Microbial carbon degradation and methanogenesis in wetland soils
generate a large proportion of atmospheric methane, a highly potent greenhouse
gas. Despite their potential to mitigate greenhouse gas emissions, knowledge about
methane-consuming methanotrophs is often limited to lower-resolution single-gene
surveys that fail to capture the taxonomic and metabolic diversity of these microorganisms
in soils. Here our objective was to use genome-enabled approaches to investigate
methanotroph membership, distribution, and in situ activity across spatial
and seasonal gradients in a freshwater wetland near Lake Erie. 16S rRNA gene analyses
demonstrated that members of the methanotrophic Methylococcales were dominant,
with the dominance largely driven by the relative abundance of four taxa, and
enriched in oxic surface soils. Three methanotroph genomes from assembled soil
metagenomes were assigned to the genus Methylobacter and represented the most
abundant methanotrophs across the wetland. Paired metatranscriptomes confirmed
that these Old Woman Creek (OWC) Methylobacter members accounted for nearly all
the aerobic methanotrophic activity across two seasons. In addition to having the
capacity to couple methane oxidation to aerobic respiration, these new genomes
encoded denitrification potential that may sustain energy generation in soils with
lower dissolved oxygen concentrations. We further show that Methylobacter members
that were closely related to the OWC members were present in many other
high-methane-emitting freshwater and soil sites, suggesting that this lineage could
participate in methane consumption in analogous ecosystems. This work contributes
to the growing body of research suggesting that Methylobacter may represent critical
mediators of methane fluxes in freshwater saturated sediments and soils worldwide.
