Permafrost regions store ~50% of global soil carbon (1). However with climate change, the permafrost carbon sink is becoming a source for microbes that may fix carbon as biomass, or release it as carbon dioxide or methane. Methane producing archaea (methanogens) in the discontinuous permafrost environment of Stordalen mire (subarctic Sweden) likely contribute to atmospheric methane levels (1). Conversely, bacterial methane-oxidizers (methanotrophs) may play an important role in controlling methane flux (1). Changes in methanotroph diversity and metabolic efficiency following a thaw progression are undetermined yet central to understanding this rapidly changing environment.
Methanotroph diversity and distribution was examined across a thaw gradient using a comprehensive dataset comprising 214 metagenomes and 24 metatranscriptomes. These data spanned triplicate samples collected at three sites, three depths and over three years. Using GraftM (2), the sequencing data and assemblies were searched for methanotrophy marker genes, specifically the particulate and soluble monooxygenases (amo/pmo/hmoCAB and mmoX). Analysis of marker genes uncovered distinct methanotroph successional and transcript expression changes as thaw progresses. Several divergent monooxygenase genes were identified in the metagenome assemblies. From these, two genomes were recovered for a perceived high-affinity methanotroph within the Beijerinckiaceae (3). Genomes with divergent monooxygenases were also recovered for a previously unknown methanotrophic member of the Hyphomicrobiaceae and two distinct Deltaproteobacteria populations.
The metagenomic and metatranscriptomic approach reveals a shift in abundance and activity of methanotrophs as permafrost thaws. Abundance and transcript expression data, combined with the recovery of novel methanotroph genomes, impacts current perspectives on the evolution of methanotrophy and the methanotroph community in a climate critical thaw environment.
This work is supported by the U.S. Department of Energy under funding opportunity announcement number DE-FOA-0000866. Pathways to carbon liberation: a systems approach to understanding carbon transformations and losses from thawing permafrost.