Unraveling microbe-mediated degradation of lignin and lignin-derived aromatic fragments in the Pearl River Estuary sediments

Abstract

Estuaries are one of the most crucial areas for the transformation and burial of terrestrial organic carbon (TerrOC), playing an important role in the global carbon cycle. While the transformation and degradation of TerrOC are mainly driven by microorganisms, the specific taxa and degradation processes involved remain largely unknown in estuaries. We collected surface sediments from 14 stations along the longitudinal section of the Pearl River Estuary (PRE), P. R. China. By combining analytical chemistry, metagenomics, and bioinformatics methods, we analyzed composition, source and degradation pathways of lignin/lignin-derived aromatic fragments and their potential decomposers in these samples. A diversity of bacterial and archaeal taxa, mostly those from Proteobacteria (Deltaproteobacteria, Gammaproteobacteria etc.), including some lineages (e.g., Nitrospria, Polyangia, Tectomicrobia_uc) not previously implicated in lignin degradation, were identified as potential polymeric lignin or its aromatic fragments degraders. The abundance of lignin degradation pathways genes exhibited distinct spatial distribution patterns with the area adjacent to the outlet of Modaomen as a potential degradation hot zone and the Syringyl lignin fragments, 3,4-PDOG, and 4,5-PDOG pathways as the primary potential lignin aromatic fragments degradation processes. Notably, the abundance of ferulic acid metabolic pathway genes exhibited significant correlations with degree of lignin oxidation and demethylation/demethoxylization and vegetation source. Additionally, the abundance of 2,3-PDOG degradation pathways genes also showed a positive significant correlation with degree of lignin oxidation. Our study provides a meaningful insight into the microbial ecology of TerrOC degradation in the estuary.

Keywords: Degradation pathways; Estuarine ecosystem; Lignin; Terrestrial organic carbon.