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

Author

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

Published
2021
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16. Colocalization and potential interactions of Endozoicomonas and chlamydiae in microbial aggregates of the coral Pocillopora acuta

Author

Maire, Justin, primary, Tandon, Kshitij, additional, Collingro, Astrid, additional, van de Meene, Allison, additional, Damjanovic, Katarina, additional, Gotze, Cecilie Ravn, additional, Stephenson, Sophie, additional, Philip, Gayle K., additional, Horn, Matthias, additional, Cantin, Neal E., additional, Blackall, Linda L., additional, and van Oppen, Madeleine J. H., additional

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

Author

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

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

Author

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

Published
2023
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21. Endozoicomonas-chlamydiae interactions in cell-associated microbial aggregates of the coralPocillopora acuta

Author

Maire, Justin, primary, Tandon, Kshitij, additional, Collingro, Astrid, additional, van de Meene, Allison, additional, Damjanovic, Katarina, additional, Gøtze, Cecilie Ravn, additional, Stephenson, Sophie, additional, Philip, Gayle K., additional, Horn, Matthias, additional, Cantin, Neal E., additional, Blackall, Linda L., additional, and van Oppen, Madeleine J. H., additional

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

Author

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

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

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

Published
2023
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28. The genome of the cereal pest Sitophilus oryzae : a transposable element haven

Author

Parisot, Nicolas, Vargas-Chavez, Carlos, Goubert, Clément, Baa-Puyoulet, Patrice, Balmand, Séverine, Beranger, Louis, Blanc, Caroline, Bonnamour, Aymeric, Boulesteix, Matthieu, Burlet, Nelly, Calevro, Federica, Callaerts, Patrick, Chancy, Théo, Charles, Hubert, Colella, Stefano, Da Silva Barbosa, André, Dell’Aglio, Elisa, Di Genova, Alex, Febvay, Gérard, Gabaldon, Toni, Galvão Ferrarini, Mariana, Gerber, Alexandra, Gillet, Benjamin, Hubley, Robert, Hughes, Sandrine, Jacquin-Joly, Emmanuelle, Maire, Justin, Marcet-Houben, Marina, Masson, Florent, Meslin, Camille, Montagne, Nicolas, Moya, Andrés, Ribeiro de Vasconcelos, Ana Tereza, Richard, Gautier, Rosen, Jeb, Sagot, Marie-France, Smit, Arian F.A., Storer, Jessica, Vincent-Monegat, Carole, Vallier, Agnès, Vigneron, Aurélien, Zaidman-Remy, Anna, Zamoum, Waël, Vieira, Cristina, Rebollo, Rita, Latorre, Amparo, Heddi, Abdelaziz, Biologie Fonctionnelle, Insectes et Interactions (BF2I), Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Centre for Genomic Regulation [Barcelona] (CRG), Universitat Pompeu Fabra [Barcelona] (UPF)-Centro Nacional de Analisis Genomico [Barcelona] (CNAG), and Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)

Subjects
[SDV.GEN.GA]Life Sciences [q-bio]/Genetics/Animal genetics, [SDV]Life Sciences [q-bio], [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], food and beverages
Abstract

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

Published
2021

31. The genome of the cereal pest Sitophilus oryzae: a transposable element haven

Author

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

Published
2021
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32. Long-Term Heat Selection of the Coral Endosymbiont Cladocopium C1 acro (Symbiodiniaceae) Stabilizes Associated Bacterial Communities.

Author

Buerger, Patrick, Vanstone, Ruby T., Maire, Justin, and van Oppen, Madeleine J. H.

Subjects
BACTERIAL communities, CORALS, HIGH temperatures, GENETIC barcoding, METAGENOMICS, COMMUNITIES
Abstract

Heat-tolerant strains of the coral endosymbiont, Cladocopium C1acro (Symbiodiniaceae), have previously been developed via experimental evolution. Here, we examine physiological responses and bacterial community composition (using 16S rRNA gene metabarcoding) in cultures of 10 heat-evolved (SS) and 9 wild-type (WT) strains, which had been exposed for 6 years to 31 °C and 27 °C, respectively. We also examine whether the associated bacterial communities were affected by a three-week reciprocal transplantation to both temperatures. The SS strains had bacterial communities with lower diversities that showed more stability and lower variability when exposed to elevated temperatures compared with the WT strains. Amplicon sequence variants (ASVs) of the bacterial genera Labrenzia, Algiphilus, Hyphobacterium and Roseitalea were significantly more associated with the SS strains compared with the WT strains. WT strains showed higher abundance of ASVs assigned to the genera Fabibacter and Tropicimonas. We hypothesize that these compositional differences in associated bacterial communities between SS and WT strains also contribute to the thermal tolerance of the microalgae. Future research should explore functional potential between bacterial communities using metagenomics to unravel specific genomic adaptations. [ABSTRACT FROM AUTHOR]

Published
2022
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34. Evaluating the essentiality of the primary endosymbiont of the rice weevil Sitophilus oryzae through genome analysis

