Moisture-driven redox dynamics shape oil-degrading microbiomes in tropical intertidal sands

Oil spills in tropical intertidal zones expose sandy shorelines to hydrocarbons under highly dynamic redox conditions, yet the fate of fuel oils in these systems remains poorly resolved. Here, we used replicated microcosms simulating unsaturated oxic and saturated anoxic regimes to quantify fuel oil degradation in tropical sands and applied functional metagenomics to resolve underlying microbial hydrocarbonoclastic processes. Abiotic depletion of petroleum hydrocarbons was 15-20% in oxic and anoxic sterile sand controls. Biodegradation under unsaturated oxic conditions was 3-fold higher than abiotic losses, whilst negligible (approximately 5%) biodegradation occurred in saturated anoxic sand over the 90 days, confirming a dominant role for aerobic microbial activity. Community composition diverged strongly by moisture regime, with aerobic Alphaproteobacteria and Gammaproteobacteria enriched under oxic conditions, and anaerobic sulfate-reducing lineages including Desulfobacteria and Desulfovibrionia dominating under anoxia. Functional analyses revealed a coordinated transition between dominant aerobic and anaerobic hydrocarbon degradation strategies, including terminal/biterminal oxidation versus fumarate addition pathways for alkanes, and ring cleavage versus carboxylation pathways for aromatics. Enhanced biosurfactant production potential suggested increased hydrocarbon bioavailability, facilitating efficient biodegradation across contrasting redox conditions. We further recovered 298 oil-associated bacterial genomes and characterized their repertoire of genes encoding oil hydrocarbon degradation pathways across diverse phylogenetic lineages. Together, these results demonstrate that moisture-driven redox dynamics regulate biodegradation rates, microbial succession, and functional partitioning in intertidal sediments, providing new mechanistic insight into the fate of fuel oil in tropical coastal systems.