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Anaerobic sulfur oxidation underlies adaptation of a chemosynthetic symbiont to oxic-anoxic interfaces

ABSTRACT: 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.

INSTRUMENT(S): LTQ Orbitrap Velos

ORGANISM(S): Laxus Oneistus Candidatus Thiosymbion Oneisti

SUBMITTER: Stephanie Markert

LAB HEAD: Stephanie Markert

PROVIDER: PXD017709 | Pride | 2021-11-10

REPOSITORIES: Pride

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Anaerobic sulfur oxidation underlies adaptation of a chemosynthetic symbiont to oxic-anoxic interfaces

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