Terrestrial mud volcanoes are surface geological features where fluidized sediments and gasses from the subsurface are discharged along a fracture network providing a window into the deep biosphere. Although mud volcanoes constitute an important source of methane emission from natural environments, their microbial communities responsible for methane cycling remain poorly characterized. Using a metagenomics approach, we investigated the taxonomic composition and metabolic potential of microbial communities in three active mud volcanoes in the Kerch-Taman mud volcanic province. Despite the volcanoes’ close proximity their microbial communities strongly differ. In the Kmv1 and Kmv2 volcanoes surface horizons mostly harbored organotrophic microbial communities, while the relative abundance of anaerobic methanotrophic archaea (ANME) increased with depth. The deep horizons (1.5 m) of Kmv1 were dominated by
Ca.
Methanoperedenaceae that lacked nitrate reductase and could couple methane oxidation to the reduction of metal oxides, while the abundance of sulfate-reducing bacteria was low. Consistently, with higher sulfate content, the deep horizon in Kmv2 was dominated by
Ca.
Methanoperedenaceae, ANME-2a/2b clade, sulfate-reducing
Desulfobacterota
and sulfur-oxidizing
Gammaproteobacteria
. No clear depth distribution of taxa was observed in the Kmv3 volcano where microorganisms of the methane and sulfur cycles, namely, methanogens, ANME-3 clade, methanotrophic bacteria, and sulfate reducers were simultaneously detected. A high-quality genome of a member of the archaeal candidate phylum EX4484-52 within the DPANN lineage was assembled from metagenomes. This archaeon, named
Candidatus Lutivulcanarchaeum fermentans
, has complete glycolytic pathway and ATP generation mechanisms, but lacked the biosynthetic pathways for many key cellular compounds, indicating a parasitic or symbiotic lifestyle.