The Black Sea is the world's largest anoxic basin and a model system for studying processes across redox gradients. In between the oxic surface and the deeper sulfidic waters there is an unusually broad layer of 10-40 m, where neither oxygen nor sulfide are detectable. In this suboxic zone, dissolved phosphate profiles display a pronounced minimum at the upper and a maximum at the lower boundary, with a peak of particulate phosphorus in between, which was suggested to be caused by the sorption of phosphate on sinking particles of metal oxides. Here we show that bacterial polyphosphate inclusions within large magnetotactic bacteria related to the genus Magnetococcus contribute substantially to the observed phosphorus peak, as they contain 26-34% phosphorus compared to only 1-5% in metal-rich particles. Furthermore, we found increased gene expression for polyphosphate kinases by several groups of bacteria including Magnetococcaceae at the phosphate maximum, indicating active bacterial polyphosphate degradation. We propose that large magnetotactic bacteria shuttle up and down within the suboxic zone, scavenging phosphate at the upper and releasing it at the lower boundary. In contrast to a passive transport via metal oxides, this bacterial transport can quantitatively explain the observed phosphate profiles.

Mn is one of the most abundant redox-sensitive metals on earth. Some microorganisms are known to use Mn(IV) oxide (MnO 2 ) as electron acceptor for the oxidation of organic compounds or hydrogen (H 2 ), but so far the use of sulfide (H 2 S) has been suggested but not proven. Here we report on a bacterial isolate which grows autotrophically and couples the reduction of MnO 2 to the oxidation of H 2 S or thiosulfate (S 2 O 3 2− ) for energy generation. The isolate, originating from the Black Sea, is a species within the genus Sulfurimonas , which typically occurs with high cell numbers in the vicinity of sulfidic environments [Y. Han, M. Perner, Front. Microbiol. 6, 989 (2015)]. H 2 S and S 2 O 3 2− are oxidized completely to sulfate (SO 4 2− ) without the accumulation of intermediates. In the culture, Mn(IV) reduction proceeds via Mn(III) and finally precipitation of Ca-rich Mn(II) carbonate [Mn(Ca)CO 3 ]. In contrast to Mn-reducing bacteria, which use organic electron donors or H 2 , Fe oxides are not observed to support growth, which may either indicate an incomplete gene set or a different pathway for extracellular electron transfer.

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The reduction of manganese oxide with sulfide in aquatic redox-stratified systems was previously considered to be mainly chemical, but recent isolation of the Black Sea isolate Candidatus Sulfurimonas marisnigri strain SoZ1 suggests an important role for biological catalyzation. Here we provide evidence from laboratory experiments, field data, and modeling that the latter process has a strong impact on redox zonation in the Black Sea. High relative abundances of Sulfurimonas spp. across the redoxcline in the central western gyre of the Black Sea coincided with the high-level expression of both the sulfide:quinone oxidoreductase gene (sqr, up to 93% expressed by Sulfurimonas spp.) and other sulfur oxidation genes. The cell-specific rate of manganese-coupled sulfide oxidation by Ca. S. marisnigri SoZ1 determined experimentally was combined with the in situ abundance of Sulfurimonas spp. in a one-dimensional numerical model to calculate the vertical sulfide distribution. Abiotic sulfide oxidation was too slow to counterbalance the sulfide flux from euxinic water. We conclude that microbially catalyzed Mn-dependent sulfide oxidation influences the element cycles of Mn, S, C, and N and therefore the prevalence of other functional groups of prokaryotes (e.g., anammox bacteria) in a sulfide-free, anoxic redox zone.

Sulfurimonas species are among the most abundant sulfur-oxidizing bacteria in the marine environment. They are capable of using different electron acceptors, this metabolic flexibility is favorable for their niche adaptation in redoxclines. When oxygen is depleted, most Sulfurimonas spp. (e.g., Sulfurimonas gotlandica) use nitrate ($${{{{{{{\mathrm{NO}}}}}}}}_3^ -$$ NO 3 − ) as an electron acceptor to oxidize sulfur, including sulfide (HS-), S0 and thiosulfate, for energy production. Candidatus Sulfurimonas marisnigri SoZ1 and Candidatus Sulfurimonas baltica GD2, recently isolated from the redoxclines of the Black Sea and Baltic Sea respectively, have been shown to use manganese dioxide (MnO2) rather than $${{{{{{{\mathrm{NO}}}}}}}}_3^ -$$ NO 3 − for sulfur oxidation. The use of different electron acceptors is also dependent on differences in the electron transport chains embedded in the cellular membrane, therefore changes in the membrane, including its lipid composition, are expected but are so far unexplored. Here, we used untargeted lipidomic analysis to reveal changes in the composition of the lipidomes of three representative Sulfurimonas species grown using either $${{{{{{{\mathrm{NO}}}}}}}}_3^ -$$ NO 3 − and MnO2. We found that all Sulfurimonas spp. produce a series of novel phosphatidyldiazoalkyl-diacylglycerol lipids. Ca. Sulfurimonas baltica GD2 adapts its membrane lipid composition depending on the electron acceptors it utilizes for growth and survival. When carrying out MnO2-dependent sulfur oxidation, the novel phosphatidyldiazoalkyl-diacylglycerol headgroup comprises shorter alkyl moieties than when sulfur oxidation is $${{{{{{{\mathrm{NO}}}}}}}}_3^ -$$ NO 3 − -dependent. This is the first report of membrane lipid adaptation when an organism is grown with different electron acceptors. We suggest novel diazoalkyl lipids have the potential to be used as a biomarker for different conditions in redox-stratified systems.