Cooperation and cheating orchestrate Vibrio assemblages and polymicrobial synergy in oysters infected with OsHV-1 virus

Type Article
Date 2023-10
Language English
Author(s) Oyanedel Daniel12, Lagorce Arnaud1, Bruto Maxime2, 3, Haffner Philippe1, Morot Amandine4, 5, Dorant Yann1, de La Forest Divonne Sebastien12, Delavat François6, Inguimbert Nicolas7, Montagnani CarolineORCID1, Morga BenjaminORCID8, Toulza Eve12, Chaparro Cristian12, Escoubas Jean-Michel12, Labreuche Yannick2, Gueguen YannickORCID1, 9, Vidal Dupiol JeremieORCID1, de Lorgeril JulienORCID1, 10, Petton BrunoORCID2, 4, Degremont LionelORCID8, Tourbiez Delphine8, Pimparé Léa-Lou12, Leroy Marc12, Romatif Oceane1, Pouzadoux Juliette1, Mitta GuillaumeORCID11, 12, Roux Frédérique Le2, 3, Charrière Guillaume M.12, Travers AgnesORCID1, Destoumieux-Garzón DelphineORCID12
Affiliation(s) 1 : IHPE, Université de Montpellier, CNRS, Ifremer, Université de Perpignan. Montpellier, France
2 : Ifremer, Unité Physiologie Fonctionnelle des Organismes Marins, ZI de la Pointe du Diable, Plouzané, France
3 : Sorbonne Université, UPMC Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, Roscoff cedex, France
4 : Université de Bretagne Occidentale, CNRS, IRD, Ifremer, LEMAR, F-29280 Plouzané, France
5 : Université de Bretagne-Sud, EA 3884, LBCM, IUEM, F-56100 Lorient, France
6 : Nantes Université, CNRS, US2B, UMR6286, F-44000 Nantes, France
7 : CRIOBE, USR EPHE-UPVD-CNRS 3278, Université de Perpignan Via Domitia, 58 Avenue Paul Alduy, 66860 Perpignan, France
8 : Ifremer, ASIM, Adaptation Santé des invertébrés, La Tremblade, France
9 : MARBEC, Univ Montpellier, CNRS, Ifremer, IRD, Sète, France
10 : Ifremer, IRD, Univ Nouvelle-Calédonie, Univ La Réunion, ENTROPIE, F-98800, Nouméa, Nouvelle-Calédonie, France
11 : Ifremer, Université de Polynésie Française, IRD, ILM, EIO, Polynésie Française
12 : IHPE, Université de Montpellier, CNRS, Ifremer, Université de Perpignan. Montpellier, France
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.)
DOI 10.1073/pnas.2305195120
Note This article is a preprint and has not been certified by peer review
Keyword(s) microbiota, mollusk, immune suppression, T3SS, iron uptake
Abstract

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 structure and function of the POMS pathobiota. We showed that cooperative behaviors contribute to synergy between bacterial and viral co-infecting partners. Additional cheating behaviors further shape the polymicrobial consortium. Controlling such behaviors or countering their effects opens new avenues for mitigating polymicrobial diseases.

Licence CC-BY-NC-ND
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Preprint - 10.1101/2023.02.11.528104 38 2 MB Open access
Supplementary material preprint 24 1 MB Open access
Publisher's official version 12 5 MB Open access
Appendix 01 23 1 MB Open access
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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). Cooperation and cheating orchestrate Vibrio assemblages and polymicrobial synergy in oysters infected with OsHV-1 virus. Proceedings Of The National Academy Of Sciences Of The United States Of America, 120(40), e23051951 (12p.). Publisher's official version : https://doi.org/10.1073/pnas.2305195120 , Open Access version : https://archimer.ifremer.fr/doc/00840/95232/