The uptake and excretion of partially oxidized sulfur expands the repertoire of energy resources metabolized by hydrothermal vent symbioses

Abstract

Symbiotic associations between animals and chemoautotrophic bacteria crowd around hydrothermal vents. In these associations, symbiotic bacteria use chemical reductants from venting fluid for the energy to support autotrophy, providing primary nutrition for the host. At vents along the Eastern Lau Spreading Center, the partially oxidized sulfur compounds (POSCs) thiosulfate and polysulfide have been detected in and around animal communities but away from venting fluid. The use of POSCs for autotrophy, as an alternative to the chemical substrates in venting fluid, could mitigate competition in these communities. To determine whether ESLC symbioses could use thiosulfate to support carbon fixation or produce POSCs during sulfide oxidation, we used high-pressure, flow-through incubations to assess the productivity of three symbiotic mollusc genera—the snails Alviniconcha spp. and Ifremeria nautilei, and the mussel Bathymodiolus brevior—when oxidizing sulfide and thiosulfate. Via the incorporation of isotopically labelled inorganic carbon, we found that the symbionts of all three genera supported autotrophy while oxidizing both sulfide and thiosulfate, though at different rates. Additionally, by concurrently measuring their effect on sulfur compounds in the aquaria with voltammetric microelectrodes, we showed that these symbioses excreted POSCs under highly sulfidic conditions, illustrating that these symbioses could represent a source for POSCs in their habitat. Furthermore, we revealed spatial disparity in the rates of carbon fixation among the animals in our incubations, which might have implications for the variability of productivity in situ. Together, these results re-shape our thinking about sulfur cycling and productivity by vent symbioses, demonstrating that thiosulfate may be an ecologically important energy source for vent symbioses and that they also likely impact the local geochemical regime through the excretion of POSCs.

Comparative proteomics of related symbiotic mussel species reveals high variability of host–symbiont interactions

“…Our results strongly support the idea that B. thermophilus turns toxic sulfide into the less toxic thiosulfate by mitochondrial sufide oxidation, which may effectively function as a means of sulfide detoxification. This concept was first described for the thiotrophic symbiont-hosting clam Solemya reidi [27], but has since been reported for various other symbiotic and nonsymbiotic animals, including Bathymodiolus species [28][29][30].…”

Hydrothermal Energy Transfer and Organic Carbon Production at the Deep Seafloor

“…How this plasticity relates to the capacity to fix carbon is, however, still largely unconstrained. Estimates of corresponding carbon fixation rates by chemoautotrophic symbionts is restricted by the inability to cultivate them, and has mostly been derived by in vivo experiments on host invertebrates in pressurized aquaria (Childress and Fisher, 1992;Girguis et al, 2000Girguis et al, , 2002Girguis and Childress, 2006;Ponsard et al, 2013;Beinart et al, 2015). Transcriptomic and proteomic studies further shed light on the activity of the metabolic machinery that allows symbionts to optimize energy acquisition and their potential limitation in their natural habitat (Markert et al, 2007;Robidart et al, 2011;Gardebrecht et al, 2012;Sanders et al, 2013;Watsuji et al, 2014).…”

Metatranscriptional Response of Chemoautotrophic Ifremeria nautilei Endosymbionts to Differing Sulfur Regimes

“…Descriptive and experimental studies over the past 30 years have enabled a broad understanding of the chemoautotrophic metabolism of vent symbionts. Physiological experiments with intact animal hosts (e.g., Childress et al, 1986 , 1991 ; Girguis et al, 2000 ; Girguis and Childress, 2006 ; Nyholm et al, 2008 ; Petersen et al, 2011 ; Goffredi et al, 2014 ; Beinart et al, 2015 ) and excised symbionts (Belkin et al, 1986 ; Fisher et al, 1987 ; Wilmot and Vetter, 1990 ; Childress et al, 1991 ; Nelson et al, 1995 ) have established that vent symbionts can fix inorganic carbon via the oxidation of hydrogen sulfide, thiosulfate, hydrogen and/or methane. Separately, analyses of symbiont gene content (Kuwahara et al, 2007 ; Newton et al, 2007 ; Robidart et al, 2008 ; Nakagawa et al, 2014 ), gene and protein expression (Markert et al, 2007 , 2011 ; Nyholm et al, 2008 ; Robidart et al, 2011 ; Gardebrecht et al, 2012 ; Wendeberg et al, 2012 ; Sanders et al, 2013 ), and enzyme activity (Felbeck, 1981 ; Stein et al, 1988 ; Robinson et al, 1998 ) from vent symbioses have clarified the pathways that symbionts employ for these metabolisms.…”

“…I. nautilei lives in mixing zones around hydrothermal vents in the southwestern Pacific, deriving its nutrition from intracellular gill symbionts that can oxidize both sulfide and thiosulfate to fuel autotrophy (thioautotrophy; Beinart et al, 2015 ). Previous characterization of the I. nautilei gill symbiont community revealed associations with a lineage of γ-proteobacterial sulfur oxidizers from the Order Chromatiales (Urakawa et al, 2005 ; Suzuki et al, 2006 ).…”

“…These experiments clarify pathways of sulfur, nitrogen, and carbon metabolism in the Ifremeria -associated bacterial community and provide the first molecular evidence for the activity of methanotrophic bacteria in the gill-associated community. The results are derived from experiments designed to study the effects of geochemical dynamics on sulfur oxidation and carbon fixation rates (Beinart et al, 2015 ). An analysis of symbiont transcripts in light of the observed metabolic rates reveals how I. nautilei symbionts sustain chemoautotrophic activity at low sulfide concentrations, but exhibit a marked change in their physiology as sulfur availability increases.…”