Methylotrophic methanogenesis is a vital driver of cryptic methane cycling in sulfate-reducing sediments, yet its relative significance and dominant controls in coastal sediments remain insufficiently understood. In this study, we investigated methanogenic substrates, metabolic activity, and microbial communities to constrain the biogeochemical dynamics and key controls on methanogenesis in coastal sediments. While high methane levels reaching a maximum of 4.2 mM were present beneath the sulfate-methane transition zone (150–170 cmbsf), micromolar methane concentrations were still detected in sulfate-rich sediments, where sediment exchanges methane with the water column. Radiotracer incubations and thermodynamic analyses suggest that, in these sulfate-rich surface sediments, hydrogen-dependent methylotrophic methanogenesis possesses higher thermodynamic feasibility and metabolic activity than methyl disproportionation (methylotrophic methanogenesis). The integration of 16S rRNA gene amplicon sequencing, public global datasets, and metagenome-assembled genomes indicated that uncultured Methanofastidiosales, key hydrogen-dependent methylotrophic methanogens, are widely distributed and predominant in coastal surface sediment methanogenic communities, which can produce methane from methanol and hydrogen, demonstrating greater metabolic availability than previously reported. Organic carbon source and composition further control methanogenic pathways and activity. Sediments at the coastal site, dominated by marine organic matter (TOC: 0.6%; C/N ratio: 6.4; δ¹³C-TOC: −22‰), favored hydrogenotrophic methanogenesis. In comparison, the estuarine site with increased terrestrial organic input (TOC: 0.5%; C/N ratio: 7.4; δ¹³C-TOC: −23‰) exhibited prominent methylotrophic methanogenesis driven by methanol and trimethylamine, which contributed up to 30.2% of total methane production. Overall, these results demonstrate that coastal methanogenic activity is regulated by the source and composition of organic carbon rather than sulfate availability. Hydrogen-dependent methylotrophic methanogenesis is more prevalent in coastal surface sediments than previously recognized, and enhanced terrestrial organic input strongly stimulates sedimentary methylotrophic methanogenesis in coastal ecosystems.

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