Metagenomics Evidence of a Novel Thermoplasmata-like Archaeon Decomposing Heterodisulfide in Nonacidic Estuary-Ocean Sediment

Abstract

Thermoplasmata archaea, renowned for their acidophilic and thermophilic traits, have been implicated in methanogenic metabolism across diverse environments. However, their metabolic capabilities in nonacidic settings remain understudied. This metagenomic investigation unveils the microbiome dynamics and metabolic processes within nonacidic estuary-ocean sediments across 19 sites (seven groups) in the Pearl River Estuary and South China Sea regions. Remarkably, the microbiomes exhibited rapid adaptation and compositional consistency despite spatial heterogeneity, suggesting the overriding influences of salinity, pH, and nutrient availability. Metabolic pathway reconstruction revealed prevalent modules for amino acid, nucleotide, lipid, vitamin, and carbohydrate metabolism, indicating community adaptation to this environment. Additionally, the high occurrence of heterodisulfide reductase (hdrA) genes implicated potential roles in CoM-S-S-CoB degradation. Notably, we discovered a novel Thermoplasmata-like genome (MAG3 in g3) that, despite sharing core genomic traits with known Thermoplasmata, harbored distinct genetic variabilities. Phylogenetic evidence robustly affiliated the Thermoplasmata-like archaeon with methanogenesis pathways, suggesting its potential involvement in CoM-S-S-CoB degradation under nonacidic conditions. This study enhances the understanding of microbiome composition and metabolic processes and highlights the pivotal contribution of Thermoplasmata archaea to sulfur cycling within nonacidic estuarine-ocean sediments.