The bacterial sulfur cycle in expanding dysoxic and euxinic marine waters

Abstract

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.

Microbiome of the Black Sea water column analyzed by genome centric metagenomics

“…The present study, together with others from the same Black Sea [5,8] (bioproject PRJNA649215) and those recent ones from the Cariaco Basin in Venezuela [21,23] show a first glimpse on the microbiome of anoxic marine water columns. The redoxclines of these habitats show a convergence of various metabolisms at a time, among which we encounter anoxygenic photosynthesis such as that one observed in Chlorobium phaeobacteroides [24], ammonia oxidation by Nitrosopumilus spp., chemolithotrophic metabolisms carried by Gammaproteobacteria such Ca .…”

“…Next, we also showed the main ecological drivers of the redoxcline layer, which included chemolithotrophic S oxidizers and C fixers such as Ca. Thioglobus and dissimilatory nitrate reducers such as Sulfurimonas , both of which were recently analyzed members by previous publication [8]. The redoxcline also showed some other ecologically relevant nitrate reducers such as Bacteroidales MAGs, ammonia oxidizers such as Nitrosopumilus spp, sulfate reducers Desulfatiglandales and Desulfococcales novel species and several Marinimicrobia representatives which are specialized in the H metabolism, denitrification and mixed-acid fermentation.…”

“…To assess the representativity of our samples we also compared the reads between our Black Sea datasets and those from a former sampling campaign [5,8], deposited into the NCBI under bioproject PRJNA649215, observing a clear 16S rRNA taxonomy and read clusterization between samples (Fig. S6).…”

“…Thioglobus, one of the most abundant and versatile players transitioning between oxic-anoxic regimes [19,25]. This microbe has been detected both in Cariaco and Black Sea basins [8] and its adaptive metabolism, which includes physiological adaptations to the oxic-anoxic growth [25] and its wide set of metabolic tools has led it to colonize these zones with a large contribution to S and N biogeochemical cycles as a denitrifier, sulfur-oxidizing and C fixer chemolithotroph. The simultaneous activity of sulfate-reducing and sulfide-oxidizing microbes in these habitats has led to a term known as the “cryptic sulfur cycle” [20].…”

“…Most recently, members of widespread clades such as SUP05 ( Ca . Thioglobus spp), Sulfurimonas bacteria, and uncultivated SAR324 and Marinimicrobia have been studied from this and other dysoxic environments [8]. Here, we present a genome resolved metagenomic study of different depths in the Black Sea adding a total of 359 high-quality MAGs.…”