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.

Marine fuel oil (MFO) spills in tropical coastal environments are under-characterized despite increasing risk from maritime activities. Microbial and geochemical responses to the June 2024 Marine Honour MFO spill on Singapore's intertidal sediments were analyzed in real time over 185 days. Using metagenomics and hydrocarbon profiling, microbial community shifts and hydrocarbon degradation were quantified across visibly oiled (high-impact) and clean (low-impact) sites. Microbiomes at all sites adapted rapidly to the spill through increased diversity and abundance of genes encoding alkane and aromatic compound degradation, detoxification, and biosurfactant production. The dominant hydrocarbon-degrading bacteria differed markedly from those reported in other crude oil spills and in regions with different climates. Oil deposition intensity strongly influenced microbial succession and hydrocarbon-degrading gene profiles, and this reflected early toxicity constraints in heavily oiled areas. The persistence of hydrocarbon degradation genes beyond hydrocarbon detection in sediments suggested long-term functional priming may occur. The study provides novel genome-resolved insight into the microbial response to MFO pollution, advances understanding of marine environmental biodegradation, and provides urgently needed baseline data for oil spill response strategies in Southeast Asia and beyond.