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

Chemosynthetic symbioses occur worldwide in marine habitats. However, physiological studies of chemoautotrophic bacteria thriving on animals are scarce. Stilbonematinae are coated by monocultures of thiotrophic Gammaproteobacteria. As these nematodes migrate through the redox zone, their ectosymbionts experience varying oxygen concentrations. Here, by applying omics, Raman microspectroscopy and stable isotope labeling, we investigated the effect of oxygen on the metabolism of Candidatus Thiosymbion oneisti. Unexpectedly, sulfur oxidation genes were upregulated in anoxic relative to oxic conditions, but carbon fixation genes and incorporation of 13C-labeled bicarbonate were not. Instead, several genes involved in carbon fixation, the assimilation of organic carbon and polyhydroxyalkanoate (PHA) biosynthesis, as well as nitrogen fixation and urea utilization were upregulated in oxic 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 a chemosynthetic ectosymbiont, we propose that, in anoxic sediment, it proliferates by utilizing nitrate to oxidize reduced sulfur, whereas in superficial sediment it exploits aerobic respiration to facilitate 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.