohamed A. Chebbi, Géraldine Dubreuil, Bernard Duvic, Natacha Kremer, Philippe Gayral, Karine Musset, Thibaut Josse, Diane Bigot, Christophe Bressac, Sébastien Moreau, Georges Periquet, Myriam Harry, Nicolas Montagné, Isabelle Boulogne, Mahnaz Sabeti-Azad, Martine Maïbèche, Thomas Chertemps, Frédérique Hilliou, David Siaussat, Joëlle Amselem, Isabelle Luyten, Claire Capdevielle-Dulac, Karine Labadie, Bruna Laís Merlin, Valérie Barbe, Jetske G. de Boer, Martial Marbouty, Fernando Luis Cônsoli, Stéphane Dupas, Aurélie Hua-Van, Gaelle Le Goff, Annie Bézier, Emmanuelle Jacquin-Joly, James B. Whitfield, Louise E. M. Vet, Hans M. Smid, Laure Kaiser, Romain Koszul, Elisabeth Huguet, Elisabeth A. Herniou, and Jean-Michel Drezen
Subjects: Biology (General), QH301-705.5
Published: 2021
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15. Proximity ligation scaffolding and comparison of two Trichoderma reesei strains genomes

Author: Etienne Jourdier, Lyam Baudry, Dante Poggi-Parodi, Yoan Vicq, Romain Koszul, Antoine Margeot, Martial Marbouty, and Frédérique Bidard
Subjects: Trichoderma reesei, Genome assembly, Hi-C, GRAAL, Centromere, Karyotype, Fuel, TP315-360, Biotechnology, TP248.13-248.65
Abstract: Abstract Background The presence of low complexity and repeated regions in genomes often results in difficulties to assemble sequencing data into full chromosomes. However, the availability of full genome scaffolds is essential to several investigations, regarding for instance the evolution of entire clades, the analysis of chromosome rearrangements, and is pivotal to sexual crossing studies. In non-conventional but industrially relevant model organisms, such as the ascomycete Trichoderma reesei, a complete genome assembly is seldom available. Results The chromosome scaffolds of T. reesei QM6a and Rut-C30 strains have been generated using a contact genomic/proximity ligation genomic approach. The original reference assembly, encompassing dozens of scaffolds, was reorganized into two sets of seven chromosomes. Chromosomal contact data also allowed to characterize 10–40 kb, gene-free, AT-rich (76%) regions corresponding to the T. reesei centromeres. Large chromosomal rearrangements (LCR) in Rut-C30 were then characterized, in agreement with former studies, and the position of LCR breakpoints used to assess the likely chromosome structure of other T. reesei strains [QM9414, CBS999.97 (1-1, re), and QM9978]. In agreement with published results, we predict that the numerous chromosome rearrangements found in highly mutated industrial strains may limit the efficiency of sexual reproduction for their improvement. Conclusions The GRAAL program allowed us to generate the karyotype of the Rut-C30 strain, and from there to predict chromosome structure for most T. reesei strains for which sequence is available. This method that exploits proximity ligation sequencing approach is a fast, cheap, and straightforward way to characterize both chromosome structure and centromere sequences and is likely to represent a popular convenient alternative to expensive and work-intensive resequencing projects.
Published: 2017
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16. MetaTOR: A Computational Pipeline to Recover High-Quality Metagenomic Bins From Mammalian Gut Proximity-Ligation (meta3C) Libraries

Author: Lyam Baudry, Théo Foutel-Rodier, Agnès Thierry, Romain Koszul, and Martial Marbouty
Subjects: metagenomics Hi-C, gut microbiome, Hi-C, metagenomics binning, metagenomic analysis, binning algorithm, Genetics, QH426-470
Abstract: Characterizing the complete genomic structure of complex microbial communities would represent a key step toward the understanding of their diversity, dynamics, and evolution. Current metagenomics approaches aiming at this goal are typically done by analyzing millions of short DNA sequences directly extracted from the environment. New experimental and computational approaches are constantly sought for to improve the analysis and interpretation of such data. We developed MetaTOR, an open-source computational solution that bins DNA contigs into individual genomes according to their 3D contact frequencies. Those contacts are quantified by chromosome conformation capture experiments (3C, Hi-C), also known as proximity-ligation approaches, applied to metagenomics samples (meta3C). MetaTOR was applied on 20 meta3C libraries of mice gut microbiota. We quantified the program ability to recover high-quality metagenome-assembled genomes (MAGs) from metagenomic assemblies generated directly from the meta3C libraries. Whereas nine high-quality MAGs are identified in the 148-Mb assembly generated using a single meta3C library, MetaTOR identifies 82 high-quality MAGs in the 763-Mb assembly generated from the merged 20 meta3C libraries, corresponding to nearly a third of the total assembly. Compared to the hybrid binning softwares MetaBAT or CONCOCT, MetaTOR recovered three times more high-quality MAGs. These results underline the potential of 3C-/Hi-C-based approaches in metagenomic projects.
Published: 2019
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17. Correction to: Proximity ligation scaffolding and comparison of two Trichoderma reesei strains genomes

Author: Etienne Jourdier, Lyam Baudry, Dante Poggi-Parodi, Yoan Vicq, Romain Koszul, Antoine Margeot, Martial Marbouty, and Frédérique Bidard
Subjects: Fuel, TP315-360, Biotechnology, TP248.13-248.65
Abstract: Following publication of the original article [1], the authors reported a problem in the drawing of Rut-C30 chromosome III in Fig. 2B of the original article [1]. The two fragments of chromosome I inserted inside chromosome III should be swapped, and the direction of the fragment containing rim101 and cel1a genes should be inverted. This reversed insertion indicates that at least 2 rearrangements occurred simultaneously, so the possible scenario proposed in Fig. 2C of the original article was inaccurate. The corrected figure with modified panels B and C is available in the figure below. The detailed description of Rut-C30 assembly in the Additional file 5 of the original article is correct.
Published: 2018
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18. Metagenomic chromosome conformation capture (meta3C) unveils the diversity of chromosome organization in microorganisms

Author: Martial Marbouty, Axel Cournac, Jean-François Flot, Hervé Marie-Nelly, Julien Mozziconacci, and Romain Koszul
Subjects: Hi-C, meta3C, metagenomics, plasmid F, meta Hi-C, genome assembly, Medicine, Science, Biology (General), QH301-705.5
Abstract: Genomic analyses of microbial populations in their natural environment remain limited by the difficulty to assemble full genomes of individual species. Consequently, the chromosome organization of microorganisms has been investigated in a few model species, but the extent to which the features described can be generalized to other taxa remains unknown. Using controlled mixes of bacterial and yeast species, we developed meta3C, a metagenomic chromosome conformation capture approach that allows characterizing individual genomes and their average organization within a mix of organisms. Not only can meta3C be applied to species already sequenced, but a single meta3C library can be used for assembling, scaffolding and characterizing the tridimensional organization of unknown genomes. By applying meta3C to a semi-complex environmental sample, we confirmed its promising potential. Overall, this first meta3C study highlights the remarkable diversity of microorganisms chromosome organization, while providing an elegant and integrated approach to metagenomic analysis.
Published: 2014
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19. The slow evolving genome of the xenacoelomorph worm Xenoturbella bocki

Author: Philipp H. Schiffer, Paschalis Natsidis, Daniel J. Leite, Helen E. Robertson, François Lapraz, Ferdinand Marlétaz, Bastian Fromm, Liam Baudry, Fraser Simpson, Eirik Høye, Anne-C. Zakrzewski, Paschalia Kapli, Katharina J. Hoff, Steven Mueller, Martial Marbouty, Heather Marlow, Richard R. Copley, Romain Koszul, Peter Sarkies, Maximilian J. Telford, University College of London [London] (UCL), Institut de Biologie Valrose (IBV), Université Nice Sophia Antipolis (1965 - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université Côte d'Azur (UCA), The Arctic University of Norway [Tromsø, Norway] (UiT), Collège Doctoral, Sorbonne Université (SU), Norwegian Radium Hospital, University of Oslo (UiO), Leibniz Institute for Evolution and Biodiversity Science, Museum für Naturkunde [Berlin], Universität Greifswald - University of Greifswald, Régulation spatiale des Génomes - Spatial Regulation of Genomes, Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité), University of Chicago, Laboratoire de Biologie du Développement de Villefranche sur mer (LBDV), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Institut de la Mer de Villefranche (IMEV), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Department of Biochemistry [Oxford], and University of Oxford
Subjects: [SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology, [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], [SDV.BID.SPT]Life Sciences [q-bio]/Biodiversity/Systematics, Phylogenetics and taxonomy
Abstract: The evolutionary origins of Bilateria remain enigmatic. One of the more enduring proposals highlights similarities between a cnidarian-like planula larva and simple acoel-like flatworms. This idea is based in part on the view of the Xenacoelomorpha as an outgroup to all other bilaterians which are themselves designated the Nephrozoa (protostomes and deuterostomes). Genome data, which can help to elucidate phylogenetic relationships and provide important comparative data, remain sparse for early branching bilaterians. Here we assemble and analyse the genome of the simple, marine xenacoelomorphXenoturbella bocki, a key species for our understanding of early bilaterian and deuterostome evolution. Our highly contiguous genome assembly ofX. bockihas a size of ∼110 Mbp in 18 chromosome like scaffolds, with repeat content, and intron, exon and intergenic space comparable to other bilaterian invertebrates. We findX. bockito have a similar number of genes to other bilaterians and to have retained ancestral metazoan synteny. Key bilaterian signalling pathways are also largely complete and most bilaterian miRNAs are present. We conclude thatX. bockihas a complex genome typical of bilaterians, in contrast to the apparent simplicity of its body plan. Overall, our data do not provide evidence supporting the idea that Xenacoelomorpha are a primitively simple outgroup to other bilaterians and gene presence/absence data support a relationship with Ambulacraria.
Published: 2022

