Introduction
The microbiome is essential for the health and resilience of marine species (Diwan et al., 2023); however, its complexity and host-specific dynamics remain poorly understood. This study presents the first comprehensive analysis of eukaryotic and prokaryotic microbiomes in three ecologically important bivalves - mussels (Mytilus galloprovincialis), clams (Ruditapes philippinarum), and cockles (Cerastoderma edule) - from a shared environment of Meira in the Ría of Vigo (NW Spain), between 2016 and 2018.
Materials and methods
The V9 (18S rRNA) and the V4 (16S rRNA) regions genes sequenced using Illumina and Ion Torrent. Alfa diversity, beta diversity (Bray-Curtis, PCoA) and PERMANOVA were used to evaluate eukaryotic and prokaryotic communities for each bivalve sample in different seasons.
Network analyses based on Spearman correlations and corrected CLR data were conducted to detect potential keystone interactions within prokaryote communities of each bivalve and its surrounding environment (mussel-water column, clam-sediment and cockle-sediment). Finally, functional activities associated with keystone taxa from each bivalve-habitat network were also identified using PICRUSt2.
Results and discussion
Each bivalve species harbored a distinct, host-specific microbiome with stable composition across seasons pointing that intrinsic host factors affect the composition of the bivalve microbiome regardless of environmental conditions and time (Neu et al., 2021)
Specific parasites, including Mytilicola intestinalis in mussels and trematodes such as Bucephalus minimus in cockles, were identified. Perkinsus olseni and Marteilia cochilia, protozoans linked to bivalve mortality and ecosystem disruption under environmental stress, were also detected.
Endozoicomonas and Vibrio dominated prokaryotic communities. A meta-analysis showed that despite the microbial diversity in the water column and sediment, each bivalve maintained its own stable and specific microbiome, distinct from its environment. These results suggest that bivalves can regulate their core microbiome through host-selective mechanisms (Brennan & Gilmore, 2018; Pierce & Ward, 2018)
We could identify Vibrio, Woeseia and Lutimonas as keystone genera shaping these microbiomes through competitive and cooperative interactions (Lu et al., 2022; Zelezniak et al., 2015). Mutualistic relationships enhanced host health via metabolic and defensive roles involving the biosynthesis of secondary metabolites.
Conclusions
Understanding host-microbe-environment interactions, particularly concerning pathogens, underscores the importance of improving ecosystem resilience and sustainability. These findings provide essential insights into microbiome dynamics, offering valuable perspectives for ecosystem and bivalve health monitoring and management.
References
Brennan, J. J., & Gilmore, T. D. (2018). Evolutionary Origins of Toll-like Receptor Signaling. Molecular Biology and Evolution, 35(7), 1576-1587. https://doi.org/10.1093/molbev/msy050
Diwan, A., Harke, S. N., & Panche, A. (Eds.). (2023). Microbiome of Finfish and Shellfish. Springer Nature Singapore. https://doi.org/10.1007/978-981-99-0852-3
Lu, L., Tang, Q., Li, H., & Li, Z. (2022). Damming river shapes distinct patterns and processes of planktonic bacterial and microeukaryotic communities. Environmental Microbiology, 24(4), 1760-1774. https://doi.org/10.1111/1462-2920.15872
Neu, A. T., Hughes, I. V., Allen, E. E., & Roy, K. (2021). Decade‐scale stability and change in a marine bivalve microbiome. Molecular Ecology, 30(5), 1237-1250. https://doi.org/10.1111/mec.15796
Pierce, M. L., & Ward, J. E. (2018). Microbial Ecology of the Bivalvia, with an Emphasis on the Family Ostreidae. Journal of Shellfish Research, 37(4), 793-806. https://doi.org/10.2983/035.037.0410
Zelezniak, A., Andrejev, S., Ponomarova, O., Mende, D. R., Bork, P., & Patil, K. R. (2015). Metabolic dependencies drive species co-occurrence in diverse microbial communities. Proceedings of the National Academy of Sciences, 112(20), 6449-6454. https://doi.org/10.1073/pnas.1421834112