A Kiritimatiellales isolate representing a novel genus shows the potential for anaerobic degradation of sulfated polysaccharides and nitrogen fixation

Na Liu, University of California Santa Barbara, Inderdepartmental Graduate Program in Marine Science, Santa Barbara, United States, Veronika Kivenson, University of California Santa Barbara, Interdepartmental Graduate Program in Marine Science, Santa Barbara, CA, United States, Zhisong Cui, Key Laboratory for Marine Bioactive Substances and Modern Analytical Technology, First Institute of Oceanography, Ministry of Natural Resources of China, Qingdao, China and David L Valentine, University of California Santa Barbara, Marine Science Institute, Santa Barbara, CA, United States; University of California Santa Barbara, Department of Earth Science, Santa Barbara, CA, United States
Abstract:
Polysaccharides are diverse compounds that exist in the cell walls of marine macroalgae and seagrass, and are important for microbial adhesion in microbial mats. Microbial degradation of these complex substances plays a key role in marine biogeochemical cycling of carbon and sulfur. Members of the recently described Kiritimatiellaeota phylum (within the Plantomycetes-Verrucomicrobia-Chlamydia superphylum) are degraders of recalcitrant polysaccharides in widespread anoxic environments. To date, three cultivated strains have been characterized, and little is known about the metabolic capabilities and functional role of this phylum in the environment. In this study, we enriched and isolated a novel anaerobic bacterium from seafloor biofilms at Shane Seep within the Coal Oil Point seep field (Santa Barbara, California). Here, we describe a novel lineage at the genus level in the order Kiritimatiellales, with a full-length 16S rRNA gene sharing ≤ 94.50% identity with the three reported cultivated strains. Members of this taxonomic group are able to utilize both agar and other sulfated polysaccharides, expanding the known substrate range of this phylum. A near-complete genome revealed an extensive metabolic capacity for anaerobic degradation of sulfated polysaccharides, as evidenced by 165 sulfatases and 93 carbohydrate-active enzymes. Additionally, the presence of multiple nitrogenases (nifDKH) encoded in the genome indicates the potential for nitrogen fixation, a previously undescribed pathway for this phylum.
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