Methane cycling microorganisms drive seasonal variation of methane emission in mangrove ecosystems

Coastal mangroves are one of the significant hotspots of natural methane (CH₄) emissions, yet the seasonal dynamics of these emissions and the underlying microbial drivers remain poorly understood. A clearer understanding of these processes is critical for predicting and mitigating methane emissions from these crucial ecosystems. In this study, we conducted a seasonal investigation (from March 2021 to January 2022) in mangrove sediments of the Futian Natural Reserve. We measured in situ methane fluxes and analyzed the microbial community structure via 16S rRNA gene sequencing, metagenomics and metatranscriptomics. Our results revealed significant seasonal variations in methane emissions, with the highest rates occurring in summer. Based on relative abundance of 16S rRNA gene amplicons and methyl-coenzyme M reductase (mcrA) and particulate methane monooxygenase (pmoA) gene sequences obtained from metagenomes, we identified three dominant methanogenic lineages (hydrogenotrophic Methanomicrobiales, acetoclastic Methanosaeta and H₂-dependent methylotrophic Methanomassiliicoccales), two anaerobic methanotrophic archaea (ANME-1 and ANME-2b) and one group of aerobic methanotrophic bacteria (Methylococcaceae). Metatranscriptomic data further illuminated that the transcripts of methanogenic mcrA genes were significantly higher in summer and autumn, while the transcriptional activity of anaerobic (ANME-mcrA) and aerobic (pmoA) methanotrophs were most pronounced in autumn. Correlation analyses established a significantly negative relationship between methane emissions and salinity levels. This study highlights that salinity is a key environmental factor mediating methane emissions in mangroves, likely through suppressing methanogenic activity. Our findings thus reveal that seasonal microbial interactions regulate mangrove methane flux, providing critical insights for modeling global methane budgets and guiding climate-smart mangrove management.