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

Type Article
Date 2020-04
Language English
Author(s) Dupont Samuel1, Lokmer A.2, Corre E.3, Auguet Jean-Christophe4, Petton Bruno5, Toulza E.13, Montagnani Caroline1, Tanguy G.6, Pecqueur D.7, Salmeron C.7, Guillou L.8, Desnues C.9, 10, La Scola B.11, 12, Bou Khalil J.12, de Lorgeril JulienORCID1, Mitta Guillaume13, Gueguen YannickORCID1, Escoubas Jean Michel14
Affiliation(s) 1 : IHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Montpellier, Univ. Perpignan Via Domitia, 34095, Montpellier, France
2 : Coastal Ecology, Wadden Sea Station Sylt, Alfred Wegener Institute - Helmholtz Centre for Polar and Marine Research, List auf Sylt, German
3 : Sorbonne Université, CNRS, FR2424 ABiMS (Analysis and Bioanalysis for Marine Sciences), Station Biologique de Roscoff SBR, 29680, Roscoff, France
4 : MARBEC, Université Montpellier, CNRS, IFREMER, IRD, CC093, place Eugène Bataillon, 34095, Montpellier, France
5 : Ifremer, LEMAR UMR 6539, 11 presqu’île du Vivier, 29840, Argenton-en-Landunvez, France
6 : Sorbonne Université, CNRS, FR2424, Genomer, Station Biologique de Roscoff SBR, 29680, Roscoff, France
7 : Observatoire Océanologique de Banyuls sur Mer, FR 3724, BioPIC, CNRS/SU, Avenue Pierre Fabre, 66650, Banyuls-sur-Mer, France
8 : Sorbonne Université, CNRS, UMR7144 Adaptation et Diversité en Milieu Marin, Ecology of Marine Plankton (ECOMAP), Station Biologique de Roscoff SBR, 29680, Roscoff, France
9 : Aix-Marseille Université, IRD 257, Assistance-Publique des Hôpitaux de Marseille, UMR Microbes, Evolution, Phylogeny and Infections (MEPHI), IHU Méditerranée Infection, 13005, Marseille, France
10 : Aix-Marseille Université, Université de Toulon, CNRS, IRD, Mediterranean Institute of Oceanography, UM 110, 13288, Marseille, France
11 : Microbes, Evolution, Phylogeny and Infection (MEΦI), Aix-Marseille Université UM63, Institut de Recherche pour le Développement IRD 198, Assistance Publique – Hôpitaux de Marseille (AP-HM), Marseille, France
12 : Institut Hospitalo-Universitaire (IHU) - Méditerranée Infection, Marseille, France
13 : IHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Montpellier, Univ. Perpignan Via Domitia, 34095, Montpellier, France
14 : IHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Montpellier, Univ. Perpignan Via Domitia, 34095, Montpellier, France
Source Animal Microbiome (2524-4671) (Springer Science and Business Media LLC), 2020-04 , Vol. 2 , N. 1 , P. 12 (16p.)
DOI 10.1186/s42523-020-00032-w
WOS© Times Cited 3
Keyword(s) Oyster genetic background, Hemolymph microbiota dynamics, Early-life microbiota, Trans-kingdom interactions, Crassostrea gigas, Within-host ecosystem
Abstract

Background

The 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.

Results

We 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.

Conclusion

Our 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 seems that the three microbiome components respond independently to environmental conditions, better characterization of hemolymph-associated viruses could change this picture.

Full Text
File Pages Size Access
Publisher's official version 16 2 MB Open access
Additional file 1: Table S1. Overview of specificity of primers used to amplify V1-V2 region of 18S rRNA genes. 49 KB Open access
Additional file 2: Table S2. Bacteria OUT table with sequence tag count per sample and taxonomic affiliations. 5 MB Open access
Additional file 3: Table S3. Protist OUT table with sequence tag count per sample and taxonomic affiliations. 521 KB Open access
Additional file 4: Table S 4. Viral contig table with sequence tag count per sample and taxonomic affiliations. 13 MB Open access
Additional file 5: Figure S1. Sample rarefaction curves of alpha diversity indices for bacterial (a) and protists (b) datasets. 995 KB Open access
Additional file 6: Table S5. Orthogonal contrasts used to examine the differences between the oyster families. 14 KB Open access
Additional file 7: Table S6. Indicator taxa for the oyster environment, family origin and phenotype. 173 KB Open access
Additional file 8: Table S7. Generalized least squares by maximum likelihood linear models testing for differences in alpha diversity between the seawater and hemolymph microbiota within each environm 16 KB Open access
Additional file 9: Table S8. Generalized least squares by maximum likelihood linear models testing for differences in alpha diversity between the families in the hatchery. 14 KB Open access
Additional file 10: Table S9. Permanova based on Bray-Curtis dissimilarities testing for differences in beta diversity between the families in the hatchery. 12 KB Open access
Additional file 11: Table S10. Linear mixed-effects models testing for effects of the environment, genitors’ origin, selection pressure and their interactions on alpha diversity. 18 KB Open access
Additional file 12: Table S11. Permanova based on Bray-Curtis dissimilarities testing for effects of the environment, genitors’ origin and selection pressure and their interactions on beta diversity. 13 KB Open access
Additional file 13: Table 12. Permanova based on Bray-Curtis dissimilarities testing for differences in beta diversity between the families in the infectious environment. 12 KB Open access
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How to cite 

Dupont Samuel, Lokmer A., Corre E., Auguet Jean-Christophe, Petton Bruno, Toulza E., Montagnani Caroline, Tanguy G., Pecqueur D., Salmeron C., Guillou L., Desnues C., La Scola B., Bou Khalil J., de Lorgeril Julien, Mitta Guillaume, Gueguen Yannick, Escoubas Jean Michel (2020). Oyster hemolymph is a complex and dynamic ecosystem hosting bacteria, protists and viruses. Animal Microbiome, 2(1), 12 (16p.). Publisher's official version : https://doi.org/10.1186/s42523-020-00032-w , Open Access version : https://archimer.ifremer.fr/doc/00627/73916/