Oyster hemolymph is a complex and dynamic ecosystem hosting bacteria, protists and viruses

• Published in: Animal Microbiome
• Main Authors: Dupont, Samuel, Lokmer, A., Corre, E., Auguet, J.-C., Petton, Bruno, Toulza, E., Montagnani, C., Tanguy, G., Pecqueur, D., Salmeron, C., Guillou, Laure, Desnues, Christelle, La Scola, B., Khalil, J., Bou, de Lorgeril, J., Mitta, G., Gueguen, Y., Escoubas, Jean-Michel
• Other Authors: Interactions Hôtes-Pathogènes-Environnements (IHPE), Université de Perpignan Via Domitia (UPVD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), Alfred-Wegener-Institut, Helmholtz-Zentrum für Polar- und Meeresforschung = Alfred Wegener Institute for Polar and Marine Research = Institut Alfred-Wegener pour la recherche polaire et marine (AWI), Helmholtz-Gemeinschaft = Helmholtz Association, Éco-Anthropologie (EA), Muséum national d'Histoire naturelle (MNHN)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité), ABiMS - Informatique et bioinformatique = Analysis and Bioinformatics for Marine Science (ABIMS), Fédération de recherche de Roscoff (FR2424), Station biologique de Roscoff = Roscoff Marine Station (SBR), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Station biologique de Roscoff = Roscoff Marine Station (SBR), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), MARine Biodiversity Exploitation and Conservation (UMR MARBEC), Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR), Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM), Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER), Observatoire océanologique de Banyuls (OOB), Adaptation et diversité en milieu marin (ADMM), Institut national des sciences de l'Univers (INSU - CNRS)-Station biologique de Roscoff = Roscoff Marine Station (SBR), ECOlogy of MArine Plankton (ECOMAP), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Institut national des sciences de l'Univers (INSU - CNRS)-Station biologique de Roscoff = Roscoff Marine Station (SBR), Microbes évolution phylogénie et infections (MEPHI), Institut de Recherche pour le Développement (IRD)-Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), Institut méditerranéen d'océanologie (MIO), Institut de Recherche pour le Développement (IRD)-Aix Marseille Université (AMU)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Toulon (UTLN)-Centre National de la Recherche Scientifique (CNRS), Institut Hospitalier Universitaire Méditerranée Infection (IHU Marseille), The present study was supported by: the DHOF program of the UMR5244/IHPE (http://ihpe.univ-perp.fr/en/ihpe-transversal-holobiont/); the Ifremer project HémoMicrobiote; EMBRC-France, whose French state funds are managed by the ANR within the Investments of the Future (ANR-10-INBS-02); the ANR projects DECIPHER (ANR-14-CE19–0023) and ENVICOPAS (ANR-15-CE35–0004); the EU funded project VIVALDI (H2020 program, n°678589); by Ifremer; CNRS, Université de Montpellier; Université de Perpignan via Domitia; by the IHU Méditerranée Infection, Marseille, France, by the French Government under the «Investissements d’avenir» program (reference: Méditerranée Infection 10-IAHU-03) and by the Région Provence-Alpes-Côte d’Azur and by the European funding FEDER PRIMI. This study is set within the framework of the “Laboratoires d’Excellences (LABEX)” TULIP (ANR-10-LABX-41)., ANR-10-INBS-0002,EMBRC-France,CENTRE NATIONAL DE RESSOURCES BIOLOGIQUES MARINES(2010), ANR-14-CE19-0023,DECIPHER,Déchiffrage des maladies multifactorielles: cas des mortalités de l'huître(2014), ANR-15-CE35-0004,ENVICOPAS,Impact des changements environnementaux sur les organismes pathogènes dans les écosystèmes côtiers(2015), ANR-11-IDEX-0002,UNITI,Université Fédérale de Toulouse(2011), European Project: 678589,H2020,H2020-SFS-2015-2,VIVALDI(2016)
• Format: Article in Journal/Newspaper
• Language: English
• Published: HAL CCSD 2020
• Subjects: Oyster genetic background; Hemolymph microbiota dynamics; Early-life microbiota; Trans-kingdom interactions; Crassostrea gigas; Within-host ecosystem; Acln; [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]; [SDE.BE]Environmental Sciences/Biodiversity and Ecology; [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology; Pacific oyster
• Online Access: https://hal.science/hal-02563300; https://hal.science/hal-02563300/document; https://hal.science/hal-02563300/file/Dupont-2020-AnimMicrob-Oyster.pdf; https://doi.org/10.1186/s42523-020-00032-w

International audience BackgroundThe impact of the microbiota on host fitness has so far mainly been demonstrated for the bacterial microbiome. We know much less about host-associated protist and viral communities, largely due to technical issues. However, all microorganisms within a microbiome potentially interact with each other as well as with the host and the environment, therefore likely affecting the host health.ResultsWe set out to explore how environmental and host factors shape the composition and diversity of bacterial, protist and viral microbial communities in the Pacific oyster hemolymph, both in health and disease. To do so, five oyster families differing in susceptibility to the Pacific oyster mortality syndrome were reared in hatchery and transplanted into a natural environment either before or during a disease outbreak. Using metabarcoding and shotgun metagenomics, we demonstrate that hemolymph can be considered as an ecological niche hosting bacterial, protist and viral communities, each of them shaped by different factors and distinct from the corresponding communities in the surrounding seawater. Overall, we found that hemolymph microbiota is more strongly shaped by the environment than by host genetic background. Co-occurrence network analyses suggest a disruption of the microbial network after transplantation into natural environment during both non-infectious and infectious periods. Whereas we could not identify a common microbial community signature for healthy animals, OsHV-1 μVar virus dominated the hemolymph virome during the disease outbreak, without significant modifications of other microbiota components.ConclusionOur study shows that oyster hemolymph is a complex ecosystem containing diverse bacteria, protists and viruses, whose composition and dynamics are primarily determined by the environment. However, all of these are also shaped by oyster genetic backgrounds, indicating they indeed interact with the oyster host and are therefore not only of transient character. Although it ...