Functional gene analysis and cultivation experiments predict the degradation of diverse extracellular polysaccharides by ubiquitous taxa in pustular microbial mats from Shark Bay, Western Australia

Abstract

Microbial exopolymeric substances (EPSs) form the organic, polysaccharide-rich matrix of marine microbial mats and can mediate the binding and precipitation of carbonate minerals therein. Here, we investigate the molecular ecology of carbohydrate degradation and production in pustular mats from Shark Bay, Western Australia, by analyzing 84 metagenome-assembled genomes (MAGs) and the composition of microbial communities enriched from a pustular mat on various polysaccharide substrates. The annotation of 4000 genes from hundreds of carbohydrate-active enzyme (CAZyme) families in the MAGs and mapping of polysaccharide-degrading CAZymes to their predicted substrates identify trends in the distribution and localization of degradation-associated CAZymes across different bacterial phyla. The compositions of microbial communities enriched on a range of polysaccharides inoculated with pustular mat material support the predicted trends. The combined metagenomic and experimental analyses reveal a widespread potential for EPS degradation among MAGs from Shark Bay pustular mats and suggest distinct roles for some phyla that are reported at high abundances in mats. Specifically, Bacteroidetes are likely to be primary degraders of polysaccharide EPSs, alongside Planctomycetes and a small subset of Alphaproteobacteria and Gammaproteobacteria. Planctomycetes, some Bacteroidetes, Verrucomicrobia, Myxococcota and Anaerolineae are also predicted to favor degradation of sulfated substrates, which are present in the EPS matrix of pustular mats. Large sets of functionally varied CAZymes without signal peptides tagging them for export implicate Anaerolineae and Verrucomicrobia in degrading the downstream products of primary EPS degradation. ImportanceModern marine microbial mats are rich in exopolymeric substances (EPSs) -- complex, high molecular weight polymers secreted by bacteria -- that mediate the formation of carbonate minerals and the preservation of microbial textures in mats. However, the organisms involved in EPS cycling in these mats have not been identified and the links between EPS degradation, carbonate precipitation, and microbial ecology in mats remain poorly understood. We define distinct roles in EPS cycling for many major microbial taxa that are both ubiquitous and abundant in pustular microbial mats from Shark Bay, Australia. The large genomic potential of these microbes for the modification and degradation of diverse extracellular organic polymers provides a blueprint for future studies aimed at quantifying and verifying the specific contributions of these microbes to EPS degradation, carbon cycling and carbonate precipitation.