20. Filling annotation gaps in yeast genomes using genome-wide contact maps.

Author: Hervé Marie-Nelly, Martial Marbouty, Axel Cournac, Gianni Liti, Gilles Fischer, Christophe Zimmer, and Romain Koszul
Published: 2014
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21. Chromosomal assembly of the flat oyster (Ostrea edulisL.) genome as a new genetic ressource for aquaculture

Author: Isabelle Boutet, Homère J. Alves Monteiro, Lyam Baudry, Takeshi Takeuchi, Eric Bonnivard, Bernard Billoud, Sarah Farhat, Ricardo Gonzales-Haraya, Benoit Salaun, Ann Andersen, Jean-Yves Toullec, François Lallier, Jean-François Flot, Nadège Guiglielmoni, Ximing Guo, Li Cui, Bassem Allam, Emmanuelle Pales-Espinoza, Jakob Hemmer-Hansen, Martial Marbouty, Romain Koszul, and Arnaud Tanguy
Abstract: The European flat oyster (Ostrea edulisL.) is the endemic species of the European coasts. Its exploitation has been reduced during the last decades, because of the appearance of two parasites that have led to the collapse of the stocks and the strong decline of the natural oyster beds.O. edulishas been the subject of numerous studies and programs in population genetics and on the presence of the parasitesBonamia ostreaeandMarteilia refringens. These studies investigated the effects of these parasites mainly on immunity at the molecular and cellular levels. Several genetic selection programs especially related to resistance to the parasite have been initiated. Within the framework of a European project (PERLE 2) which aims to produce genetic lines ofO. eduliswith hardiness traits (growth, survival, resistance) for the purpose of repopulating natural oyster beds in Brittany and reviving the culture of this species on the foreshore, obtaining a reference genome has proved to be essential as done recently in many bivalve species of aquaculture interest. Here, we present a chromosome-level genome assembly and annotation for the European flat oyster, generated by combining PacBio technology, Illumina, 10X linked and Hi-C sequencing. The finished assembly is 887.2 Mb with a scaffold-N50 of 97.1 Mb scaffolded on the expected 10 pseudo-chromosomes. Annotation of the genome revealed the presence of 35962 protein-coding genes. We analyzed in details the transposable elements (TE) diversity in the flat oyster genome, highlight some specificities in tRNA and miRNA composition and provide first insights in the molecular response ofO. edulistoM. refringens. This genome will serve as a reference for genomic studies onO. edulisto better understand its basic physiology or developing genetic markers in breeding projects for aquaculture or natural reef restoration.
Published: 2022
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22. Chromosome folding and prophage activation reveal gut-specific genome dynamics of bacteria in the OMM12consortium

Author: Quentin Lamy-Besnier, Amaury Bignaud, Julian R. Garneau, Marie Titecat, Devon Conti, Alexandra Von Strempel, Marc Monot, Bärbel Stecher, Romain Koszul, Laurent Debarbieux, and Martial Marbouty
Abstract: Bacteria and their viruses, bacteriophages, are the most abundant entities of the gut microbiota, a complex community of microorganisms associated with human health and disease. In this ecosystem the interactions between these two key components are still largely unknown. In particular, the impact of the gut environment on bacteria and their associated prophages is yet to be deciphered. To gain insight into the activity of lysogenic phages within the context of their host genomes, we performed Hi-C on the 12 strains of the OMM12synthetic bacterial community stably associated within mice gut (gnotobiotic mouse line OMM12) in bothin vitroandin vivoconditions. High-resolution contact maps of the chromosome 3D organization of the bacterial genomes revealed a wide diversity of architectures, differences between environments and an overall stability over time in the gut of mice. The DNA contacts also pointed at 3D signatures of prophages leading to predict 16 of them as functional. We identified circularization signals and observed different 3D patterns depending on the condition. Concurrent virome analysis showed that 11 of these prophages produced viral particlesin vivoand/orin vitro, and that OMM12mice do not carry other intestinal viruses. By predicting functional prophages, the Hi-C approach unlocks the study of phage-bacteria interaction dynamics.
Published: 2022
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23. Chromosome organization by a conserved condensin-ParB system in the actinobacterium Corynebacterium glutamicum

Author: Marc Bramkamp, Romain Koszul, Andreas Schmidt, Kati Boehm, Martial Marbouty, Axel Imhof, Giacomo Giacomelli, Ludwig-Maximilians-Universität München (LMU), Institut für Allgemeine Mikrobiologie, Christian-Albrechts-Universität zu Kiel (CAU), Régulation spatiale des Génomes - Spatial Regulation of Genomes, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Centre de Bioinformatique, Biostatistique et Biologie Intégrative (C3BI), This work was funded by grants to M.B. from the Deutsche Forschungsgemeinschaft (project 326464754 in TRR174 and BR2815/6-2) and the Ministry of Science and Education (BMBF: 031A302 e:Bio-Modul II: 0.6 plus). This research was supported by funding to R.K. from the European Research Council under the Horizon 2020 Program (ERC grant agreement 260822), and from Agence Nationale pour la Recherche (HiResBac ANR-15-CE11-0023-03) and JPI-EC-AMR STARCS ANR-16-JPEC-0003-05 all to R.K., ANR-15-CE11-0023,HiResBaCS,Structure des chromosomes bactériens revélée a haute résolution(2015), ANR-16-JPEC-0003,STARCS,Selection and Transmission of Antimicrobial Resistance in Complex Systems(2016), European Project: 260822,EC:FP7:ERC,ERC-2010-StG_20091118,DICIG(2011), and Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS)
Subjects: DNA, Bacterial, 0301 basic medicine, [SDV]Life Sciences [q-bio], Condensin, Science, Centromere, General Physics and Astronomy, Replication Origin, DNA Primase, macromolecular substances, Article, General Biochemistry, Genetics and Molecular Biology, Corynebacterium glutamicum, Plasmid maintenance, Chromosome segregation, Chromosome conformation capture, 03 medical and health sciences, Condensin complex, 0302 clinical medicine, Bacterial Proteins, Cellular microbiology, lcsh:Science, 030304 developmental biology, Adenosine Triphosphatases, 0303 health sciences, Multidisciplinary, Bacteria, biology, Chemistry, Circular bacterial chromosome, Chromosome, General Chemistry, Chromosomes, Bacterial, Cell biology, DNA-Binding Proteins, Nucleoproteins, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, 030104 developmental biology, Chromosome Structures, Multiprotein Complexes, biology.protein, bacteria, lcsh:Q, Nucleoid organization, 030217 neurology & neurosurgery, Bacillus subtilis
Abstract: Higher-order chromosome folding and segregation are tightly regulated in all domains of life. In bacteria, details on nucleoid organization regulatory mechanisms and function remain poorly characterized, especially in non-model species. Here, we investigate the role of DNA-partitioning protein ParB and SMC condensin complexes in the actinobacterium Corynebacterium glutamicum. Chromosome conformation capture reveals SMC-mediated long-range interactions around ten centromere-like parS sites clustered at the replication origin (oriC). At least one oriC-proximal parS site is necessary for reliable chromosome segregation. We use chromatin immunoprecipitation and photoactivated single-molecule localization microscopy to show the formation of distinct, parS-dependent ParB-nucleoprotein subclusters. We further show that SMC/ScpAB complexes, loaded via ParB at parS sites, mediate chromosomal inter-arm contacts (as previously shown in Bacillus subtilis). However, the MukBEF-like SMC complex MksBEFG does not contribute to chromosomal DNA-folding; instead, this complex is involved in plasmid maintenance and interacts with the polar oriC-tethering factor DivIVA. Our results complement current models of ParB-SMC/ScpAB crosstalk and show that some condensin complexes evolved functions that are apparently uncoupled from chromosome folding., The regulation of higher-order chromosome folding and segregation in bacteria is poorly understood. Here, Böhm et al. provide insights into the roles of DNA partitioning protein ParB and SMC condensin complexes in Corynebacterium glutamicum.
Published: 2020
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24. Chromosome-level genome assembly reveals homologous chromosomes and recombination in asexual rotifer Adineta vaga

