van Vliet, Daan M.

Dysoxic marine waters (DMW, < 1 μM oxygen) are currently expanding in volume in the oceans, which has biogeochemical, ecological and societal consequences on a global scale. In these environments, distinct bacteria drive an active sulfur cycle, which has only recently been recognized for open‐ocean DMW. This review summarizes the current knowledge on these sulfur‐cycling bacteria. Critical bottlenecks and questions for future research are specifically addressed. Sulfate‐reducing bacteria (SRB) are core members of DMW. However, their roles are not entirely clear, and they remain largely uncultured. We found support for their remarkable diversity and taxonomic novelty by mining metagenome‐assembled genomes from the Black Sea as model ecosystem. We highlight recent insights into the metabolism of key sulfur‐oxidizing SUP05 and Sulfurimonas bacteria, and discuss the probable involvement of uncultivated SAR324 and BS‐GSO2 bacteria in sulfur oxidation. Uncultivated Marinimicrobia bacteria with a presumed organoheterotrophic metabolism are abundant in DMW. Like SRB, they may use specific molybdoenzymes to conserve energy from the oxidation, reduction or disproportionation of sulfur cycle intermediates such as S 0 and thiosulfate, produced from the oxidation of sulfide. We expect that tailored sampling methods and a renewed focus on cultivation will yield deeper insight into sulfur‐cycling bacteria in DMW.

Recently, we isolated two marine strains, F1T and F21T, which together with Kiritimatiella glycovorans L21-Fru-ABT are the only pure cultures of the class Kiritimatiellae within the phylum Verrucomicrobiota. Here, we present an in-depth genome-guided characterization of both isolates with emphasis on their exopolysaccharide synthesis. The strains only grew fermentatively on simple carbohydrates and sulfated polysaccharides. Strains F1T, F21T and K. glycovorans reduced elemental sulfur, ferric citrate and anthraquinone-2,6-disulfonate during anaerobic growth on sugars. Both strains produced exopolysaccharides during stationary phase, probably with intracellularly stored glycogen as energy and carbon source. Exopolysaccharides included N-sulfated polysaccharides probably containing hexosamines and thus resembling glycosaminoglycans. This implies that the isolates can both degrade and produce sulfated polysaccharides. Both strains encoded an unprecedently high number of glycoside hydrolase genes (422 and 388, respectively), including prevalent alpha-L-fucosidase genes, which may be necessary for degrading complex sulfated polysaccharides such as fucoidan. Strain F21T encoded three putative glycosaminoglycan sulfotransferases and a putative sulfate glycosaminoglycan biosynthesis gene cluster. Based on phylogenetic and chemotaxonomic analyses, we propose the taxa Pontiella desulfatans F1T gen. nov., sp. nov. and Pontiella sulfatireligans F21T sp. nov. as representatives of the Pontiellaceae fam. nov. within the class Kiritimatiellae.

Oil-rich sediments from the Gulf of Mexico were found to contain diverse alkane-degrading groups of archaea. The symbiotic, consortium-forming “ Candidatus Argoarchaeum” and “ Candidatus Syntrophoarchaeum” are likely responsible for the degradation of ethane and short-chain alkanes, with the help of sulfate-reducing bacteria. “ Ca. Methanoliparia” occurs as single cells associated with oil droplets. These archaea encode two phylogenetically different methyl-coenzyme M reductases that may allow this organism to thrive as a methanogen on a substrate of long-chain alkanes. Based on a library survey, we show that “ Ca. Methanoliparia ” is frequently detected in oil reservoirs and may be a key agent in the transformation of long-chain alkanes to methane. Our findings provide evidence for the important and diverse roles of archaea in alkane-rich marine habitats and support the notion of a significant functional versatility of the methyl coenzyme M reductase.