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Metabolic flexibility of SUP05 under low DO growth conditions

ABSTRACT: Chemoautotrophic bacteria from the SUP05 clade often dominate anoxic waters in marine oxygen minimum zones (OMZs) where reduced sulfur can fuel carbon fixation and denitrification. Some members of the SUP05 clade are facultative aerobes that thrive at the boundaries of OMZs where they experience fluctuations in dissolved oxygen (DO). The degree to which SUP05 contribute to nitrate reduction in these regions depends on their sensitivity to oxygen. We evaluated growth and quantified differences in gene expression in Ca. T. autotrophicus strain EF1 from the SUP05 clade under high DO (22 μM), anoxic, and low DO (3.8 μM) concentrations. We show that strain EF1 cells respire oxygen and nitrate and that cells have higher growth rates, express more genes, and fix more carbon when oxygen becomes available for aerobic respiration. Evidence that facultatively aerobic SUP05 are more active and respire nitrate when oxygen becomes available at low concentrations suggests that they are an important source of nitrite across marine OMZ boundary layers.

ORGANISM(S): Candidatus Thioglobus autotrophicus

PROVIDER: GSE144480 | GEO | 2020/06/01

REPOSITORIES: GEO

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Project description:Chemosynthetic symbioses between bacteria and invertebrates occur worldwide in a wide range of marine habitats. Although they have been intensively investigated, molecular physiological studies of chemoautotrophic bacteria colonizing the surface of animals (ectosymbioses) are scarce. Stilbonematinae nematodes are the only known invertebrates capable of cultivating monocultures of thiotrophic Gammaproteobacteria on their surface. Crucially, as these nematodes migrate through the redox zone of marine sediments, the ectosymbionts directly experience drastic variations in oxygen concentration. Here, by applying an array of omics, Raman microspectroscopy and stable isotope labeling-based techniques, we investigated the effect of varying concentrations of dissolved oxygen on physiology and metabolism of Candidatus Thiosymbion oneisti, the longitudinally dividing ectosymbiont of Laxus oneistus. We show that, unexpectedly, sulfur oxidation genes were upregulated in anoxic relative to oxic conditions, and that carbon fixation genes and incorporation of 13C-labeled bicarbonate were not. Instead, several genes involved in carbon fixation in addition to genes responsible for assimilating organic carbon compounds and polyhydroxyalkanoate (PHA) biosynthesis, as well as nitrogen fixation and urea utilization genes were upregulated in oxic versus anoxic conditions. Furthermore, in the presence of oxygen, stress-related genes were upregulated together with vitamin and cofactor biosynthesis genes likely necessary to withstand its deleterious effects. Based on this first global physiological study of an uncultured, chemosynthetic ectosymbiont, we propose that, in anoxic pore water, it proliferates by utilizing nitrate to oxidize reduced sulfur compounds, whereas, when exposed to oxygen, it exploits aerobic respiration to facilitate energetically costly assimilation of carbon and nitrogen to survive oxidative stress. Both anaerobic sulfur oxidation and its decoupling from carbon fixation represent unprecedented adaptations among chemosynthetic symbionts. We postulate that Ca. T. oneisti originated from an obligate anaerobic, denitrifying sulfur-oxidizer, which, while transitioning from the free-living to the symbiotic lifestyle, evolved mechanisms to survive the oxidative stress inherent to a life attached to an animal.

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Metabolic flexibility of SUP05 under low DO growth conditions

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