Author: Karine Van Doninck, Richard Cordaux, Thomas Lenormand, Clément Gilbert, Karine Labadie, Lyam Baudry, Julie Virgo, Boris Hespeels, Djampa K. L. Kozlowski, Jitendra Narayan, Alessandro Derzelle, Marie Cariou, Antoine Limasset, Florence Gaudray, Bernard Hallet, Martial Marbouty, Etienne Danchin, Antoine Houtain, Rohan Arora, Matthieu Terwagne, Corinne Cruaud, Nadège Guiglielmoni, Jean-François Flot, Romain Koszul, Paul Simion, Emilien Nicolas, Marc Llirós, Université de Namur [Namur] (UNamur), Régulation spatiale des Génomes - Spatial Regulation of Genomes, Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité), Collège Doctoral, Sorbonne Université (SU), Université libre de Bruxelles (ULB), 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), Genoscope - Centre national de séquençage [Evry] (GENOSCOPE), Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Evolution, génomes, comportement et écologie (EGCE), Institut de Recherche pour le Développement (IRD)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Institut Sophia Agrobiotech (ISA), Université Nice Sophia Antipolis (1965 - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Côte d'Azur (UCA), Centre de Recherche en Informatique, Signal et Automatique de Lille - UMR 9189 (CRIStAL), Centrale Lille-Université de Lille-Centre National de la Recherche Scientifique (CNRS), Institut d'Investigació Biomèdica de Girona Dr. Josep Trueta - Girona Biomedical Research Institute (IDIBGI), Ecologie et biologie des interactions (EBI), Université de Poitiers-Centre National de la Recherche Scientifique (CNRS), Louvain Institute of Biomolecular Science and Technology (LIBST), Université Catholique de Louvain = Catholic University of Louvain (UCL), Centre d’Ecologie Fonctionnelle et Evolutive (CEFE), Université Paul-Valéry - Montpellier 3 (UPVM)-École Pratique des Hautes Études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut Agro - Montpellier SupAgro, 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), Interuniversity Institute of Bioinformatics in Brussels (IB2), Université libre de Bruxelles (ULB)-Vrije Universiteit Brussel (VUB), This project received funding from the Horizon 2020 research and innovation program under European Research Council (ERC) grant agreement 725998 (RHEA) and from BELSPO PRODEX for the ESA selected ILSRA-2014-0106 Project to K.V.D., from the Fédération Wallonie-Bruxelles via an 'Action de Recherche Concertée' (ARC) grant to K.V.D. and B.Ha., from the European Union’s Horizon 2020 research and innovation programme under Marie Skłodowska-Curie grant agreement 764840 to J.-F.F. (ITN IGNITE), from the Fédération Wallonie-Bruxelles via an Action de Recherche Concertée (ARC) grant to J.-F.F., from the European Research Council under the Horizon 2020 Program (ERC grant agreement 260822) and JPI-EC-AMR STARCS ANR-16-JPEC-0003-05 grant to R.K., and through funding by the French Government 'Investissement d’Avenir' program FRANCE GENOMIQUE (ANR-10-INBS-09). E.N. obtained an FSR UNamur fund. A.H., A.D., and R.A. are Research Fellows of the Fonds de la Recherche Scientifique—FNRS., ANR-16-JPEC-0003,STARCS,Selection and Transmission of Antimicrobial Resistance in Complex Systems(2016), ANR-10-INBS-0009,France-Génomique,Organisation et montée en puissance d'une Infrastructure Nationale de Génomique(2010), European Project: 764840,IGNITE, European Project: 260822,EC:FP7:ERC,ERC-2010-StG_20091118,DICIG(2011), Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Collège doctoral [Sorbonne universités], Centre International de Recherche en Infectiologie - UMR (CIRI), Institut National de la Santé et de la Recherche Médicale (INSERM)-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), Université Nice Sophia Antipolis (... - 2019) (UNS), Université Paul-Valéry - Montpellier 3 (UPVM)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-École pratique des hautes études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-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: 0106 biological sciences, Sequence assembly, Rotifer, Evolution des espèces, Biology, 010603 evolutionary biology, 01 natural sciences, 03 medical and health sciences, chemistry.chemical_compound, Homologous chromosome, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, Océanographie biologique, Clade, 030304 developmental biology, Genetics, 0303 health sciences, Multidisciplinary, Biologie moléculaire, Chromosome, Adineta vaga, Genome, LOH, Adineta vaga, bdelloid rotifer, biology.organism_classification, [SDV.GEN.GH]Life Sciences [q-bio]/Genetics/Human genetics, chemistry, Génétique, cytogénétique, Systématique des espèces [zoologie], DNA, Recombination
Abstract: Bdelloid rotifers are notorious as a speciose ancient clade comprising only asexual lineages. Thanks to their ability to repair highly fragmented DNA, most bdelloid species also withstand complete desiccation and ionizing radiation. Producing a well-assembled reference genome is a critical step to developing an understanding of the effects of long-term asexuality and DNA breakage on genome evolution. To this end, we present the first high-quality chromosome-level genome assemblies for the bdelloid Adineta vaga, composed of six pairs of homologous (diploid) chromosomes with a footprint of paleotetraploidy. The observed large-scale losses of heterozygosity are signatures of recombination between homologous chromosomes, either during mitotic DNA double-strand break repair or when resolving programmed DNA breaks during a modified meiosis. Dynamic subtelomeric regions harbor more structural diversity (e.g. chromosome rearrangements, transposable elements, and haplotypic divergence). Our results trigger the reappraisal of potential meiotic processes in bdelloid rotifers and help unravel the factors underlying their long-term asexual evolutionary success., SCOPUS: ar.j, info:eu-repo/semantics/published
Published: 2021
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25. Chromosome-level genome assembly reveals homologous chromosomes and recombination in asexual rotifer

Author: Paul, Simion, Jitendra, Narayan, Antoine, Houtain, Alessandro, Derzelle, Lyam, Baudry, Emilien, Nicolas, Rohan, Arora, Marie, Cariou, Corinne, Cruaud, Florence Rodriguez, Gaudray, Clément, Gilbert, Nadège, Guiglielmoni, Boris, Hespeels, Djampa K L, Kozlowski, Karine, Labadie, Antoine, Limasset, Marc, Llirós, Martial, Marbouty, Matthieu, Terwagne, Julie, Virgo, Richard, Cordaux, Etienne G J, Danchin, Bernard, Hallet, Romain, Koszul, Thomas, Lenormand, Jean-Francois, Flot, and Karine, Van Doninck
Subjects: Genetics, SciAdv r-articles, Biomedicine and Life Sciences, Research Article
Abstract: Description, High-quality genome assembly of ancient asexual rotifer reveals homologous chromosomes that frequently recombine., Bdelloid rotifers are notorious as a speciose ancient clade comprising only asexual lineages. Thanks to their ability to repair highly fragmented DNA, most bdelloid species also withstand complete desiccation and ionizing radiation. Producing a well-assembled reference genome is a critical step to developing an understanding of the effects of long-term asexuality and DNA breakage on genome evolution. To this end, we present the first high-quality chromosome-level genome assemblies for the bdelloid Adineta vaga, composed of six pairs of homologous (diploid) chromosomes with a footprint of paleotetraploidy. The observed large-scale losses of heterozygosity are signatures of recombination between homologous chromosomes, either during mitotic DNA double-strand break repair or when resolving programmed DNA breaks during a modified meiosis. Dynamic subtelomeric regions harbor more structural diversity (e.g., chromosome rearrangements, transposable elements, and haplotypic divergence). Our results trigger the reappraisal of potential meiotic processes in bdelloid rotifers and help unravel the factors underlying their long-term asexual evolutionary success.
Published: 2021

26. Metagenomes Binning Using Proximity-Ligation Data

Author: Romain Koszul, Martial Marbouty, Régulation spatiale des Génomes - Spatial Regulation of Genomes, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), This research was supported by funding to R.K. from the European Research Council under the Horizon 2020 Program (ERC grant agreement 771813) and Agence Nationale pour la Recherche JPI-EC-AMR STARCS (ANR-16-JPEC-0003-05)., ANR-16-JPEC-0003,STARCS,Selection and Transmission of Antimicrobial Resistance in Complex Systems(2016), European Project: 771813,SynarchiC, Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité), and European Project: 771813,ERC-2017-COG,SynarchiC(2018)
Subjects: Metagenomic Hi-C, Chromosome conformation capture, 0303 health sciences, Contig, [SDV]Life Sciences [q-bio], Metagenomes assemble genomes, Binning, Computational biology, Biology, Genome, 03 medical and health sciences, chemistry.chemical_compound, 0302 clinical medicine, chemistry, Hi-C, Metagenomics, Extrachromosomal DNA, metaHiC, 030217 neurology & neurosurgery, DNA, Meta3C, 030304 developmental biology
Abstract: International audience; Microbial communities are key components of all ecosystems, but characterization of their complete genomic structure remains challenging. Typical analysis tends to elude the complexity of the mixes in terms of species, strains, as well as extrachromosomal DNA molecules. Recently, approaches have been developed that bins DNA contigs into individual genomes and episomes according to their 3D contact frequencies. Those contacts are quantified by chromosome conformation capture experiments (3C, Hi-C), also known as proximity-ligation approaches, applied to metagenomics samples. Here, we present a simple computational pipeline that allows to recover high-quality Metagenomics Assemble Genomes (MAGs) starting from metagenomic 3C or Hi-C datasets and a metagenome assembly.
Published: 2021
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27. Author Correction: Chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization

Author: Martine Maïbèche, Hélène Boulain, Christophe Bressac, Laure Kaiser, Emma Persyn, Valérie Barbe, Anthony Bretaudeau, Martial Marbouty, Bernard Duvic, Georges Periquet, Annie Bézier, Lyam Baudry, Jean-Marc Aury, Mahnaz Sabeti-Azad, Géraldine Dubreuil, Karine Labadie, Fernando Luis Cônsoli, Benjamin Noel, Frédérique Hilliou, Thomas Chertemps, Elisabeth A. Herniou, Mohamed Amine Chebbi, Fabrice Legeai, Jérémy Gauthier, Jetske G. de Boer, Nicolas Montagné, Joelle Amselem, Jean-Michel Drezen, Thibaut Josse, Sébastien J. M. Moreau, Sven Warris, Louise E. M. Vet, Isabelle Boulogne, Myriam Harry, Diane Bigot, Elisabeth Huguet, Karine Musset, Natacha Kremer, Claire Capdevielle-Dulac, Joke J.F.A. van Vugt, James B. Whitfield, Aurélie Hua-Van, Hans M. Smid, Gaëlle Le Goff, Romain Koszul, Bruna Laís Merlin, Stéphane Dupas, Isabelle Luyten, Philippe Gayral, Emmanuelle Jacquin-Joly, and David Siaussat
Subjects: Scale (ratio), QH301-705.5, Genome, Insect, Wasps, Medicine (miscellaneous), Computational biology, Biology, Receptors, Odorant, Synteny, Genome, Evolutionary genetics, General Biochemistry, Genetics and Molecular Biology, Virus, 03 medical and health sciences, 0302 clinical medicine, Animals, Nudiviridae, Colonization, Biology (General), Author Correction, Symbiosis, Conserved Sequence, 030304 developmental biology, 0303 health sciences, Base Sequence, Biological Evolution, Genome evolution, Chromosomes, Insect, Smell, Polydnaviridae, General Agricultural and Biological Sciences, Entomology, 030217 neurology & neurosurgery
Abstract: Endogenous viruses form an important proportion of eukaryote genomes and a source of novel functions. How large DNA viruses integrated into a genome evolve when they confer a benefit to their host, however, remains unknown. Bracoviruses are essential for the parasitism success of parasitoid wasps, into whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome at a chromosomal scale, that bracovirus genes colonized all ten chromosomes of Cotesia congregata. Most form clusters of genes involved in particle production or parasitism success. Genomic comparison with another wasp, Microplitis demolitor, revealed that these clusters were already established ~53 mya and thus belong to remarkably stable genomic structures, the architectures of which are evolutionary constrained. Transcriptomic analyses highlight temporal synchronization of viral gene expression without resulting in immune gene induction, suggesting that no conflicts remain between ancient symbiotic partners when benefits to them converge.
Published: 2021
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28. Decision letter: Linking plasmid-based beta-lactamases to their bacterial hosts using single-cell fusion PCR

