Degradation of polymeric carbohydrates coupled with cellular motility driving microbial niche separation in the Pearl River Estuary surface sediment

Abstract

Estuaries are key areas for organic carbon cycling, where polymeric carbohydrates are abundant and chemically diverse. The recycling of these polymers by microbes depends on a variety of carbohydrate-active enzymes (CAZymes). However, it remains unclear whether other gene traits, particularly those related to cell motility toward polymeric carbohydrates, are intertwined with carbohydrate depolymerization and niche specialization in estuarine sediment soils. In this study, estuarine sediments were incubated with four prevalent polymeric carbohydrates (laminarin, fucan, cellulose, and chitin) under anaerobic conditions. Based on metagenomic analysis, we identified potential responses to the degradation and utilization of polymeric carbohydrate substrates from the perspectives of CAZymes and sugar transporters. The analysis of metagenomic gene data also revealed a positive correlation between chemotaxis and the abundance of CAZymes genes. Furthermore, metagenomes-assembled genomes (MAGs) that exhibited higher abundance in polysaccharide-treated samples compared to controls also featured elevated copies of genes involved in polysaccharide utilization loci (PULs), chemotaxis, as well as those associated with flagellar or gliding movement. SprB and CTDs associated with gliding proteins genes are essential for type IX secretion system-mediated secretion of CAZymes and gliding motility in Bacteroidota. The enhanced potential for mobility, coupled with the ability to degrade polymeric carbohydrates, may enable these bacteria to exploit nutrients beyond carbon sources, thereby potentially broadening their ecological niches.