Successional action of Bacteroidota and Firmicutes in decomposing straw polymers in a paddy soil

Abstract

Abstract Background Decomposition of plant biomass is vital for carbon cycling in terrestrial ecosystems. In waterlogged soils including paddy fields and natural wetlands, plant biomass degradation generates the largest natural source of global methane emission. However, the intricate process of plant biomass degradation by diverse soil microorganisms remains poorly characterized. Here we report a chemical and metagenomic investigation into the mechanism of straw decomposition in a paddy soil. Results The chemical analysis of 16-day soil microcosm incubation revealed that straw decomposition could be divided into two stages based on the dynamics of methane, short chain fatty acids, dissolved organic carbon and monosaccharides. Metagenomic analysis revealed that the relative abundance of glucoside hydrolase (GH) encoding genes for cellulose decomposition increased rapidly during the initial stage (3–7 days), while genes involved in hemicellulose decomposition increased in the later stage (7–16 days). The increase of cellulose GH genes in initial stage was derived mainly from Firmicutes while Bacteroidota contributed mostly to the later stage increase of hemicellulose GH genes. Flagella assembly genes were prevalent in Firmicutes but scarce in Bacteroidota. Wood–Ljungdahl pathway (WLP) was present in Firmicutes but not detected in Bacteroidota. Overall, Bacteroidota contained the largest proportion of total GHs and the highest number of carbohydrate active enzymes gene clusters in our paddy soil metagenomes. The strong capacity of the Bacteroidota phylum to degrade straw polymers was specifically attributed to Bacteroidales and Chitinophagales orders, the latter has not been previously recognized. Conclusions This study revealed a collaborating sequential contribution of microbial taxa and functional genes in the decomposition of straw residues in a paddy soil. Firmicutes with the property of mobility, WLP and cellulose decomposition could be mostly involved in the initial breakdown of straw polymers, while Bacteroidota became abundant and possibly responsible for the decomposition of hemicellulosic polymers during the later stage.