Cooperation and cheating orchestrate Vibrio assemblages and polymicrobial synergy in oysters infected with OsHV-1 virus
Polymicrobial diseases significantly impact the health of humans and animals but remain understudied in natural systems. We recently described the Pacific Oyster Mortality Syndrome (POMS), a polymicrobial disease that impacts oyster production and is prevalent worldwide. Analysis of POMS-infected oy...
Published in: | Proceedings of the National Academy of Sciences |
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National Academy of Sciences
2023
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Online Access: | https://archimer.ifremer.fr/doc/00840/95232/102978.pdf https://archimer.ifremer.fr/doc/00840/95232/102979.pdf https://archimer.ifremer.fr/doc/00840/95232/105276.pdf https://archimer.ifremer.fr/doc/00840/95232/105277.pdf https://doi.org/10.1073/pnas.2305195120 https://archimer.ifremer.fr/doc/00840/95232/ |
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ftarchimer:oai:archimer.ifremer.fr:95232 2023-12-10T09:51:42+01:00 Cooperation and cheating orchestrate Vibrio assemblages and polymicrobial synergy in oysters infected with OsHV-1 virus Oyanedel, Daniel Lagorce, Arnaud Bruto, Maxime Haffner, Philippe Morot, Amandine Dorant, Yann De La Forest Divonne, Sebastien Delavat, François Inguimbert, Nicolas Montagnani, Caroline Morga, Benjamin Toulza, Eve Chaparro, Cristian Escoubas, Jean-michel Labreuche, Yannick Gueguen, Yannick Vidal Dupiol, Jeremie De Lorgeril, Julien Petton, Bruno Degremont, Lionel Tourbiez, Delphine Pimparé, Léa-lou Leroy, Marc Romatif, Oceane Pouzadoux, Juliette Mitta, Guillaume Roux, Frédérique Le Charrière, Guillaume M. Travers, Agnes Destoumieux-garzón, Delphine 2023-10 application/pdf https://archimer.ifremer.fr/doc/00840/95232/102978.pdf https://archimer.ifremer.fr/doc/00840/95232/102979.pdf https://archimer.ifremer.fr/doc/00840/95232/105276.pdf https://archimer.ifremer.fr/doc/00840/95232/105277.pdf https://doi.org/10.1073/pnas.2305195120 https://archimer.ifremer.fr/doc/00840/95232/ eng eng National Academy of Sciences https://archimer.ifremer.fr/doc/00840/95232/102978.pdf https://archimer.ifremer.fr/doc/00840/95232/102979.pdf https://archimer.ifremer.fr/doc/00840/95232/105276.pdf https://archimer.ifremer.fr/doc/00840/95232/105277.pdf doi:10.1073/pnas.2305195120 https://archimer.ifremer.fr/doc/00840/95232/ info:eu-repo/semantics/openAccess restricted use Proceedings Of The National Academy Of Sciences Of The United States Of America (0027-8424) (National Academy of Sciences), 2023-10 , Vol. 120 , N. 40 , P. e23051951 (12p.) microbiota mollusk immune suppression T3SS iron uptake text Article info:eu-repo/semantics/article 2023 ftarchimer https://doi.org/10.1073/pnas.2305195120 2023-11-14T23:51:09Z Polymicrobial diseases significantly impact the health of humans and animals but remain understudied in natural systems. We recently described the Pacific Oyster Mortality Syndrome (POMS), a polymicrobial disease that impacts oyster production and is prevalent worldwide. Analysis of POMS-infected oysters on the French North Atlantic coast revealed that the disease involves co-infection with the endemic ostreid herpesvirus 1 (OsHV-1) and virulent bacterial species such asVibrio crassostreae. However, it is unknown whether consistentVibriopopulations are associated with POMS in different regions, howVibriocontribute to POMS, and how they interact with the OsHV-1 virus during pathogenesis. We resolved theVibriopopulation structure in oysters from a Mediterranean ecosystem and investigated their functions in POMS development. We find thatVibrio harveyiandVibrio rotiferianusare the predominant species found in OsHV-1-diseased oysters and show that OsHV-1 is necessary to reproduce the partition of theVibriocommunity observed in the