Mapping the soil microbiome functions shaping wetland methane emissions

Abstract

Accounting for only 8% of Earth's land coverage, freshwater wetlands remain the foremost contributor to global methane emissions. Yet the microorganisms and processes underlying methane emissions from wetland soils remain poorly understood. Over a five-year period, we surveyed the microbial membership and in situ methane measurements from over 700 samples in one of the most prolific methane-emitting wetlands in the United States. We constructed a catalog of 2,502 metagenome-assembled genomes (MAGs), with nearly half of the 72 bacterial and archaeal phyla sampled containing novel lineages. Integration of these data with 133 soil metatranscriptomes provided a genome-resolved view of the biogeochemical specialization and versatility expressed in wetland soils. Centimeter-scale depth differences best explained patterns of microbial community structure and transcribed functionalities, even more so than land coverage or temporal information. Moreover, while extended flooding restructured soil redox, this perturbation failed to reconfigure the transcriptional profiles of methane cycling microorganisms, contrasting with theoretical expected responses to hydrological perturbations. Co-expression analyses coupled to depth resolved methane measurements exposed the metabolisms and trophic structures most predictive of methane hotspots. This compendium of biogeochemically-classified genomes and their spatiotemporal transcriptional patterns begins to untangle the microbial carbon, energy and nutrient processing contributing to soil methane production.