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

Coastal areas are responsible for over 75% of global marine methane emissions and this proportion is predicted to grow due to an increase in anthropogenically induced eutrophication and deoxygenation. Prolonged periods of low oxygen and high organic matter input have been put forward to cause an imbalanced microbial methane cycle, as methane oxidation cannot keep up with methane production. However, it is still unclear what factors affect each process and which microorganisms are responsible. Here we show that methanogenic processes dominate microbial methane cycling in the anoxic sediments of marine Lake Grevelingen (NL) after summer stratification with bottom water anoxia. We observed a shallow and narrow sulfate-methane transition zone between 5 and 15 cm depth, with high methane concentrations (> 5 mM) below this zone. Methanogenesis was dominant over methanotrophy in all investigated layers as active methanogenesis potential was detected down to 60 cm below sea floor, but methane oxidation was only observed in a narrow section of the sulfate-methane transition zone. Based on amplicon sequencing and sediment incubations, we uncovered a metabolically and phylogenetically diverse methanogenic community with distinct niche separation in different sediment layers. ANME archaea and their putative syntrophic sulfate-reducing bacteria were restricted to a narrow zone and were co-occurring with the detected methane oxidation activity. Our results suggest that eutrophication and deoxygenation will further contribute to rising methane emissions in coastal areas, as the microbial methane cycle will be tilted towards increased methanogenesis while the efficiency of the microbial methane filter is expected to decline.