Salinity-driven microbial adaptation of hydrocarbon-degrading communities in coastal sediments

Salinity is a major abiotic driver of microbial diversity and metabolic function in coastal ecosystems. While its broad ecological impacts are well established, its role in shaping hydrocarbon-degrading communities and their adaptive mechanisms remains poorly understood. Here, we integrated gene- and genome-resolved metagenomics to investigate how salinity regulates the diversity, ecological interactions, and evolutionary dynamics of aerobic hydrocarbon-degrading microbes in Zhenhai Bay sediments (0.17-28.54 practical salinity units [PSU]). Across the natural salinity gradient, 10 types of hydrocarbon-degrading genes and 30 bacterial genomes spanning four phyla were identified, revealing extensive metabolic potential for the aerobic degradation of both aliphatic and aromatic hydrocarbons. The functional diversity and relative abundance of these genes increased significantly with salinity, accompanied by strong correlations with organic carbon parameters and nitrogen availability. Co-occurrence network analyses showed that hydrocarbon degraders, particularly Gammaproteobacteria, acted as key taxa maintaining community stability under saline conditions. Comparative genomics revealed that these bacteria possess multiple halotolerance strategies, including compatible solute biosynthesis and ion transport, supported by diverse energy-generating pathways. Frequent horizontal gene transfer and duplication of alkane monooxygenases (alkB and cyp153) expanded substrate ranges and enhanced functional diversity in hydrocarbon oxidation, highlighting salinity-driven evolutionary innovation. Together, these findings demonstrate that salinity governs the structure, metabolism, and evolution of hydrocarbon-degrading microbes, promoting microbial adaptation and functional diversification in coastal sediments.IMPORTANCESalinity is a defining feature of coastal ecosystems and a major regulator of microbial processes that support carbon cycling and pollutant degradation. This study highlights that salinity plays a central role in structuring hydrocarbon-degrading microbial communities and shaping their functional capacities and evolutionary trajectories in coastal sediments. By integrating osmoadaptation, metabolic potential, and community organization, our work shows that hydrocarbon degraders function as key links between environmental conditions and ecological processes. Salinity-driven shifts in microbial networks and metabolic strategies illustrate how environmental gradients can foster resilience and stability in highly dynamic coastal systems. Beyond advancing understanding of microbial responses, this study has potential implications for the rational design of bioremediation strategies targeting hydrocarbon pollutants in saline and estuarine environments.