PMID- 37751557
OWN - NLM
STAT- MEDLINE
DCOM- 20230928
LR  - 20240327
IS  - 1091-6490 (Electronic)
IS  - 0027-8424 (Print)
IS  - 0027-8424 (Linking)
VI  - 120
IP  - 40
DP  - 2023 Oct 3
TI  - Cooperation and cheating orchestrate Vibrio assemblages and polymicrobial synergy 
      in oysters infected with OsHV-1 virus.
PG  - e2305195120
LID - 10.1073/pnas.2305195120 [doi]
LID - e2305195120
AB  - Polymicrobial infections threaten the health of humans and animals but remain 
      understudied in natural systems. We recently described the Pacific Oyster 
      Mortality Syndrome (POMS), a polymicrobial disease affecting oyster production 
      worldwide. In the French Atlantic coast, the disease involves coinfection with 
      ostreid herpesvirus 1 (OsHV-1) and virulent Vibrio. However, it is unknown 
      whether consistent Vibrio populations are associated with POMS in different 
      regions, how Vibrio contribute to POMS, and how they interact with OsHV-1 during 
      pathogenesis. By connecting field-based approaches in a Mediterranean ecosystem, 
      laboratory infection assays and functional genomics, we uncovered a web of 
      interdependencies that shape the structure and function of the POMS pathobiota. 
      We show that Vibrio harveyi and Vibrio rotiferianus are predominant in 
      OsHV-1-diseased oysters and that OsHV-1 drives the partition of the Vibrio 
      community observed in the field. However only V. harveyi synergizes with OsHV-1 
      by promoting mutual growth and accelerating oyster death. V. harveyi shows 
      high-virulence potential and dampens oyster cellular defenses through a type 3 
      secretion system, making oysters a more favorable niche for microbe colonization. 
      In addition, V. harveyi produces a key siderophore called vibrioferrin. This 
      important resource promotes the growth of V. rotiferianus, which cooccurs with V. 
      harveyi in diseased oysters, and behaves as a cheater by benefiting from V. 
      harveyi metabolite sharing. Our data show that cooperative behaviors contribute 
      to synergy between bacterial and viral coinfecting partners. Additional cheating 
      behaviors further shape the polymicrobial consortium. Controlling cooperative 
      behaviors or countering their effects opens avenues for mitigating polymicrobial 
      diseases.
FAU - Oyanedel, Daniel
AU  - Oyanedel D
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
FAU - Lagorce, Arnaud
AU  - Lagorce A
AUID- ORCID: 0000-0002-7828-0300
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
FAU - Bruto, Maxime
AU  - Bruto M
AD  - Ifremer, Unite Physiologie Fonctionnelle des Organismes Marins, ZI de la Pointe 
      du Diable, Plouzane F-29280, France.
AD  - Sorbonne Universite, Universite Pierre et Marie Curie Paris 06, CNRS, UMR8227, 
      Integrative Biology of Marine Models, Station Biologique de Roscoff, Roscoff 
      F-29680, France.
FAU - Haffner, Philippe
AU  - Haffner P
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
FAU - Morot, Amandine
AU  - Morot A
AD  - Universite de Bretagne Occidentale, CNRS, Institut de recherche pour le 
      developpement (IRD), Ifremer, Laboratoire des sciences de l'environnement marin 
      (LEMAR), Plouzane, F-29280, France.
AD  - Laboratoire de Biotechnologie et Chimie Marines, Universite Bretagne Sud, EMR 
      CNRS 6076, Institut Universitaire Europeen de la Mer, Lorient F-56100, France.
FAU - Labreuche, Yannick
AU  - Labreuche Y
AUID- ORCID: 0000-0002-5265-4669
AD  - Ifremer, Unite Physiologie Fonctionnelle des Organismes Marins, ZI de la Pointe 
      du Diable, Plouzane F-29280, France.
AD  - Sorbonne Universite, Universite Pierre et Marie Curie Paris 06, CNRS, UMR8227, 
      Integrative Biology of Marine Models, Station Biologique de Roscoff, Roscoff 
      F-29680, France.
FAU - Dorant, Yann
AU  - Dorant Y
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
FAU - de La Forest Divonne, Sebastien
AU  - de La Forest Divonne S
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
FAU - Delavat, Francois
AU  - Delavat F
AUID- ORCID: 0000-0002-5985-4583
AD  - Nantes Universite, CNRS, Unite en Sciences Biologiques et Biotechnologies (US2B), 
      UMR6286, Nantes, F-44000, France.
FAU - Inguimbert, Nicolas
AU  - Inguimbert N
AUID- ORCID: 0000-0002-0309-9048
AD  - Centre de Recherches Insulaires et OBservatoire de l'Environnement (CRIOBE), 
      UAR3278, Ecole Pratique des Hautes Etudes (EPHE), Universite de Perpignan Via 
      Domitia, CNRS, Perpignan F-66860, France.
FAU - Montagnani, Caroline
AU  - Montagnani C
AUID- ORCID: 0000-0002-0861-7967
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
FAU - Morga, Benjamin
AU  - Morga B
AUID- ORCID: 0000-0002-3196-4537
AD  - Ifremer, Adaptation Sante des invertebres Marins (ASIM), La Tremblade F-17390, 
      France.
