Abundant and persistent sulfur-oxidizing microbial populations are responsive to hypoxia in the Chesapeake Bay.

The number, size and severity of aquatic low-oxygen dead zones are increasing worldwide. Microbial processes in low-oxygen environments have important ecosystem-level consequences, such as denitrification, greenhouse gas production and acidification. To identify key microbial processes occurring in low-oxygen bottom waters of the Chesapeake Bay, we sequenced both 16S rRNA genes and shotgun metagenomic libraries to determine the identity, functional potential and spatiotemporal distribution of microbial populations in the water column. Unsupervised clustering algorithms grouped samples into three clusters using water chemistry or microbial communities, with extensive overlap of cluster composition between methods. Clusters were strongly differentiated by temperature, salinity and oxygen. Sulfur-oxidizing microorganisms were found to be enriched in the low-oxygen bottom water and predictive of hypoxic conditions. Metagenome-assembled genomes demonstrate that some of these sulfur-oxidizing populations are capable of partial denitrification and transcriptionally active in a prior study. These results suggest that microorganisms capable of oxidizing reduced sulfur compounds are a previously unidentified microbial indicator of low oxygen in the Chesapeake Bay and reveal ties between the sulfur, nitrogen and oxygen cycles that could be important to capture when predicting the ecosystem response to remediation efforts or climate change.