Author

Vargas-Chavez, Carlos, Parisot, Nicolas, Goubert, C., Baa-Puyoulet, Patrice, Balmand, Severine, Boulesteix, M., Burlet, Nelly, Callaerts, Patrick, Charles, Hubert, Colella, Stefano, Febvay, Gérard, Gabaldon, Toni, Jacquin-Joly, Emmanuelle, Loska, Damian, Maire, Justin, MASSON, Florent, Meslin, Camille, montagné, N, Moya, Andres, Vincent-Monégat, Carole, Rebollo, Rita, Vallier, Agnès, Vigneron, Aurélien, Zaidman-Rémy, A., Calevro, Federica, Vieira, Cristina, Latorre, Amparo, Heddi, Abdelaziz, Charles, Hubert, Biologie Fonctionnelle, Insectes et Interactions (BF2I), Institut National de la Recherche Agronomique (INRA)-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA), Eléments transposables, évolution, populations, Département génétique, interactions et évolution des génomes [LBBE] (GINSENG), Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Catholic University of Leuven - Katholieke Universiteit Leuven (KU Leuven), Laboratoire des symbioses tropicales et méditerranéennes (UMR LSTM), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Université Montpellier 1 (UM1)-Institut de Recherche pour le Développement (IRD)-Institut National de la Recherche Agronomique (INRA)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Unité de recherche Productions végétales (CRAG ANT PROD V), Institut National de la Recherche Agronomique (INRA), Barcelona Supercomputing Center - Centro Nacional de Supercomputacion (BSC - CNS), Institut d'écologie et des sciences de l'environnement de Paris (iEES), Institut National de la Recherche Agronomique (INRA)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12)-Centre National de la Recherche Scientifique (CNRS), Barcelona Institute of Science and Technology (BIST), Department ofComputationaland Systems Biology, University of Pittsburgh (PITT), Pennsylvania Commonwealth System of Higher Education (PCSHE)-Pennsylvania Commonwealth System of Higher Education (PCSHE), Institut Cavanilles de Biodiversitat i Biologia Evolutiva (ICBiBE), Universitat de València (UV), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Institut d'Ecologie et des Sciences de l'Environnement de Paris, Institut National de la Recherche Agronomique (INRA)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut de Recherche pour le Développement (IRD [France-Ouest])-Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12)-Centre National de la Recherche Scientifique (CNRS)-Ecole Normale Supérieure Paris-Saclay (ENS Paris Saclay), Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut de Recherche pour le Développement (IRD)-Université de Montpellier (UM)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), and Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)

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

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

Published
2018

35. Intracellular bacteria are common and taxonomically diverse in cultured and in hospitealgal endosymbionts of coral reefs

Author

Maire, Justin, Girvan, Sam K, Barkla, Sophie E, Perez-Gonzalez, Alexis, Suggett, David J, Blackall, Linda L, and van Oppen, Madeleine J H

Abstract

Corals house a variety of microorganisms which they depend on for their survival, including endosymbiotic dinoflagellates (Symbiodiniaceae) and bacteria. While cnidarian–microorganism interactions are widely studied, Symbiodiniaceae–bacteria interactions are only just beginning to receive attention. Here, we describe the localization and composition of the bacterial communities associated with cultures of 11 Symbiodiniaceae strains from nine species and six genera. Three-dimensional confocal laser scanning and electron microscopy revealed bacteria are present inside the Symbiodiniaceae cells as well as closely associated with their external cell surface. Bacterial pure cultures and 16S rRNA gene metabarcoding from Symbiodiniaceae cultures highlighted distinct and highly diverse bacterial communities occur intracellularly, closely associated with the Symbiodiniaceae outer cell surface and loosely associated (i.e., in the surrounding culture media). The intracellular bacteria are highly conserved across Symbiodiniaceae species, suggesting they may be involved in Symbiodiniaceae physiology. Our findings provide unique new insights into the biology of Symbiodiniaceae.

Published
2021
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36. Chlamydiae as symbionts of photosynthetic dinoflagellates

Author

Maire, Justin, Collingro, Astrid, Tandon, Kshitij, Jameson, Vanta J, Judd, Louise M, Horn, Matthias, Blackall, Linda L, and van Oppen, Madeleine J H

Abstract

Chlamydiae are ubiquitous intracellular bacteria and infect a wide diversity of eukaryotes, including mammals. However, chlamydiae have never been reported to infect photosynthetic organisms. Here, we describe a novel chlamydial genus and species, Candidatus Algichlamydia australiensis, capable of infecting the photosynthetic dinoflagellate Cladocopiumsp. (originally isolated from a scleractinian coral). Algichlamydia australiensiswas confirmed to be intracellular by fluorescence in situhybridization and confocal laser scanning microscopy and temporally stable at the population level by monitoring its relative abundance across four weeks of host growth. Using a combination of short- and long-read sequencing, we recovered a high-quality (completeness 91.73% and contamination 0.27%) metagenome-assembled genome of A. australiensis. Phylogenetic analyses show that this chlamydial taxon represents a new genus and species within the Simkaniaceaefamily. Algichlamydia australiensispossesses all the hallmark genes for chlamydiae–host interactions, including a complete type III secretion system. In addition, a type IV secretion system is encoded on a plasmid and has previously been observed for only three other chlamydial species. Twenty orthologous groups of genes are unique to A. australiensis, one of which is structurally similar to a protein known from Cyanobacteriaand Archaeplastida involved in thylakoid biogenesis and maintenance, hinting at potential chlamydiae interactions with the chloroplasts of Cladocopiumcells. Our study shows that chlamydiae infect dinoflagellate symbionts of cnidarians, the first photosynthetic organism reported to harbor chlamydiae, thereby expanding the breadth of chlamydial hosts and providing a new contribution to the discussion around the role of chlamydiae in the establishment of the primary plastid.

Published
2024
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