Microbial methane oxidizers in permafrost thawing ponds, Siberia

High-latitude ecosystems are strongly affected by climate change. Accelerated thawing of permanently frozen soils (permafrost) generates ponds, lakes and wetlands, which are major sources of biogenic methane emissions. With its high warming potential, methane constitutes a positive feedback on global warming. Global changes may disrupt the methane cycle by affecting the metabolic pathways, kinetics, abundances and community composition of the microbial key players involved in methane production and consumption. Surveying the microbial diversity and functionalities in these ecosystems is essential for a better understanding of their potential feedback to climate change. In this study, methane cycling was investigated in four glaciar lakes under thermokarst influence in Igarka, Northern Siberian Arctic (discontinuous permafrost). Biogeochemical analyses (dissolved gases concentration, stable isotopes) along the water column profiles demonstrated that methane oxidation occurred mainly in the anoxic layer of the lakes. In some cases, it could totally mitigate the methane produced deeper in the lake sediment. DNA was extracted from superficial sediment and water samples at different depths. The quantification of mcrA and pmoA gene (functional marker of methanogeny and methanotrophy) and the analysis of bacterial and archaeal diversity by 16S amplicon sequencing (Illumina MiSeq) revealed that the same Methylomonadaceae-members, including Methylobacter and Crenothrix, were the major contributors of methane oxidation in the anoxic water of the four lakes under study. This result raises the question of how these supposedly aerobic methanotrophs can carry out an oxic reaction in fully anoxic waters. Our study highlighted the importance of potential metabolic partners identified in these anaerobic methane oxidation (AOM) layers and co-occurring with the methanotrophs, such as iron-reducers (Rhodoferax, Geothrix and Geobacter) and iron oxidizers (Galionella). The reduction of iron oxides might consume the electrons resulting from methane oxidation. This study provides insight into an anaerobic oxidation process highly relevant for methane emission mitigation.