Hydrostatic pressure drives metabolic strategies for anaerobic hydrocarbon degradation in cold seep sediments: from autonomy to syntrophic cooperation revealed by metagenomics.

Petroleum pollution poses a significant threat to marine ecosystems, extending its impact to deep-sea environments. Cold seeps represent unique deep-sea ecosystems and are natural hotspots for studying anaerobic hydrocarbon degradation, yet the specific influence of hydrostatic pressure on the microbial process remains poorly understood. In this study, we established incubation systems with sediments from the Haima cold seep, enriched with n-hexadecane and naphthalene under varying hydrostatic pressures (0.1, 5, and 11 MPa). After seven months, naphthalene degradation consistently exceeded that of n-hexadecane across all pressures, yet was suppressed under high-pressure conditions. Notably, pressure selectively shaped the community structure: Marinobacter and Desulfoscipio were enriched at 0.1 MPa, while Halomonas and Sulfitobacter maintained stable dominance under high pressure. Metagenomic analysis revealed 0.1-bin.35, a bacterium affiliated with Desulfotomaculia, as a key hydrocarbon degrader encoding self-sufficient pathways for hydrocarbon degradation and dissimilatory sulfite reduction. However, under high pressure, dominant Sulfitobacter (5-bin.13, 11-bin.4) likely relied on syntrophy with sulfate-reducing bacteria to complement its incomplete catabolic pathways for hydrocarbons. This study reveals key hydrocarbon degraders in cold seep environments, advancing our understanding of deep-sea hydrocarbon-degrading microbiomes. Moreover, it unveils a possible pressure-induced adaptation strategy from autonomous degradation to syntrophic cooperation, providing insights into their ecological significance and potential applications in deep-sea oil pollutant bioremediation.