Microbially driven methane and sulfur cycling processes and coupling mechanisms in mangrove sediments

Methane (CH₄) as a powerful greenhouse gas is the second largest contributor to global climate warming. Mangrove sediments are an important natural source of biogenic CH₄ with rich organic carbon (C) and diverse sulfur (S) compounds, ideally for studying CH₄ and S cycling processes and coupling mechanisms. Here we sampled mangrove sediment cores and analyzed their key microbial groups, key environmental factors and possible coupling mechanisms for CH₄ and S cycling by metagenome sequencing approaches.

Our results showed that Methanomicrobiales and Methanophagales were predominant methanogens, Methanospirareceae was a representative of anaerobic methanotrophic archaea (ANME), and Desulfobacteraceae and Desulfobulbaceae were abundant sulfate-reducing bacteria (SRB), while Ectothiorhodospiraceae, Chromatiaceae and Comamonadaceae were dominant S-oxidizers. Correlation network analysis revealed positive interactions among methanogens, ANME and SRB. Also, metagenome-assembled genome (MAG) analysis indicated interspecies hydrogen transfer and extracellular electron exchange via conductive pili, flagella, and cytochromes were potential coupling mechanisms between methanogens and SRB. ANME could form consortia with SRB by intermediate metabolites (e.g., acetate) and/or direct interspecies electron transfer (e.g., flagella, pili, cytochromes). Furthermore, methanogen MAGs encoded thiosulfate oxidation and partial sulfate reduction pathways, while the ANME MAGs possessed potentials for S disproportionation and incomplete sulfate reduction. Additionally, SO₄^2-, total sulfur, moisture content and salinity were important environmental factors affecting the microbial community structure and gene families involved in CH₄ and S cycling.

This study provides novel insights into coupling mechanisms of CH₄ and S cycling processes in mangrove sediments, having important implications for mitigating global warming.