field. By characterizing the interspecific interactions between OsHV-1,V. harveyiandV. rotiferianus, we find that onlyV. harveyisynergizes with OsHV-1. When co-infected, OsHV-1 andV. harveyibehave cooperatively by promoting mutual growth and accelerating oyster death.V. harveyishowed high virulence potential in oysters and dampened host cellular defenses, making oysters a more favorable niche for microbe colonization. We next investigated the interactions underlying the co-occurrence of diverseVibriospecies in diseased oysters. We found thatV. harveyiharbors genes responsible for the biosynthesis and uptake of a key siderophore called vibrioferrin. This important resource promotes the growth ofV. rotiferianus, a cheater that efficiently colonizes oysters during POMS without costly investment in host manipulation nor metabolite sharing. By connecting field-based approaches, laboratory infection assays and functional genomics, we have uncovered a web of interdependencies that shape the ... Article in Journal/Newspaper North Atlantic Pacific oyster Archimer (Archive Institutionnelle de l'Ifremer - Institut français de recherche pour l'exploitation de la mer) Pacific Proceedings of the National Academy of Sciences 120 40 |
institution |
Open Polar |
collection |
Archimer (Archive Institutionnelle de l'Ifremer - Institut français de recherche pour l'exploitation de la mer) |
op_collection_id |
ftarchimer |
language |
English |
topic |
microbiota mollusk immune suppression T3SS iron uptake |
spellingShingle |
microbiota mollusk immune suppression T3SS iron uptake Oyanedel, Daniel Lagorce, Arnaud Bruto, Maxime Haffner, Philippe Morot, Amandine Dorant, Yann De La Forest Divonne, Sebastien Delavat, François Inguimbert, Nicolas Montagnani, Caroline Morga, Benjamin Toulza, Eve Chaparro, Cristian Escoubas, Jean-michel Labreuche, Yannick Gueguen, Yannick Vidal Dupiol, Jeremie De Lorgeril, Julien Petton, Bruno Degremont, Lionel Tourbiez, Delphine Pimparé, Léa-lou Leroy, Marc Romatif, Oceane Pouzadoux, Juliette Mitta, Guillaume Roux, Frédérique Le Charrière, Guillaume M. Travers, Agnes Destoumieux-garzón, Delphine Cooperation and cheating orchestrate Vibrio assemblages and polymicrobial synergy in oysters infected with OsHV-1 virus |
topic_facet |
microbiota mollusk immune suppression T3SS iron uptake |
description |
Polymicrobial diseases significantly impact the health of humans and animals but remain understudied in natural systems. We recently described the Pacific Oyster Mortality Syndrome (POMS), a polymicrobial disease that impacts oyster production and is prevalent worldwide. Analysis of POMS-infected oysters on the French North Atlantic coast revealed that the disease involves co-infection with the endemic ostreid herpesvirus 1 (OsHV-1) and virulent bacterial species such asVibrio crassostreae. However, it is unknown whether consistentVibriopopulations are associated with POMS in different regions, howVibriocontribute to POMS, and how they interact with the OsHV-1 virus during pathogenesis. We resolved theVibriopopulation structure in oysters from a Mediterranean ecosystem and investigated their functions in POMS development. We find thatVibrio harveyiandVibrio rotiferianusare the predominant species found in OsHV-1-diseased oysters and show that OsHV-1 is necessary to reproduce the partition of theVibriocommunity observed in the field. By characterizing the interspecific interactions between OsHV-1,V. harveyiandV. rotiferianus, we find that onlyV. harveyisynergizes with OsHV-1. When co-infected, OsHV-1 andV. harveyibehave cooperatively by promoting mutual growth and accelerating oyster death.V. harveyishowed high virulence potential in oysters and dampened host cellular defenses, making oysters a more favorable niche for microbe colonization. We next investigated the interactions underlying the co-occurrence of diverseVibriospecies in diseased oysters. We found thatV. harveyiharbors genes responsible for the biosynthesis and uptake of a key siderophore called vibrioferrin. This important resource promotes the growth ofV. rotiferianus, a cheater that efficiently colonizes oysters during POMS without costly investment in host manipulation nor metabolite sharing. By connecting field-based approaches, laboratory infection assays and functional genomics, we have uncovered a web of interdependencies that shape the ... |