Author: Martial Marbouty
Published: 2021
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29. Chromosomal scale assembly of parasitic wasp genome reveals symbiotic virus colonization

Author: Myriam Harry, Bernard Duvic, Anthony Bretaudeau, Hélène Boulain, Jetske G. de Boer, Jean-Marc Aury, Claire Capdevielle-Dulac, Annie Bézier, Diane Bigot, Natacha Kremer, Laure Kaiser, Lyam Baudry, Joke J.F.A. van Vugt, Jean-Michel Drezen, Georges Periquet, Stéphane Dupas, Romain Koszul, Aurélie Hua-Van, Jérémy Gauthier, Fabrice Legeai, Emma Persyn, Mahnaz Sabeti-Azad, Fernando Luis Cônsoli, Valérie Barbe, Joelle Amselem, Karine Labadie, Benjamin Noel, Frédérique Hilliou, Martine Maïbèche, Géraldine Dubreuil, Isabelle Luyten, Karine Musset, Martial Marbouty, Christophe Bressac, Isabelle Boulogne, Louise E. M. Vet, Thibaut Josse, Philippe Gayral, Hans M. Smid, Emmanuelle Jacquin-Joly, David Siaussat, James B. Whitfield, Elisabeth A. Herniou, Mohamed Amine Chebbi, Thomas Chertemps, Nicolas Montagné, Sébastien J. M. Moreau, Elisabeth Huguet, Bruna Laís Merlin, Gaëlle Le Goff, Sven Warris, Institut de recherche sur la biologie de l'insecte UMR7261 (IRBI), Université de Tours-Centre National de la Recherche Scientifique (CNRS), Natural History Museum [Geneva], Swiss Federal Insitute of Aquatic Science and Technology [Dübendorf] (EAWAG), Netherlands Institute of Ecology - NIOO-KNAW (NETHERLANDS), Régulation spatiale des Génomes - Spatial Regulation of Genomes, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Collège doctoral [Sorbonne universités], Sorbonne Université (SU), 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)-Université de Paris (UP)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Génomique métabolique (UMR 8030), Genoscope - Centre national de séquençage [Evry] (GENOSCOPE), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Université d'Évry-Val-d'Essonne (UEVE), Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Université de Bretagne Sud (UBS)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National de Recherche en Informatique et en Automatique (Inria)-École normale supérieure - Rennes (ENS Rennes)-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-CentraleSupélec-IMT Atlantique Bretagne-Pays de la Loire (IMT Atlantique), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT), Institut de Génétique, Environnement et Protection des Plantes (IGEPP), 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), Scalable, Optimized and Parallel Algorithms for Genomics (GenScale), Inria Rennes – Bretagne Atlantique, Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)-GESTION DES DONNÉES ET DE LA CONNAISSANCE (IRISA-D7), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Université de Bretagne Sud (UBS)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Institut de Recherche en Informatique et Systèmes Aléatoires (IRISA), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-École normale supérieure - Rennes (ENS Rennes)-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1), Wageningen University and Research [Wageningen] (WUR), Diversité, Génomes & Interactions Microorganismes - Insectes [Montpellier] (DGIMI), Université de Montpellier (UM)-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), Evolution, génomes, comportement et écologie (EGCE), Institut de Recherche pour le Développement (IRD)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Unité de Recherche Génomique Info (URGI), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay, Escola Superior de Agricultura 'Luiz de Queiroz' (ESALQ), Universidade de São Paulo (USP), Department of Entomology [Urbana], University of Illinois System, Department of Terrestrial Ecology [Wageningen], Netherlands Institute of Ecology (NIOO-KNAW), ANR-12-ADAP-0001, Agence Nationale de la Recherche, Université de Tours (UT)-Centre National de la Recherche Scientifique (CNRS), Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Collège Doctoral, 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), Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS), Université de Rennes (UR)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique (IMT Atlantique), 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), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Université de Rennes (UR)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique (IMT Atlantique), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Universidade de São Paulo = University of São Paulo (USP), ANR-12-ADAP-0001,ABC - PaPoGen,Adaptation en lutte biologique - Génomique des populations de parasitoïdes(2012), Evolutionary Genetics, Development & Behaviour, Terrestrial Ecology (TE), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-Institut National de Recherche en Informatique et en Automatique (Inria)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique (IMT Atlantique), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-INSTITUT AGRO Agrocampus Ouest, Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Université de Rennes 1 (UR1), and Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Bretagne Sud (UBS)-École normale supérieure - Rennes (ENS Rennes)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS)-IMT Atlantique (IMT Atlantique)
Subjects: Genome evolution, food.ingredient, QH301-705.5, Bioinformatics, [SDV]Life Sciences [q-bio], Medicine (miscellaneous), macromolecular substances, Biology, Genome, Article, Evolutionary genetics, General Biochemistry, Genetics and Molecular Biology, Plan_S-Compliant-OA, Parasitoid wasp, 03 medical and health sciences, BIOS Applied Bioinformatics, 0302 clinical medicine, food, Bioinformatica, Life Science, Cotesia congregata, VÍRUS DE DNA, Biology (General), Laboratory of Entomology, Gene, 030304 developmental biology, 0303 health sciences, [SDV.GEN]Life Sciences [q-bio]/Genetics, Human evolutionary genetics, Chromosome, biology.organism_classification, PE&RC, Laboratorium voor Entomologie, Evolutionary biology, international, EPS, General Agricultural and Biological Sciences, Bracovirus, Entomology, 030217 neurology & neurosurgery
Abstract: Endogenous viruses form an important proportion of eukaryote genomes and a source of novel functions. How large DNA viruses integrated into a genome evolve when they confer a benefit to their host, however, remains unknown. Bracoviruses are essential for the parasitism success of parasitoid wasps, into whose genomes they integrated ~103 million years ago. Here we show, from the assembly of a parasitoid wasp genome at a chromosomal scale, that bracovirus genes colonized all ten chromosomes of Cotesia congregata. Most form clusters of genes involved in particle production or parasitism success. Genomic comparison with another wasp, Microplitis demolitor, revealed that these clusters were already established ~53 mya and thus belong to remarkably stable genomic structures, the architectures of which are evolutionary constrained. Transcriptomic analyses highlight temporal synchronization of viral gene expression without resulting in immune gene induction, suggesting that no conflicts remain between ancient symbiotic partners when benefits to them converge., Jeremy Gauthier et al. present the chromosome scale assembly of the genome of the parasitic wasp C. congregata and show that bracovirus genes have colonized all ten chromosomes. Comparison with genome scaffolds of another wasp reveals a striking stability of these regions over ~53 million years, suggesting strong evolutionary constraints.
Published: 2021
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30. Author response: MetaHiC phage-bacteria infection network reveals active cycling phages of the healthy human gut

Author: Romain Koszul, Martial Marbouty, Gaël A. Millot, and Agnès Thierry
Subjects: Human gut, biology, Cycling, biology.organism_classification, Bacteria, Microbiology
Published: 2021
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31. Homologous chromosomes in asexual rotifer Adineta vaga suggest automixis

Author: Martial Marbouty, Benjamin Noel, Bernard Hallet, Paul Simion, Patrick Wincker, Djampa K. L. Kozlowski, Romain Koszul, Etienne Danchin, Jitendra Narayan, Antoine Houtain, Antoine Limasset, Marie Cariou, Emilien Nicolas, Florence Gaudray, Lyam Baudry, Julie Virgo, Karine Van Doninck, Alessandro Derzelle, Jean-François Flot, Matthieu Terwagne, and Nadège Guiglielmoni
Subjects: Genetics, Genome evolution, Meiosis, Homologous chromosome, Chromosome, Parthenogenesis, Biology, Genome, Synteny, Reference genome
Abstract: The several hundreds of species of bdelloid rotifers are notorious because they represent an ancient clade comprising only asexual lineages1. Moreover, most bdelloid species have the ability to withstand complete desiccation and high doses of ionizing radiation, being able to repair their DNA after massive genome breakage2. To better understand the impact of long-term asexuality and DNA breakage on genome evolution, a telomere-to-tolemere reference genome assembly of a bdelloid species is critical3, 4. Here we present the first, high quality chromosome-scale genome assembly for the bdelloid A. vaga validated using three complementary assembly procedures combined with chromosome conformation capture (Hi-C) data. The different assemblies reveal the same genome architecture and using fluorescent in situ hybridization (FISH), we demonstrate that the A. vaga genome is composed of six pairs of homologous chromosomes, compatible with meiosis. Moreover, the synteny between homoeologous (or ohnologous) chromosomes is also preserved, confirming their paleotetraploidy. The diploid genome structure of A. vaga and the presence of very long homozygous tracts show that recombination between homologous chromosomes occurs in this ancient asexual scandal, either during DSB repair or during meiotic pairing. These homozygosity tracts are mainly observed towards the chromosome ends in the clonal A. vaga suggesting signatures of a parthenogenetic mode of reproduction equivalent to central fusion automixis, in which homologous chromosomes are not segregated during the meiotic division.
Published: 2020
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32. Phages - bacteria interactions network of the healthy human gut

