Environmental gradients shape the hydrocarbon-degrading microbiome in two mid-Atlantic bays

ABSTRACT Hydrocarbons are recalcitrant organic matter that is released into the environment via natural and anthropogenic activities. We hypothesized that abiotic and biotic factors, including salinity, temperature, seasonality, microbial interactions, and functional redundancy, influence the abundance and activity of potential hydrocarbon degraders in the Delaware and Chesapeake Bays. We identified key genes in hydrocarbon degradation pathways in metagenomes, metatranscriptomes, and metagenome-assembled genomes (MAGs) from these estuaries. In the surface waters of both estuaries, aerobic aromatic and alkane degradation pathways predominated, with higher gene abundances observed in low-salinity spring and summer samples. Salinity significantly structured both hydrocarbon-degrading MAG abundances, alongside temperature, nitrate, and silicate concentrations, and hydrocarbon degradation gene expression, which additionally varied seasonally, with the highest relative expression of aromatic degradation genes in low-salinity samples. Catechol degradation pathways exhibited high functional redundancy, whereas the naphthalene degradation pathway showed restricted distribution. Co-expression analysis revealed that Burkholderiales displayed condition-dependent metabolic coupling, while Pseudomonadales integrated hydrocarbon degradation with fermentation and central metabolism, demonstrating complementary strategies that support multi-scale ecosystem resilience. Together, these results support our hypothesis that environmental gradients and taxon-specific metabolic strategies jointly structure the abundance and in situ activity of hydrocarbon degraders, with implications for predicting ecosystem responses to hydrocarbon inputs under changing conditions. IMPORTANCE Coastal estuaries are among the most contaminated aquatic environments on Earth, receiving continuous hydrocarbon inputs from industrial activity, urban runoff, and natural sources. Microorganisms are the primary agents of hydrocarbon breakdown in these systems, yet predicting when and where this capacity is active and how resilient it is to environmental change remains a major challenge. Using paired genomic and transcriptomic data from microbial genomes across two major mid-Atlantic estuaries, we show that hydrocarbon degradation capacity is not uniformly distributed but is instead shaped by salinity, nutrients, and seasonality in pathway-specific ways. Critically, dominant degrader taxa employ fundamentally different metabolic strategies to sustain this function across fluctuating conditions, providing a form of community-level insurance against environmental disturbance. These findings advance our ability to predict microbial hydrocarbon degradation in coastal systems and inform nature-based approaches to bioremediation under increasing climate and anthropogenic pressures.