Biofilms from a deep brine pool of the Red Sea. marine metagenome

, we demonstrate microbial interactions with polysaccharides in biofilms from a deep brine pool of the Red Sea. Partial to near-complete genomes of 66 microbes were reconstructed, exemplified by Candidatus Marinimicrobia, Candidatus Cloacimonetes, and Miscellaneous Crenarchaeotic Group (MCG). Genomic analyses revealed a large number and diverse genes associated with polysaccharide fermentation and energy generation, including glycoside hydrolases, nitrate and sulfate reductases, putative bacterial microcompartment biosynthetic clusters (BMC), and F420H2 dehydrogenases. Unique genes and pathways, particularly polysaccharide breakdown and electron transfer were identified in several microbial groups. These features differentiated Marinimicrobia, Cloacimonetes and MCG members from previously reported relatives, suggesting metabolic plasticity and niche-associated evolution, which would be facilitated by horizontal gene transfer (HGT). The capacities of polysaccharide utilization was further evidenced by metatranscriptomic analyses and in vitro characterization of novel enzymes catalyzing the deconstruction of both α- and β-D-glucosides. In conclusion, nitrate and sulfate reducers are also effective participants in polysaccharide degradation; polysaccharide metabolism is likely an important selective force in shaping microbial genomic content and post-genomic activity; and the simultaneous expression of diverse electron transfer systems (ETSs), consistent with enzymatic flexibility, underlies microbial polysaccharide utilization. The present study sheds new light on the three-way relationship among brine environments, microbial evolution and deep-sea carbon cycling.