Major trends and environmental correlates of spatiotemporal shifts in the distribution of genes compared to a biogeochemical model simulation in the Chesapeake Bay

Microorganisms mediate critical biogeochemical transformations that affect the productivity and health of aquatic ecosystems. Metagenomic sequencing can be used to identify how the taxonomic and functional potential of microbial communities change in response to environmental variables by investigating changes in microbial genes. However, few studies directly compare gene changes to biogeochemical model predictions of corresponding processes, especially in dynamic estuarine ecosystems. We aim to understand the major drivers of spatiotemporal shifts in microbial genes and genomes within the water column of the Chesapeake and highlight the largest discrepancies of these observations with model predictions. We used a previously published shotgun metagenomic dataset from multiple months, sites, and depths within Chesapeake Bay in 2017 and a metatranscriptomic dataset from 2010-2011. We compared metagenomic observations with rates predicted with a comprehensive physical-biogeochemical model of the Bay. We found the largest changes in the relative abundance of genes involved in carbon, nitrogen, and sulfur metabolism associated with variables that change with depth and season. Several genes associated with the largest changes in gene abundance are significantly correlated to corresponding modeled processes. Yet, several discrepancies in key genes were identified, such as differences between genes mediating nitrification, higher than expected abundance and expression of denitrification genes in aerobic waters, and nitrogen fixation genes in environments with relatively high ammonia but low oxygen concentrations. This study identifies processes that align with model expectations and others that require additional investigation to determine the biogeochemical consequences of these discrepancies and their impact within an important estuarine ecosystem.