Methyl-processing metabolisms play central roles in methane cycling during rice cultivation

Abstract

Rice cultivation accounts for a significant proportion of agricultural greenhouse gas (GHG) emissions, while also generating a staple food for over half of the world’s population. Under continually flooded conditions, a common agronomic practice for rice cultivation, anoxia can stimulate the enrichment of methanogenic archaea, leading to large methane fluxes. However, the development of the microbial carbon decomposition networks that provide substrates to methanogens throughout the growing season is less well understood. Here, we sampled soil and water from eight rice fields at three rice growing stages in Arkansas, USA, to identify temporal changes in methanogen populations, and their interactions with other metabolically intertwined microorganisms. Methanogen abundance and activity increased over the course of the growing season, with noted enrichment of methylotrophic methanogens at later time points. These methanogen populations were supported by an increasingly complex network of microorganisms that catalyze carbon transformations to produce methanogenic substrates. We identified extensive genomic functional potential for the processing of complex carbon to yield methylated substrates/compounds for methylotrophic methanogenesis, indicating that methylated oxygen (methyl-O) and methylated sulfur (methyl-S) compounds may support a significant fraction of methane generation. Finally, we mined existing rice cultivation datasets to reveal the conservation of specific methanogenic taxa across distinct global regions, highlighting the strong selective pressure that rice cultivation has on shaping the soil microbial communities responsible for GHG production and offering opportunities for targeted practices to mitigate GHG emissions from rice paddies.