Author: Agnès Thierry, Martial Marbouty, and Romain Koszul
Subjects: Human gut, Metagenomics, Evolutionary biology, Human microbiome, Bacteroidetes, Ecosystem, Single sample, Biology, biology.organism_classification, Prophage, Bacteria
Abstract: With an estimated 1031particles on earth, bacteriophages are the most abundant genomic entities across all habitats and important drivers of microbial communities. Growing evidence suggest that they play roles in intestinal human microbiota homeostasis, and recent metagenomics studies on the viral fraction of this ecosystem have provided crucial information about their diversity and specificity. However, the bacterial hosts of this viral fraction, a necessary information to characterize further the balance of these ecosystems, remain poorly characterized. Here we unveil, using an enhanced metagenomic Hi-C approach, a large network of 6,651 host-phage relationships in the healthy human gut allowing to studyin situphage-host ratio. We notably found that half of these contigs appear to be sleeping prophages whereas ¼ exhibit a higher coverage than their associated MAG representing potentially active phages impacting the ecosystem. We also detect different candidate members of the crAss-like phage family as well as their bacterial hosts showing that these elusive phages infect different genus of Bacteroidetes. This work opens the door to single sample analysis and concomitant study of phages and bacteria in complex communities.
Published: 2020
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33. Tridimensional infiltration of DNA viruses into the host genome shows preferential contact with active chromatin

Author: Martial Marbouty, Stefano Cairo, Christine Neuveut, Romain Koszul, Agnès Thierry, Gianna Aurora Palumbo, Marc Lavigne, Shogofa Mortaza, Axel Cournac, Pierrick Moreau, Hépacivirus et Immunité innée, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Régulation spatiale des Génomes - Spatial Regulation of Genomes, XenTech [Évry], Institut Cochin (IC UM3 (UMR 8104 / U1016)), Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université de Paris (UP), Département de Virologie - Department of Virology, Institut Pasteur [Paris], This work was supported by funding to C.N. from the Agence Nationale de la Recherche sur le Sida et les Hépatites Virales (ANRS) and Fondation pour la Recherche sur le Cancer (ARC). This research was also supported by funding to R.K. from the European Research Council under the 7th and H2020 Framework Program (FP7/2007-2013, ERC grant agreement 260822 and H2020 ERC grant agreement DLV-771813), and from Agence Nationale pour la Recherche (MeioRec ANR-13-BSV6-0012). P.M. was supported by ANRS and Institut Carnot. This study makes use of data generated by the ENCODE Consortium and the ENCODE production laboratories., We thank C. Seeger and S. Urban for kindly providing cell lines used in this study. We thank the UTechS PBI (Imagopole)-DTPS/C2RT, part of the France-BioImaging infrastructure network supported by the ANR (ANR-10-INSB-04, Investments for theFuture), for the use of the Zeiss widefield apotome microscope., ANR-13-BSV6-0012,MeioRec,Dynamique chromosomique et recombinaison au cours de la méiose(2013), European Project: 260822,EC:FP7:ERC,ERC-2010-StG_20091118,DICIG(2011), Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité), Institut Pasteur [Paris] (IP), THIERRY, AGNES, Blanc 2013 - Dynamique chromosomique et recombinaison au cours de la méiose - - MeioRec2013 - ANR-13-BSV6-0012 - Blanc 2013 - VALID, and Dynamic Interplay between Eukaryotic Chromosomes: Impact on Genome Stability - DICIG - - EC:FP7:ERC2011-06-01 - 2017-05-31 - 260822 - VALID
Subjects: 0301 basic medicine, Transcription, Genetic, viruses, General Physics and Astronomy, MESH: Base Sequence, Genome, chemistry.chemical_compound, MESH: Chromatin / metabolism, 0302 clinical medicine, Transcription (biology), Adenovirus, Viral Regulatory and Accessory Proteins, lcsh:Science, [SDV.MP.VIR] Life Sciences [q-bio]/Microbiology and Parasitology/Virology, Multidisciplinary, Virus–host interactions, Hep G2 Cells, MESH: Gene Expression Regulation, Chromatin, 3. Good health, Cell biology, Up-Regulation, CpG site, [SDV.MP.VIR]Life Sciences [q-bio]/Microbiology and Parasitology/Virology, MESH: Transcription Initiation Site, Transcription Initiation Site, Plasmids, Hepatitis B virus, Science, MESH: Hep G2 Cells, Biology, Models, Biological, General Biochemistry, Genetics and Molecular Biology, Article, 03 medical and health sciences, MESH: Plasmids / metabolism, MESH: Genome, Human, MESH: Up-Regulation / genetics, Humans, MESH: DNA, Viral / genetics, Enhancer, Gene, Transcription factor, MESH: Humans, Base Sequence, Genome, Human, MESH: Transcription, Genetic, MESH: Models, Biological, General Chemistry, MESH: Hepatitis B virus / physiology, MESH: CpG Islands / genetics, MESH: Hepatocytes / virology, MESH: Trans-Activators / metabolism, 030104 developmental biology, chemistry, Gene Expression Regulation, DNA, Viral, Hepatocytes, Trans-Activators, CpG Islands, lcsh:Q, 030217 neurology & neurosurgery, DNA
Abstract: Whether non-integrated viral DNAs distribute randomly or target specific positions within the higher-order architecture of mammalian genomes remains largely unknown. Here we use Hi-C and viral DNA capture (CHi-C) in primary human hepatocytes infected by either hepatitis B virus (HBV) or adenovirus type 5 (Ad5) virus to show that they adopt different strategies in their respective positioning at active chromatin. HBV contacts preferentially CpG islands (CGIs) enriched in Cfp1 a factor required for its transcription. These CGIs are often associated with highly expressed genes (HEG) and genes deregulated during infection. Ad5 DNA interacts preferentially with transcription start sites (TSSs) and enhancers of HEG, as well as genes upregulated during infection. These results show that DNA viruses use different strategies to infiltrate genomic 3D networks and target specific regions. This targeting may facilitate the recruitment of transcription factors necessary for their own replication and contribute to the deregulation of cellular gene expression., Whether DNA viruses contact specific regions of host genomes or make random contacts is unclear. Here, the authors use Hi-C and show that HBV cccDNA and Ad5 DNA contact preferentially active chromatin at CpG islands for the former and at transcription start sites and enhancers for the latter.
Published: 2018
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34. Chromosome-level quality scaffolding of brown algal genomes using InstaGRAAL, a proximity ligation-based scaffolder

Author: Hervé Marie-Nelly, Nadège Guiglielmoni, Susana M. Coelho, Romain Koszul, Alexandre Cormier, Komlan Avia, Christophe Zimmer, Martial Marbouty, Mie Yl, Sterck L, Lyam Baudry, Olivier Godfroy, J. M. Cock, Régulation spatiale des Génomes - Spatial Regulation of Genomes, Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Centre de Bioinformatique, Biostatistique et Biologie Intégrative (C3BI), Collège Doctoral, Sorbonne Université (SU), Laboratoire de Biologie Intégrative des Modèles Marins (LBI2M), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Station biologique de Roscoff (SBR), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Université libre de Bruxelles (ULB), Imagerie et Modélisation - Imaging and Modeling, This research was supported by funding to R.K. and S.M.C. from the European Research Council under the Horizon 2020 Program (ERC grant agreements 260822 and 638240, respectively) and from Agence Nationale pour la Recherche (JPI-EC-AMR STARCS ANR-16-JPEC-0003-05) to R.K. This project has received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No 764840, ANR-16-JPEC-0003,STARCS,Selection and Transmission of Antimicrobial Resistance in Complex Systems(2016), European Project: 260822,EC:FP7:ERC,ERC-2010-StG_20091118,DICIG(2011), European Project: 638240,H2020,ERC-2014-STG,SEXSEA(2015), European Project: 764840,IGNITE, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), and Collège doctoral [Sorbonne universités]
Subjects: Scaffold, MCMC, Computer science, media_common.quotation_subject, [SDV]Life Sciences [q-bio], GPU, Sequence assembly, Locus (genetics), Computational biology, Hi-C scaffolding, Genome, 03 medical and health sciences, 0302 clinical medicine, Chromosome (genetic algorithm), Quality (business), 030304 developmental biology, media_common, 0303 health sciences, Contig, biology, business.industry, parallel computing, Chromosome, Ectocarpus, Modular design, biology.organism_classification, Hi-C genome assembly, Ligation, business, 030217 neurology & neurosurgery, Desmarestia herbacea
Abstract: Hi-C has become a popular technique in recent genome assembly projects. Hi-C exploits contact frequencies between pairs of loci to bridge and order contigs in draft genomes, resulting in chromosome-level assemblies. However, application of this approach is currently hampered by a lack of robust programs that are capable of effectively treating this type of data, particularly open source programs. We developed instaGRAAL, a complete overhaul of the GRAAL program, which has adapted the latter to allow efficient assembly of large genomes. Both GRAAL, and instaGRAAL use a Markov Chain Monte Carlo algorithm to perform Hi-C scaffolding, but instaGRAAL features a number of improvements including a modular polishing approach that optionally integrates independent data. To validate the program, we used it to generate chromosome-level assemblies for two brown algae, Desmarestia herbacea and the model Ectocarpus sp., and quantified improvements compared to the initial draft for the latter. Overall, instaGRAAL is a program able to generate, using default parameters with minimal human intervention, near-complete assemblies.
Published: 2019
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35. Generation of a Metagenomics Proximity Ligation 3C Library of a Mammalian Gut Microbiota