format |
Article in Journal/Newspaper |
author |
Oyanedel, Daniel Lagorce, Arnaud Bruto, Maxime Haffner, Philippe Morot, Amandine Dorant, Yann De La Forest Divonne, Sebastien Delavat, François Inguimbert, Nicolas Montagnani, Caroline Morga, Benjamin Toulza, Eve Chaparro, Cristian Escoubas, Jean-michel Labreuche, Yannick Gueguen, Yannick Vidal Dupiol, Jeremie De Lorgeril, Julien Petton, Bruno Degremont, Lionel Tourbiez, Delphine Pimparé, Léa-lou Leroy, Marc Romatif, Oceane Pouzadoux, Juliette Mitta, Guillaume Roux, Frédérique Le Charrière, Guillaume M. Travers, Agnes Destoumieux-garzón, Delphine |
author_facet |
Oyanedel, Daniel Lagorce, Arnaud Bruto, Maxime Haffner, Philippe Morot, Amandine Dorant, Yann De La Forest Divonne, Sebastien Delavat, François Inguimbert, Nicolas Montagnani, Caroline Morga, Benjamin Toulza, Eve Chaparro, Cristian Escoubas, Jean-michel Labreuche, Yannick Gueguen, Yannick Vidal Dupiol, Jeremie De Lorgeril, Julien Petton, Bruno Degremont, Lionel Tourbiez, Delphine Pimparé, Léa-lou Leroy, Marc Romatif, Oceane Pouzadoux, Juliette Mitta, Guillaume Roux, Frédérique Le Charrière, Guillaume M. Travers, Agnes Destoumieux-garzón, Delphine |
author_sort |
Oyanedel, Daniel |
title |
Cooperation and cheating orchestrate Vibrio assemblages and polymicrobial synergy in oysters infected with OsHV-1 virus |
title_short |
Cooperation and cheating orchestrate Vibrio assemblages and polymicrobial synergy in oysters infected with OsHV-1 virus |
title_full |
Cooperation and cheating orchestrate Vibrio assemblages and polymicrobial synergy in oysters infected with OsHV-1 virus |
title_fullStr |
Cooperation and cheating orchestrate Vibrio assemblages and polymicrobial synergy in oysters infected with OsHV-1 virus |
title_full_unstemmed |
Cooperation and cheating orchestrate Vibrio assemblages and polymicrobial synergy in oysters infected with OsHV-1 virus |
title_sort |
cooperation and cheating orchestrate vibrio assemblages and polymicrobial synergy in oysters infected with oshv-1 virus |
publisher |
National Academy of Sciences |
publishDate |
2023 |
url |
https://archimer.ifremer.fr/doc/00840/95232/102978.pdf https://archimer.ifremer.fr/doc/00840/95232/102979.pdf https://archimer.ifremer.fr/doc/00840/95232/105276.pdf https://archimer.ifremer.fr/doc/00840/95232/105277.pdf https://doi.org/10.1073/pnas.2305195120 https://archimer.ifremer.fr/doc/00840/95232/ |
geographic |
Pacific |
geographic_facet |
Pacific |
genre |
North Atlantic Pacific oyster |
genre_facet |
North Atlantic Pacific oyster |
op_source |
Proceedings Of The National Academy Of Sciences Of The United States Of America (0027-8424) (National Academy of Sciences), 2023-10 , Vol. 120 , N. 40 , P. e23051951 (12p.) |
op_relation |
https://archimer.ifremer.fr/doc/00840/95232/102978.pdf https://archimer.ifremer.fr/doc/00840/95232/102979.pdf https://archimer.ifremer.fr/doc/00840/95232/105276.pdf https://archimer.ifremer.fr/doc/00840/95232/105277.pdf doi:10.1073/pnas.2305195120 https://archimer.ifremer.fr/doc/00840/95232/ |
op_rights |
info:eu-repo/semantics/openAccess restricted use |
op_doi |
https://doi.org/10.1073/pnas.2305195120 |
container_title |
Proceedings of the National Academy of Sciences |
container_volume |
120 |
container_issue |
40 |
_version_ |
1784897466260258816 |