A ubiquitous and diverse methanogenic community drives microbial methane cycling in eutrophic coastal sediments

Coastal areas contribute over 75% of global marine methane emissions, a proportion predicted to increase with anthropogenic eutrophication and deoxygenation. Prolonged low oxygen and high organic matter input can disrupt the methane cycle, favoring methane production over oxidation. However, factors influencing this imbalance remain unclear. Here, we show that methanogenesis dominates microbial methane cycling in the anoxic sediments of eutrophic coastal marine Lake Grevelingen (The Netherlands) after summer stratification. A shallow sulfate-methane transition zone (SMTZ; 5-15 cm depth) was observed, with high methane concentrations below. Methane was produced in all investigated layers, while methane oxidation was restricted to the narrow SMTZ. Amplicon sequencing, metagenomics, and incubations revealed a metabolically and phylogenetically diverse methanogenic community with niche separation, and methylotrophic methanogenesis prevalent in all layers. Two clades of ANME archaea, ANME-2a/b and ANME-3, were restricted to a narrow zone together with their putative syntrophic sulfate-reducing bacteria, coinciding with the observed methane oxidation activity. Our results suggest that eutrophication and deoxygenation will further contribute to rising methane emissions, tilting the microbial methane cycle toward increased methanogenesis, and decreasing the efficiency of the microbial methane filter.