Genome-resolved metagenomic revealed novel microbial taxa and distinct metabolism from giant filamentous microbial mats inhabiting anoxic deep reefs of the Maldivian Blue Hole

Blue holes are vertical water-filled openings in carbonate rock that exhibit complex morphologies, ecologies, and water chemistry. In this study, giant filamentous microbial mats found in complete anoxic conditions at 70m depth in the Faanu Mudugau Blue Hole (Maldives) were studied by metagenomic methods. Such communities have likely been evolutionary isolated from the surrounding marine environment for more than 10.000 years since the Blue Hole formation during the last Ice Age. A total of 48 high-quality metagenome-assembled genomes (MAGs) were recovered, predominantly composed of Chloroflexota, Proteobacteria and Desulfobacterota phyla. Interestingly, none of these MAGs have been classified to species level, suggesting the discovery of several new uncharacterized microbial taxa. In particular MAGs belonging to novel bacterial genus within the order Dehalococcoidales accounted for 20% of the filamentous mat community. Genome-resolved metabolic analysis of this dominant microbial fraction revealed a mixotrophic lifestyle based on energy conservation via fermentation, hydrogen metabolism and anaerobic CO2 fixation through the Wood-Ljungdahl pathway. In addition, these bacteria shared several genetic traits with ancestral organisms providing intriguing perspectives on mechanisms driving microbial evolution across different time scales. Overall, our result provides new knowledge for understanding microbial life under extreme conditions in blue hole environments.