You are what you eat: How nutrient availability and organic matter source dictate microbial community composition and activity in coastal anoxic sediment

Abstract:

Prokaryotes make up the majority of the biomass in sediment, where they cycle organic carbon and regulate the fluctuation of organic matter. The microbes inhabiting sediment are diverse, but the factors impacting microbial community composition are not fully understood. Our goal was to better understand the relationships between nutrient load and organic matter source with microbial community composition. We subsampled a 90 cm (~1,500 years old) sediment core from an anoxic marine basin (Blackwood Sinkhole, Bahamas) into 24 distinct stratigraphic layers. The benthos in tropical sinkholes and blue holes, which are developed from the subsurface dissolution and subsequent collapse of limestone bedrock, can be rich in organic matter derived from the overlying water column or adjacent terrestrial environment, and they can serve as a model for understanding similar processes that may be operating in offshore anoxic marine basins. The C:N ratio was used to evaluate the organic matter source composition within the sedimentary intervals (terrestrial vs phytodetritus) Using 16S rRNA gene sequencing and metagenomics, we characterized the microbial community composition, which was dominated by members of the Alphaproteobacteria, Dehalococcoidia, Gammaproteobacteria, Bathyarchaeota, and Campylobacter classes, and three different community structures occurred through time that corresponded with changes in the source of organic matter. The microbial community composition reflected these age groups and the C:N ratio was statistically correlated (p < 0.05) to the relative abundance of the microbial classes, suggesting that the source of carbon at time of deposition significantly affects the microbial community composition. Metagenomics revealed a community rich in sulfur, nitrogen and aromatic compounds metabolisms. As a proxy for microbial activity, we also measured virus-induced microbial mortality, which positively correlated with the concentration of available electron acceptors. Overall, these results showed that the source of carbon and availability of electron acceptors are drivers of the microbial community composition and activity inhabiting anoxic sediment, which could impact our understanding of global carbon cycling in sedimentary basins.