Taxonomic diversity and functional potential of microbial communities in oyster calcifying fluid

Abstract

Creating and maintaining an appropriate chemical environment is essential for biomineralization, the process by which organisms precipitate minerals to form their shells or skeletons, yet the mechanisms involved in maintaining calcifying fluid chemistry are not fully defined. In particular, the role of microorganisms in facilitating or hindering animal biomineralization is poorly understood. Here, we investigated the taxonomic diversity and functional potential of microbial communities inhabiting oyster calcifying fluid. We used shotgun metagenomics to survey calcifying fluid microbial communities from three different oyster harvesting sites. There was a striking consistency in taxonomic composition across the three collection sites. We also observed archaea and viruses that had not been previously identified in oyster calcifying fluid. Furthermore, we identified microbial energy-conserving metabolisms that could influence the host’s calcification, including genes involved in sulfate reduction and denitrification that are thought to play pivotal roles in inorganic carbon chemistry and calcification in microbial biofilms. These findings provide new insights into the taxonomy and functional capacity of oyster calcifying fluid microbiomes, highlighting their potential contributions to shell biomineralization, and contribute to a deeper understanding of the interplay between microbial ecology and biogeochemistry that could potentially bolster oyster calcification. IMPORTANCE Previous research has underscored the influence of microbial metabolisms in carbonate deposition throughout the geological record. Despite the ecological importance of microbes to animals and inorganic carbon transformations, there have been limited studies characterizing the potential role of microbiomes in calcification by animals such as bivalves. Here, we use metagenomics to investigate the taxonomic diversity and functional potential of microbial communities in calcifying fluids from oysters collected at three different locations. We show a diverse microbial community that includes bacteria, archaea, and viruses, and we discuss their functional potential to influence calcifying fluid chemistry via reactions like sulfate reduction and denitrification. We also report the presence of carbonic anhydrase and urease, both of which are critical in microbial biofilm calcification. Our findings have broader implications in understanding what regulates calcifying fluid chemistry and consequentially the resilience of calcifying organisms to 21st century acidifying oceans.