FAU - Toulza, Eve
AU  - Toulza E
AUID- ORCID: 0000-0003-2049-2279
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
FAU - Chaparro, Cristian
AU  - Chaparro C
AUID- ORCID: 0000-0002-5162-349X
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
FAU - Escoubas, Jean-Michel
AU  - Escoubas JM
AUID- ORCID: 0000-0002-6138-1148
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
FAU - Gueguen, Yannick
AU  - Gueguen Y
AUID- ORCID: 0000-0002-8749-9582
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
AD  - MARine Biodiversity, Exploitation and Conservation (MARBEC) Univ Montpellier, 
      CNRS, Ifremer, IRD, Sete F-34200, France.
FAU - Vidal-Dupiol, Jeremie
AU  - Vidal-Dupiol J
AUID- ORCID: 0000-0002-0577-2953
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
FAU - de Lorgeril, Julien
AU  - de Lorgeril J
AUID- ORCID: 0000-0002-6400-5455
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
AD  - Ifremer, IRD, Univ Nouvelle-Caledonie, Univ La Reunion, ENTROPIE, Noumea, 
      Nouvelle-Caledonie, F-98800, France.
FAU - Petton, Bruno
AU  - Petton B
AUID- ORCID: 0000-0002-4169-2811
AD  - Ifremer, Unite Physiologie Fonctionnelle des Organismes Marins, ZI de la Pointe 
      du Diable, Plouzane F-29280, France.
AD  - Universite de Bretagne Occidentale, CNRS, Institut de recherche pour le 
      developpement (IRD), Ifremer, Laboratoire des sciences de l'environnement marin 
      (LEMAR), Plouzane, F-29280, France.
FAU - Degremont, Lionel
AU  - Degremont L
AD  - Ifremer, Adaptation Sante des invertebres Marins (ASIM), La Tremblade F-17390, 
      France.
FAU - Tourbiez, Delphine
AU  - Tourbiez D
AD  - Ifremer, Adaptation Sante des invertebres Marins (ASIM), La Tremblade F-17390, 
      France.
FAU - Pimpare, Lea-Lou
AU  - Pimpare LL
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
FAU - Leroy, Marc
AU  - Leroy M
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
FAU - Romatif, Oceane
AU  - Romatif O
AUID- ORCID: 0009-0004-5182-9772
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
FAU - Pouzadoux, Juliette
AU  - Pouzadoux J
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
FAU - Mitta, Guillaume
AU  - Mitta G
AUID- ORCID: 0000-0003-1188-1467
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
AD  - Ifremer, Universite de Polynesie Francaise, IRD, Institut Louis Malarde (ILM), 
      Ecosystemes Insulaires Oceaniens (EIO), Vairao F-98719, Polynesie Francaise.
FAU - Le Roux, Frederique
AU  - Le Roux F
AD  - Ifremer, Unite Physiologie Fonctionnelle des Organismes Marins, ZI de la Pointe 
      du Diable, Plouzane F-29280, France.
AD  - Sorbonne Universite, Universite Pierre et Marie Curie Paris 06, CNRS, UMR8227, 
      Integrative Biology of Marine Models, Station Biologique de Roscoff, Roscoff 
      F-29680, France.
FAU - Charriere, Guillaume M
AU  - Charriere GM
AUID- ORCID: 0000-0002-4796-1488
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
FAU - Travers, Marie-Agnes
AU  - Travers MA
AUID- ORCID: 0000-0001-5340-7435
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
FAU - Destoumieux-Garzon, Delphine
AU  - Destoumieux-Garzon D
AUID- ORCID: 0000-0002-8793-9138
AD  - Interactions Hotes Pathogenes Environnements (IHPE), Universite de Montpellier, 
      CNRS, Ifremer, Universite de Perpignan Via Domitia, Montpellier F-34090, France.
LA  - eng
PT  - Journal Article
PT  - Research Support, Non-U.S. Gov't
DEP - 20230926
PL  - United States
TA  - Proc Natl Acad Sci U S A
JT  - Proceedings of the National Academy of Sciences of the United States of America
JID - 7505876
SB  - IM
MH  - Animals
MH  - Humans
MH  - Ecosystem
MH  - Biological Assay
MH  - *Coinfection
MH  - Cooperative Behavior
MH  - *Ostreidae
PMC - PMC10556616
OTO - NOTNLM
OT  - T3SS
OT  - immune suppression
OT  - iron uptake
OT  - microbiota
OT  - mollusk
COIS- The authors declare no competing interest.
EDAT- 2023/09/26 18:42
MHDA- 2023/09/28 06:42
PMCR- 2024/03/26
CRDT- 2023/09/26 15:43
PHST- 2023/09/28 06:42 [medline]
PHST- 2023/09/26 18:42 [pubmed]
PHST- 2023/09/26 15:43 [entrez]
PHST- 2024/03/26 00:00 [pmc-release]
AID - 202305195 [pii]
AID - 10.1073/pnas.2305195120 [doi]
PST - ppublish
SO  - Proc Natl Acad Sci U S A. 2023 Oct 3;120(40):e2305195120. doi: 
      10.1073/pnas.2305195120. Epub 2023 Sep 26.