Abstract
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 seems that the three microbiome components respond independently to environmental conditions, better characterization of hemolymph-associated viruses could change this picture.
Highlights
The impact of the microbiota on host fitness has so far mainly been demonstrated for the bacterial microbiome
Hemolymph hosts a complex microbiota different from the environment and shaped by the oyster genetic background Our results show that oyster hemolymph hosts a complex community of bacteria, protists and viruses, which differs from the microbial community in the seawater column at the OUT level (Additional file 8: Table S7), and at higher taxonomic levels (Fig. 2a-c)
Hemolymph microbiota dynamics in the context of Pacific oyster mortality syndrome To evaluate the role of hemolymph microbiota in health and disease, we further investigated the effect of oyster genetic background on β-diversity during the infectious period
Summary
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. The presence of protozoa correlates with higher diversity of the bacterial gut microbiome in humans, suggesting their potential beneficial role in the maintenance of homeostasis [3]. The human body (including the circulatory system [4, 5]) is inhabited by highly diverse viral communities that can directly or indirectly influence the balance between health and disease [6], notably through their ability to modulate microbiota by infecting both bacteria and eukaryotes [7, 8]. The role and dynamics of host-associated non-bacterial microbiotas in invertebrates is understudied, with a few exceptions like corals [10, 11], hydra [12] or some insects [13,14,15]
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