Author: Théo, Foutel-Rodier, Agnès, Thierry, Romain, Koszul, and Martial, Marbouty
Subjects: Animals, High-Throughput Nucleotide Sequencing, Metagenome, Metagenomics, Sequence Analysis, DNA, Genome, Bacterial, Gastrointestinal Microbiome
Abstract: Microbial species thrive in very diverse environments and play fundamental roles in their equilibrium and dynamics. Metagenomics consists in extracting, sequencing, and studying the DNA present in ecosystems to better understand their regulation. Ideally, the maximal amount of information would be gathered from the full sequences of the genomes, episomes, and phages present in the microbial communities. Current high-throughput DNA sequencing produces reads ranging in size from a few dozen base pairs for the most commonly used technologies to several kb for emerging single-molecule real-time sequencing techniques. Although valuable information can be extracted from processing these DNA sequences into contigs, reconstructing full genomes remains a difficult task. Clustering contigs according to their similarities or read coverage covariations gives some insights on these genomes, but remains limited as viral sequences, or recent horizontal gene transfers, often differ from their host genomes. We recently developed meta3C, a proximity ligation approach that bins contigs in a sequence-independent way by quantifying and exploiting their tridimensional collisions frequencies in vivo. This technique has demonstrated a great potential to reconstruct genomes as well as to assign plasmids and phages to their hosts. It nevertheless requires a specific processing of the microbial samples before sequencing, which has to be carefully planned.
Published: 2018

36. Correction to: Proximity ligation scaffolding and comparison of two Trichoderma reesei strains genomes

Author: Antoine Margeot, Etienne Jourdier, Frédérique Bidard, Martial Marbouty, Dante Poggi-Parodi, Lyam Baudry, Yoan Vicq, and Romain Koszul
Subjects: 0106 biological sciences, 0301 basic medicine, Renewable Energy, Sustainability and the Environment, lcsh:Biotechnology, Computational biology, Management, Monitoring, Policy and Law, Biology, biology.organism_classification, 01 natural sciences, Applied Microbiology and Biotechnology, Genome, lcsh:Fuel, 03 medical and health sciences, 030104 developmental biology, General Energy, lcsh:TP315-360, Chromosome (genetic algorithm), Fragment (logic), lcsh:TP248.13-248.65, 010608 biotechnology, Ligation, Gene, Trichoderma reesei, Biotechnology
Abstract: Following publication of the original article [1], the authors reported a problem in the drawing of Rut-C30 chromosome III in Fig. 2B of the original article [1]. The two fragments of chromosome I inserted inside chromosome III should be swapped, and the direction of the fragment containing rim101 and cel1a genes should be inverted. This reversed insertion indicates that at least 2 rearrangements occurred simultaneously, so the possible scenario proposed in Fig. 2C of the original article was inaccurate. The corrected figure with modified panels B and C is available in the figure below. The detailed description of Rut-C30 assembly in the Additional file 5 of the original article is correct.
Published: 2018
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37. Multiscale Structuring of the E. coli Chromosome by Nucleoid-Associated and Condensin Proteins

Author: Frédéric Boccard, Axel Cournac, Virginia S. Lioy, Romain Koszul, Olivier Espéli, Stéphane Duigou, Martial Marbouty, Julien Mozziconacci, Conformation et Ségrégation du chromosome bactérien (OCB), Département Biologie des Génomes (DBG), 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)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-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)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Régulation spatiale des Génomes - Spatial Regulation of Genomes, Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Laboratoire de Physique Théorique de la Matière Condensée (LPTMC), Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS), Centre interdisciplinaire de recherche en biologie (CIRB), Labex MemoLife, École normale supérieure - Paris (ENS-PSL), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Collège de France (CdF (institution))-Ecole Superieure de Physique et de Chimie Industrielles de la Ville de Paris (ESPCI Paris), Université Paris sciences et lettres (PSL)-École normale supérieure - Paris (ENS-PSL), Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), This research was supported by funding from the European Research Council under the 7th Framework Program (FP7/2007-2013, ERC Grant Agreement 260822 to R.K.), by the Agence Nationale pour la Recherche (HiResBac ANR-15-CE11-0023-03 to R.K., O.E., and J.M.), by the Fondation pour la Recherche Médicale (to V.S.L.), and by the Agence Nationale pour la Recherche (ANR-12-BSV8-0020-01 to F.B.)., ANR-15-CE11-0023,HiResBaCS,Structure des chromosomes bactériens revélée a haute résolution(2015), European Project: 260822,EC:FP7:ERC,ERC-2010-StG_20091118,DICIG(2011), Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), École normale supérieure - Paris (ENS Paris), and Université Paris sciences et lettres (PSL)-École normale supérieure - Paris (ENS Paris)
Subjects: 0301 basic medicine, MESH: Chromosomes, Bacterial, MESH: Protein Structure, Quaternary, Chromosomal Proteins, Non-Histone, DBG, Condensin, [SDV]Life Sciences [q-bio], MESH: Escherichia coli Proteins, Bacterial genome size, Origin of replication, Genome, General Biochemistry, Genetics and Molecular Biology, MESH: Escherichia coli K12, 03 medical and health sciences, 0302 clinical medicine, HU, Hi-C, MESH: Chromosomal Proteins, Non-Histone, MESH: Adenosine Triphosphatases, Nucleoid, genome organization, Protein Structure, Quaternary, bacteria, Genetics, Adenosine Triphosphatases, OCB, biology, Escherichia coli K12, SMC, Circular bacterial chromosome, Escherichia coli Proteins, Chromosome, Chromosomes, Bacterial, MESH: Multiprotein Complexes, MatP, DNA-Binding Proteins, Repressor Proteins, 030104 developmental biology, MESH: Repressor Proteins, Multiprotein Complexes, biology.protein, chromatin, Nucleoid organization, 030217 neurology & neurosurgery, MESH: DNA-Binding Proteins
Abstract: International audience; As in eukaryotes, bacterial genomes are not randomly folded. Bacterial genetic information is generally carried on a circular chromosome with a single origin of replication from which two replication forks proceed bidirectionally toward the opposite terminus region. Here, we investigate the higher-order architecture of the Escherichia coli genome, showing its partition into two structurally distinct entities by a complex and intertwined network of contacts: the replication terminus (ter) region and the rest of the chromosome. Outside of ter, the condensin MukBEF and the ubiquitous nucleoid-associated protein (NAP) HU promote DNA contacts in the megabase range. Within ter, the MatP protein prevents MukBEF activity, and contacts are restricted to ∼280 kb, creating a domain with distinct structural properties. We also show how other NAPs contribute to nucleoid organization, such as H-NS, which restricts short-range interactions. Combined, these results reveal the contributions of major evolutionarily conserved proteins in a bacterial chromosome organization.
Published: 2018
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38. Functional Partition of a Bacterial Chromosome Through the Interplay of Nucleoid Associated Proteins and Condensin

Author: Olivier Espéli, Romain Koszul, Virginia S. Lioy, Frédéric Boccard, Stéphane Duigou, Axel Cournac, Martial Marbouty, and Julien Mozziconacci
Subjects: Circular bacterial chromosome, Condensin, Chromosome, Biology, medicine.disease_cause, Origin of replication, Cell biology, chemistry.chemical_compound, chemistry, medicine, biology.protein, Nucleoid, Nucleoid organization, Escherichia coli, DNA
Abstract: Bacterial genetic information is generally carried on a single circular chromosome with a unique origin of replication from which two replication forks proceeds bidirectionaly to the opposite terminus region. Here we investigated the higher-order genome architecture of the of the model bacteria Escherichia coli. We show that the chromosome is partitioned into two structuraly distinct entities through a complex and intertwined network of contacts: the replication terminus (ter) region and the rest of the chromosome. Outside ter, the condensin MukBEF and the ubiquitous nucleoid-associated protein (NAP) HU promote contacts in the megabase range. Within ter, the MatP protein prevents MukBEF activity and contacts are restricted to ~280 kb creating a domain with unique structural properties. We also show how other NAPs contribute to nucleoid organization, such as H-NS that constrains and insulate DNA segments. Combined, these results reveal the contributions of major, evolutionary conserved proteins in a bacterial chromosome organization.
Published: 2018
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39. Generation of a Metagenomics Proximity Ligation 3C Library of a Mammalian Gut Microbiota

Author: Romain Koszul, Théo Foutel-Rodier, Agnès Thierry, Martial Marbouty, Régulation spatiale des Génomes - Spatial Regulation of Genomes, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Centre de Bioinformatique, Biostatistique et Biologie Intégrative (C3BI), Sorbonne Université (SU), and Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS)
Subjects: 0301 basic medicine, MESH: Sequence Analysis, DNA, Base pair, Assembly, Computational biology, Biology, MESH: Genome, Bacterial, Genome, Human gut, DNA sequencing, MESH: Gastrointestinal Microbiome, 03 medical and health sciences, 0302 clinical medicine, Plasmid, Meta Hi-C, Metagenomics binning, MESH: Animals, Microbiome, Gene, MESH: High-Throughput Nucleotide Sequencing, Meta3C, Contig, MESH: Metagenome, 030104 developmental biology, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, Metagenomics, MESH: Metagenomics, 030217 neurology & neurosurgery
Abstract: International audience; Microbial species thrive in very diverse environments and play fundamental roles in their equilibrium and dynamics. Metagenomics consists in extracting, sequencing, and studying the DNA present in ecosystems to better understand their regulation. Ideally, the maximal amount of information would be gathered from the full sequences of the genomes, episomes, and phages present in the microbial communities. Current high-throughput DNA sequencing produces reads ranging in size from a few dozen base pairs for the most commonly used technologies to several kb for emerging single-molecule real-time sequencing techniques. Although valuable information can be extracted from processing these DNA sequences into contigs, reconstructing full genomes remains a difficult task. Clustering contigs according to their similarities or read coverage covariations gives some insights on these genomes, but remains limited as viral sequences, or recent horizontal gene transfers, often differ from their host genomes. We recently developed meta3C, a proximity ligation approach that bins contigs in a sequence-independent way by quantifying and exploiting their tridimensional collisions frequencies in vivo. This technique has demonstrated a great potential to reconstruct genomes as well as to assign plasmids and phages to their hosts. It nevertheless requires a specific processing of the microbial samples before sequencing, which has to be carefully planned.
Published: 2018
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40. Metagenome Analysis Exploiting High-Throughput Chromosome Conformation Capture (3C) Data

