Microbial assemblages in the active layer of thawing permafrost were investigated over two years across a spatially related thaw gradient. This is the first massive pyrosequencing project to investigate, document and compare the microbial community of such systems. In situ measurements of geochemical parameters enabled linkage of the community dynamics to significant shifts in C (carbon) balance and community structure. The study investigated communities from a palsa mire with three internal sites selected that were representative of distinct stages of permafrost degradation. The pristine stage of permafrost, here called ‘palsa’, was represented by the raised section of a palsa, a periglacial geomorphological form with intact permafrost and tundra vegetation. The end stage of thaw was represented by a thermokarst feature with open water and graminoid vegetation sunken several meters below the palsa in which no permafrost exists and here called ‘fen’. The intermediate thawing stage, here classified as ‘bog’, was an actively subsiding karst with a perched water table covered by a sphagnum lawn.
The community membership of each site was distinct with few commonalities at the operational taxonomic unit (OTU) level. Microbial assemblage structure in the palsa and fen samples had high diversity, richness, and evenness supporting ecological theories of climax communities. The level of novelty, percentage of singletons and number of OTUs that could only be classified at order or higher taxonomic level was high. The palsa site had typical soil and permafrost microbes being dominated by Acidobacteria and Proteobacteria. The structure of microbial assemblages within the bog varied with depth becoming highly dominated with loss of richness and diversity typically associated with ecosystems undergoing disturbance or succession processes. Archaea, especially Methanogens, dominated the bog and fen being most abundant nearest the water table. A shift from mostly hydrogenotrophic methanogens in the acidic ombrotrophic bog to methanogens capable of utilising acetate in the minerotrophic fen samples was distinct and supported by C isotope signatures.
Increased thawing of permafrost, a significant global C sink, makes cryo-sequestered C available for microbial degradation. Methanogenic Archaea convert this C to the potent greenhouse gas methane. The discovery of a novel methanogen of the RCII archaeal lineage at up to 70% abundance of the community allowed recovery of a population genome. The environmentally recovered genome and proteome of this archaea, 'Candidatus Methanoflorens stordalenmirensis', indicates that hydrogenotrophic methanogenesis is its main energy conservation pathway. Enrichment of C storage and membrane associated genes support 'Ca. M. stordalenmirensis' genomic adaption to its active layer environment. Meta-analysis of community surveys, 16S rRNA and mcrA genes, suggested that ‘Methanoflorens spp.’ are dominant and ubiquitous methanogens in permafrost and peatland soils. This lineage had previously been identified as significant in temperate peatlands but was thought to be a negligible contributor to methanogenesis at high latitudes.