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...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences
Main Authors: 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
Format: Article in Journal/Newspaper
Language:English
Published: National Academy of Sciences 2023
Subjects:
microbiota
mollusk
immune suppression
T3SS
iron uptake
Pacific
North Atlantic
Pacific oyster
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/
Description
Summary: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 ...

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