Author: Romain Koszul, Martial Marbouty, Régulation spatiale des Génomes - Spatial Regulation of Genomes, Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), This research was supported by funding to R.K. from the European Research Council under the 7th Framework Program (FP7/2007-2013)/ERC grant agreement 260822., European Project: 260822,EC:FP7:ERC,ERC-2010-StG_20091118,DICIG(2011), and Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS)
Subjects: Genetics, [SDV.GEN]Life Sciences [q-bio]/Genetics, MESH: High-Throughput Screening Assays, [SDV]Life Sciences [q-bio], Chromosome, Computational biology, MESH: Metagenome, Biology, Genome, Chromosomes, Article, DNA sequencing, High-Throughput Screening Assays, Chromosome conformation capture, chemistry.chemical_compound, Plasmid, chemistry, Metagenomics, Metagenome, MESH: Chromosomes, Mobile genetic elements, DNA
Abstract: Microbial communities are extremely complex and constitute critical actors of our environment. Genomic analyses of these populations are a dynamic research area but remain limited by the difficulty to assemble full genomes of individual species. Recently, a new method for metagenome assembly/analysis based on chromosome conformation capture has emerged (meta3C). This approach quantifies the collisions experienced by DNA molecules to identify those sharing the same cellular compartments, allowing the characterization of genomes present within complex mixes of species. The exploitation of these chromosome 3D signatures holds important premises regarding reaching at the genome sequences from discrete species in complex populations. It also has the potential to correctly assign extra-chromosomal elements, such as plasmids, mobile elements and phages, to their host cells.
Published: 2015
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41. Generation and Analysis of Chromosomal Contact Maps of Bacteria

Author: Martial, Marbouty and Romain, Koszul
Subjects: Bacteria, Chromosome Mapping, Nucleic Acid Conformation, Chromosomes, Bacterial
Abstract: This methods article described a protocol aiming at generating chromosome contact maps of bacterial species using a genome-wide derivative of the chromosome conformation capture (3C) technique. The approach is readily applicable on a broad variety of gram + and gram-bacterial species. It describes and addresses known caveats and technicalities associated with the technique, and should be of interest to any laboratory interested to perform a multiscale analysis of the genome structure of its species of interest.
Published: 2017

42. Generation and Analysis of Chromosomal Contact Maps of Bacteria

Author: Martial Marbouty, Romain Koszul, Régulation spatiale des Génomes - Spatial Regulation of Genomes, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), and Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS)
Subjects: 0301 basic medicine, Genetics, Chromosome conformation capture, MESH: Chromosomes, Bacterial, biology, Computer science, Chromosome, Nucleoid, Computational biology, Genome structure, biology.organism_classification, Genome organization, 03 medical and health sciences, MESH: Bacteria, 030104 developmental biology, MESH: Nucleic Acid Conformation, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, Hi-C, 3C, MESH: Chromosome Mapping, Bacteria, Genomic organization
Abstract: International audience; This methods article described a protocol aiming at generating chromosome contact maps of bacterial species using a genome-wide derivative of the chromosome conformation capture (3C) technique. The approach is readily applicable on a broad variety of gram + and gram-bacterial species. It describes and addresses known caveats and technicalities associated with the technique, and should be of interest to any laboratory interested to perform a multiscale analysis of the genome structure of its species of interest.
Published: 2017
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43. Purification of G1daughter cells from differentSaccharomycetesspecies through an optimized centrifugal elutriation procedure

Author: Romain Koszul, Bernard Dujon, Martial Marbouty, Guy-Franck Richard, and Caroline Ermont
Subjects: Genetics, 0303 health sciences, education.field_of_study, Candida glabrata, biology, Cell division, Saccharomycetes, Saccharomyces cerevisiae, Population, Bioengineering, Elutriation, biology.organism_classification, Applied Microbiology and Biotechnology, Biochemistry, Yeast, 03 medical and health sciences, 0302 clinical medicine, Lachancea kluyveri, Biological system, education, 030217 neurology & neurosurgery, 030304 developmental biology, Biotechnology
Abstract: Centrifugal elutriation discriminates cells according to their sedimentation coefficients, generating homogeneous samples well suited for genomic comparative approaches. It can, for instance, isolate G1 daughter cells from a Saccharomyces cerevisiae unsynchronized population, alleviating ageing and cell-cycle biases when conducting genome-wide/single-cell studies. The present report describes a straightforward and robust procedure to determine whether a cell population of virtually any yeast species can be efficiently elutriated, while offering solutions to optimize success. This approach was used to characterize elutriation parameters and S-phase progression of four yeast species (S. cerevisiae, Candida glabrata, Lachancea kluyveri and Pichia sorbitophila) and could theoretically be applied to any culture of single, individual cells.
Published: 2014
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44. Proximity ligation scaffolding and comparison of two

Author: Etienne, Jourdier, Lyam, Baudry, Dante, Poggi-Parodi, Yoan, Vicq, Romain, Koszul, Antoine, Margeot, Martial, Marbouty, and Frédérique, Bidard
Subjects: Correction
Abstract: The presence of low complexity and repeated regions in genomes often results in difficulties to assemble sequencing data into full chromosomes. However, the availability of full genome scaffolds is essential to several investigations, regarding for instance the evolution of entire clades, the analysis of chromosome rearrangements, and is pivotal to sexual crossing studies. In non-conventional but industrially relevant model organisms, such as the ascomyceteThe chromosome scaffolds ofThe GRAAL program allowed us to generate the karyotype of the Rut-C30 strain, and from there to predict chromosome structure for most
Published: 2016

45. A checkpoint control orchestrates the replication of the two chromosomes of Vibrio cholerae

Author: Michael J. Bland, Christophe Possoz, Romain Koszul, Didier Mazel, Martial Marbouty, Francisco de Lemos Martins, Ole Skovgaard, Marie-Eve Val, Harry Kemble, Sean Kennedy, Plasticité du Génome Bactérien - Bacterial Genome Plasticity (PGB), Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Régulation spatiale des Génomes - Spatial Regulation of Genomes, Biomics, Centre de Recherche et Innovation Technologique (CITECH), Institut Pasteur [Paris] (IP)-Institut Pasteur [Paris] (IP), Département Biologie des Génomes (DBG), 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)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Department of Science, Systems and Models, Roskilde Universitet [Roskilde], This research was funded by the Institut Pasteur, INSERM, and CNRS. This work was supported by a grant from the French National Research Agency (ANR-10-BLAN-131301). R.K. was funded by the European Research Council (FP7/2007-2013, ERC grant agreement 260822). M.M. was funded by the Association pour la Recherche sur le Cancer fellowship(20100600373). F.d.L.M. and M.J.B. were supported by the Pasteur-Paris University Program., ANR-14-CE10-0007,MAGISBAC,Génèse et maintenance des chromosomes secondaire bactériens(2014), ANR-10-BLAN-1313,BMC,Bactéries à multiple chromosomes : liens entre architecture du génome et physiologie cellulaire(2010), European Project: 260822,EC:FP7:ERC,ERC-2010-StG_20091118,DICIG(2011), Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Institut Pasteur [Paris]-Institut Pasteur [Paris], Plasticité du Génome Bactérien, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique ( CNRS ), Centre d’Innovation et Recherche Technologique ( CITECH ), Département Biologie des Génomes ( DBG ), Institut de Biologie Intégrative de la Cellule ( I2BC ), Université Paris-Saclay-Centre National de la Recherche Scientifique ( CNRS ) -Commissariat à l'énergie atomique et aux énergies alternatives ( CEA ) -Université Paris-Sud - Paris 11 ( UP11 ) -Université Paris-Saclay-Centre National de la Recherche Scientifique ( CNRS ) -Commissariat à l'énergie atomique et aux énergies alternatives ( CEA ) -Université Paris-Sud - Paris 11 ( UP11 ), ANR-14-CE10-0007,MAGISBAC,Génèse et maintenance des chromosomes secondaire bactériens ( 2014 ), ANR-10-BLAN-1313,BMC,Bactéries à multiple chromosomes : liens entre architecture du génome et physiologie cellulaire ( 2010 ), and European Project : 260822,EC:FP7:ERC,ERC-2010-StG_20091118,DICIG ( 2011 )
Subjects: 0301 basic medicine, DNA Replication, plasmids, replication, 030106 microbiology, multipartite genome, cholera, Eukaryotic DNA replication, Replication Origin, [SDV.BC]Life Sciences [q-bio]/Cellular Biology, Biology, [ SDV.MP.BAC ] Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology, Pre-replication complex, Origin of replication, Microbiology, 03 medical and health sciences, Minichromosome maintenance, Control of chromosome duplication, Bacterial Proteins, Chromosome Segregation, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, chromosome, [ SDV.BBM ] Life Sciences [q-bio]/Biochemistry, Molecular Biology, Vibrio cholerae, replication initiation, Research Articles, Vibrio, Genetics, secondary chromosome, [SDV.GEN]Life Sciences [q-bio]/Genetics, Multidisciplinary, [ SDV.BC ] Life Sciences [q-bio]/Cellular Biology, SciAdv r-articles, pathogens, Cell Cycle Checkpoints, Gene Expression Regulation, Bacterial, Chromosomes, Bacterial, D-loop replication, [SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology, 3. Good health, 030104 developmental biology, Licensing factor, Origin recognition complex, cell cycle, [ SDV.GEN ] Life Sciences [q-bio]/Genetics, Genome, Bacterial, Research Article
Abstract: Replication of a specific site on the main chromosome of V. cholerae triggers the replication initiation of its secondary chromosome., Bacteria with multiple chromosomes represent up to 10% of all bacterial species. Unlike eukaryotes, these bacteria use chromosome-specific initiators for their replication. In all cases investigated, the machineries for secondary chromosome replication initiation are of plasmid origin. One of the important differences between plasmids and chromosomes is that the latter replicate during a defined period of the cell cycle, ensuring a single round of replication per cell. Vibrio cholerae carries two circular chromosomes, Chr1 and Chr2, which are replicated in a well-orchestrated manner with the cell cycle and coordinated in such a way that replication termination occurs at the same time. However, the mechanism coordinating this synchrony remains speculative. We investigated this mechanism and revealed that initiation of Chr2 replication is triggered by the replication of a 150-bp locus positioned on Chr1, called crtS. This crtS replication–mediated Chr2 replication initiation mechanism explains how the two chromosomes communicate to coordinate their replication. Our study reveals a new checkpoint control mechanism in bacteria, and highlights possible functional interactions mediated by contacts between two chromosomes, an unprecedented observation in bacteria.
Published: 2016
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46. Generation and Analysis of Chromosomal Contact Maps of Yeast Species

