Changes in the membrane lipid composition of a Sulfurimonas species depend on the electron acceptor used for sulfur oxidation

Abstract

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.

Mode of carbon and energy metabolism shifts lipid composition in the thermoacidophile Acidianus

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