Methanotrophy across a natural permafrost thaw environment

Abstract

The fate of carbon sequestered in permafrost is a key concern for future global warming as this large carbon stock is rapidly becoming a net methane source due to widespread thaw. Methane release from permafrost is moderated by methanotrophs, which oxidise 20–60% of this methane before emission to the atmosphere. Despite the importance of methanotrophs to carbon cycling, these microorganisms are under-characterised and have not been studied across a natural permafrost thaw gradient. Here, we examine methanotroph communities from the active layer of a permafrost thaw gradient in Stordalen Mire (Abisko, Sweden) spanning three years, analysing 188 metagenomes and 24 metatranscriptomes paired with in situ biogeochemical data. Methanotroph community composition and activity varied significantly as thaw progressed from intact permafrost palsa, to partially thawed bog and fully thawed fen. Thirteen methanotroph population genomes were recovered, including two novel genomes belonging to the uncultivated upland soil cluster alpha (USCα) group and a novel potentially methanotrophic Hyphomicrobiaceae. Combined analysis of porewater δ13C-CH4 isotopes and methanotroph abundances showed methane oxidation was greatest below the oxic–anoxic interface in the bog. These results detail the direct effect of thaw on autochthonous methanotroph communities, and their consequent changes in population structure, activity and methane moderation potential.

Thaw Transitions and Redox Conditions Drive Methane Oxidation in a Permafrost Peatland

“…Our incubation results support the broad thaw patterns identified by Singleton et al (), who found high expression of pmoA , a key gene for CH 4 oxidation, in a fully thawed fen site and observed that transcripts of pmoA comprised a greater proportion of total metatranscriptome reads in a fen at Stordalen Mire than in a bog or palsa. However, unlike Singleton et al (), who observed shifts in MOB abundances within the depths we sampled in both bog and fen sites, our incubation results showed no depth differences in CH 4 oxidation rates at any thaw stage. Incubation studies that quantify potential rates of CH 4 cycling are needed to make functional assessments for metabolic insights from metagenomic approaches, as measurements of potential reaction rates can be used to validate and upscale modeling of landscape‐level C budgets.…”

“…Our incubation results reinforce previous work that suggests the expansion of sedge-dominated sites as permafrost peatlands thaw may provide a mechanism in rhizospheric oxidation that attenuates CH 4 emissions from submerged sites with high rates of methanogenesis (Preuss et al, 2013;Rupp et al, 2019;Watson et al, 1997), which stands in contrast to work that highlights the zone of aerated peat above the water table as the key site of CH 4 oxidation (Granberg et al, 1997;Sundh et al, 1994Sundh et al, , 1995. Singleton et al (2018) examined CH 4 oxidation at Stordalen Mire, using metagenome and metatranscriptome sequencing of peat from the active layer of a permafrost palsa, partially thawed bog dominated by Sphagnum spp., and a fully thawed fen dominated by E. angustifolium. Our incubation results support the broad thaw patterns identified by Singleton et al (2018), who found high expression of pmoA, a key gene for CH 4 oxidation, in a fully thawed fen site and observed that transcripts of pmoA comprised a greater proportion of total metatranscriptome reads in a fen at Stordalen Mire than in a bog or palsa.…”

“…Potential for CH 4 oxidation in reduced, low‐O 2 conditions has been observed in alpine lakes and permafrost thaw ponds, suggesting that MOB are resilient to changing oxygenation regimes (Blees et al, ; Crevecoeur et al, ). Gammaproteobacterial methanotrophs within the Methylococcaceae family have been found to be abundant and active at depth across Arctic wetland sites (Christiansen et al, ; Liebner & Wagner, ; Singleton et al, ; Tveit et al, ), indicating that they are able to oxidize CH 4 under micro‐aerobic conditions. Singleton et al () identified genes for dissimilatory nitrate and sulfate reduction in MOB genomes recovered from submerged fen samples, which allow MOB to use alternate TEAs for energy generation in low‐O 2 environments in order to utilize available O 2 for CH 4 oxidation.…”

“…Permafrost thaw in permafrost peatlands can cause palsa mounds with intact permafrost to subside into submerged fens (Malmer et al, 2005), increasing methane (CH 4 ) emissions as the water table rises above the peat surface and active layer depth and graminoid vegetation cover increase (Johnston et al, 2014;Malhotra & Roulet, 2015;Turetsky et al, 2002). These changes are associated with shifts in the abundance and activity of CH 4 -cycling microbes, including aerobic methane oxidizing bacteria (MOB; Singleton et al, 2018;Woodcroft et al, 2018). Methane oxidation may attenuate a significant fraction of potential CH 4 emissions from peatlands (Frenzel & Karofeld, 2000;Nielsen et al, 2019), and inhibition and isotopic studies indicate that 0-50% of CH 4 in northern peatlands is oxidized by aerobic MOB before emission to the atmosphere (Moosavi & Crill, 1998;Popp et al, 2000;Preuss et al, 2013).…”

Evidence for non-methanogenic metabolisms in globally distributed archaeal clades basal to the Methanomassiliicoccales

“…High-throughput sequencing of environmental DNA, metagenomic assembly of DNA sequence reads into contigs, and binning of contigs into metagenome-assembled genomes (MAGs) has provided unprecedented insights into the metabolic potential and evolutionary history of many uncultivated lineages (Hug et al , 2016; Brown et al , 2015; Woodcroft et al , 2018; Castelle et al , 2013; Crits-Christoph et al , 2018; Castelle et al , 2015; Anantharaman et al , 2016). In addition to revealing numerous new phyla, MAG analyses have identified new clades of microorganisms within longstanding phylogenetic groups, assigned biogeochemical roles to known but uncultivated lineages, and attributed new functions to diverse relatives of model prokaryotes (Graham et al , 2018; Mondav et al , 2014; Tully, 2019; Boyd et al , 2019; Solden et al , 2016; Singleton et al , 2018; Martinez et al , 2019). With these advances in sequencing technology, a more complex view of microbial evolution and metabolism has emerged.…”