Author: Axel Cournac, Romain Koszul, Julien Mozziconacci, and Martial Marbouty
Subjects: 0301 basic medicine, Genetics, Yeast artificial chromosome, Chromosome conformation capture, 03 medical and health sciences, 030104 developmental biology, biology, Saccharomyces cerevisiae, Sequence assembly, Computational biology, biology.organism_classification, Yeast, Genomic organization
Abstract: Genome-wide derivatives of the chromosome conformation capture (3C) technique are now well-established approaches to study the multiscale average organization of chromosomes from bacteria to mammals. However, the experimental parameters of the protocol have to be optimized for different species, and the downstream experimental products (i.e., pair-end sequences) are influenced by these parameters. Here, we describe a complete pipeline to generate 3C-seq libraries and compute chromosomal contact maps of yeast species.
Published: 2016
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47. Evidence for actin dual role in regulating chromosome organization and dynamics in yeast

Author: Maya Spichal, Martial Marbouty, Axel Cournac, Alice Brion, Sébastien Herbert, Christophe Zimmer, Romain Koszul, and Emmanuelle Fabre
Subjects: 0301 basic medicine, biology, Arp2/3 complex, Actin remodeling, macromolecular substances, Cell Biology, Cell biology, Chromosome conformation capture, 03 medical and health sciences, 030104 developmental biology, Profilin, biology.protein, Actin-binding protein, MDia1, Nuclear pore, Cytoskeleton
Abstract: Eukaryotic chromosomes undergo movements that are involved in the regulation of functional processes such as DNA repair. To better understand the origin of these movements, we used fluorescence microscopy, image analysis and chromosome conformation capture to quantify the actin contribution to chromosome movements and interactions in budding yeast. We show that both the cytoskeletal and nuclear actin drive local chromosome movements, independently of Csm4, a putative LINC protein. Inhibition of actin polymerization reduces subtelomere dynamics, resulting in more confined territories and enrichment in subtelomeric contacts. Artificial tethering of actin to nuclear pores increased both nuclear pore complex (NPC) and subtelomere motion. Chromosome loci that were positioned away from telomeres exhibited reduced motion in the presence of an actin polymerization inhibitor but were unaffected by the lack of Csm4. We further show that actin was required for locus mobility that was induced by targeting the chromatin-remodeling protein Ino80. Correlated with this, DNA repair by homologous recombination was less efficient. Overall, interphase chromosome dynamics are modulated by the additive effects of cytoskeletal actin through forces mediated by the nuclear envelope and nuclear actin, probably through the function of actin in chromatin-remodeling complexes.
Published: 2016
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48. ZipN, an FtsA-like orchestrator of divisome assembly in the model cyanobacteriumSynechocystisPCC6803

Author: Corinne Cassier-Chauvat, Cyril Saguez, Martial Marbouty, and Franck Chauvat
Subjects: chemistry.chemical_classification, Microbial Viability, biology, Cell growth, Synechocystis, Mutagenesis (molecular biology technique), biology.organism_classification, Microbiology, Cell biology, Green fluorescent protein, Amino acid, Chloroplast, Bacterial Proteins, chemistry, Protein Interaction Mapping, Mutagenesis, Site-Directed, biology.protein, Immunoprecipitation, Cloning, Molecular, FtsA, FtsZ, Molecular Biology, Cytokinesis
Abstract: We pursued the characterization of the divisome of the spherical-celled cyanobacterium Synechocystis PCC6803, through deletion, site-directed mutagenesis, GFP tagging, two-hybrid and co-immunoprecipitation assays. We presently report that the DivIVA-like protein Cdv3 is essential to both cell growth and division, whereas the AmiC, AmpH, FtsE, FtsN, SpoIID, YlmD, YlmE and YlmG proteins are dispensable. With the exception of the self-interacting protein YlmD, none of these dispensable factors appeared to interact with ZipN, the crucial cytokinetic factor we previously characterized. By contrast, we found that ZipN interacts with itself and the self-interacting protein Cdv3, as well as with all other crucial cytokinetic factors we previously characterized, namely: FtsZ, FtsI, FtsQ, SepF and ZipS. We also identified ZipN amino acids selectively involved in ZipN interaction with one of its following partners, Cdv3, FtsQ or SepF. Finally, we found no direct interaction between Cdv3, SepF and ZipS. Collectively, these results indicate that ZipN is a central player of divisome assembly in cyanobacteria, similarly to the FtsA protein of E. coli that is absent in cyanobacteria and chloroplast.
Published: 2009
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49. Meta3C analysis of a mouse gut microbiome

Author: Romain Koszul, Axel Cournac, Lyam Baudry, and Martial Marbouty
Subjects: Genetics, 0303 health sciences, Circular bacterial chromosome, Human microbiome, Sequence assembly, Genomics, Bacteria Present, Computational biology, Biology, Gut flora, biology.organism_classification, Complex ecosystem, Gut microbiome, 03 medical and health sciences, 0302 clinical medicine, 030217 neurology & neurosurgery, 030304 developmental biology
Abstract: Microbial populations as well as they biochemical activities are important components of environmental ecosystems, including the human microbiome. Deciphering the genomic content of these complex mixes of species is an important challenge but is essential to fully understand the regulation of their ecological balance. Here we apply meta3C, an experimental and computational approach that exploits the physical contacts between chromosomes to characterize large genomic regions of bacterial species mixed together, on a truly complex ecosystem: the mouse gut microbiota. Meta3C, which was initially described and applied onto controlled mixes of microorganisms, allowed the de novo assembly and scaffolding of numerous bacteria present into this natural mix. Importantly, the scaffolds analyzed exhibit the structural properties expected from typical bacterial chromosomes. Meta3C therefore paves the way to the in-depth analysis of genomic structuration of complex populations.
Published: 2015
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50. Spatial reorganization of telomeres in long-lived quiescent cells

Author: Angela Taddei, Antoine Hocher, Romain Koszul, Julien Mozziconacci, Martial Marbouty, Axel Cournac, Cyrille Billaudeau, Myriam Ruault, Micol Guidi, Isabelle Loïodice, Dynamique du noyau, Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut Curie [Paris]-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Génétique des génomes - Genetics of Genomes (UMR 3525), Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Régulation spatiale des Génomes - Spatial Regulation of Genomes, Laboratoire de Physique Théorique de la Matière Condensée (LPTMC), Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS), HAL-UPMC, Gestionnaire, Centre National de la Recherche Scientifique (CNRS)-Institut Curie [Paris]-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Pierre et Marie Curie - Paris 6 (UPMC), Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), and Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)
Subjects: Genetics, [SDV.GEN]Life Sciences [q-bio]/Genetics, Research, Centromere, Saccharomyces cerevisiae, [SDV.GEN] Life Sciences [q-bio]/Genetics, Telomere, Biology, biology.organism_classification, Resting Phase, Cell Cycle, Genome, Carbon, Chromatin, Chromosome conformation capture, [SDV.BBM] Life Sciences [q-bio]/Biochemistry, Molecular Biology, Gene silencing, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, Chromosomes, Fungal, Reactive Oxygen Species, Gene, Silent Information Regulator Proteins, Saccharomyces cerevisiae
Abstract: Background The spatiotemporal behavior of chromatin is an important control mechanism of genomic function. Studies in Saccharomyces cerevisiae have broadly contributed to demonstrate the functional importance of nuclear organization. Although in the wild yeast survival depends on their ability to withstand adverse conditions, most of these studies were conducted on cells undergoing exponential growth. In these conditions, as in most eukaryotic cells, silent chromatin that is mainly found at the 32 telomeres accumulates at the nuclear envelope, forming three to five foci. Results Here, combining live microscopy, DNA FISH and chromosome conformation capture (HiC) techniques, we report that chromosomes adopt distinct organizations according to the metabolic status of the cell. In particular, following carbon source exhaustion the genome of long-lived quiescent cells undergoes a major spatial re-organization driven by the grouping of telomeres into a unique focus or hypercluster localized in the center of the nucleus. This change in genome conformation is specific to quiescent cells able to sustain long-term viability. We further show that reactive oxygen species produced by mitochondrial activity during respiration commit the cell to form a hypercluster upon starvation. Importantly, deleting the gene encoding telomere associated silencing factor SIR3 abolishes telomere grouping and decreases longevity, a defect that is rescued by expressing a silencing defective SIR3 allele competent for hypercluster formation. Conclusions Our data show that mitochondrial activity primes cells to group their telomeres into a hypercluster upon starvation, reshaping the genome architecture into a conformation that may contribute to maintain longevity of quiescent cells. Electronic supplementary material The online version of this article (doi:10.1186/s13059-015-0766-2) contains supplementary material, which is available to authorized users.
Published: 2015
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