Abstract
Endosymbioses between animals and chemoautotrophic bacteria are ubiquitous at hydrothermal vents. These environments are distinguished by high physico-chemical variability, yet we know little about how these symbioses respond to environmental fluctuations. We therefore examined how the γ-proteobacterial symbionts of the vent snail Ifremeria nautilei respond to changes in sulfur geochemistry. Via shipboard high-pressure incubations, we subjected snails to 105 μM hydrogen sulfide (LS), 350 μM hydrogen sulfide (HS), 300 μM thiosulfate (TS) and seawater without any added inorganic electron donor (ND). While transcript levels of sulfur oxidation genes were largely consistent across treatments, HS and TS treatments stimulated genes for denitrification, nitrogen assimilation, and CO2 fixation, coincident with previously reported enhanced rates of inorganic carbon incorporation and sulfur oxidation in these treatments. Transcripts for genes mediating oxidative damage were enriched in the ND and LS treatments, potentially due to a reduction in O2 scavenging when electron donors were scarce. Oxidative TCA cycle gene transcripts were also more abundant in ND and LS treatments, suggesting that I. nautilei symbionts may be mixotrophic when inorganic electron donors are limiting. These data reveal the extent to which I. nautilei symbionts respond to changes in sulfur concentration and species, and, interpreted alongside coupled biochemical metabolic rates, identify gene targets whose expression patterns may be predictive of holobiont physiology in environmental samples.
Highlights
Hydrothermal vents are dynamic ecosystems where the vigorous emission of hot, chemically reduced fluid from the seafloor into the surrounding seawater results in a temporally and spatially variable physico-chemical environment
Snails used for the HS, TS, and LS treatments were acclimated without an electron donor, whereas those used in the no electron donor (ND) treatment were acclimated with 300 μM sulfide, achieved by bubbling input water with gaseous hydrogen sulfide (5% H2S/95% N2)
The origin and composition of the organic carbon for symbiont heterotrophy is unknown in I. nautilei, but could involve recycling of organics leaked from host cells or the catabolism of internally stored carbon (Kleiner et al, 2012b)
Summary
Hydrothermal vents are dynamic ecosystems where the vigorous emission of hot, chemically reduced fluid from the seafloor into the surrounding seawater results in a temporally and spatially variable physico-chemical environment. Vent symbioses thrive in mixing zones where fluid turbulence causes conditions to change rapidly over small spatial scales such that adjacent animals may experience vastly different chemical and physical environments (Johnson et al, 1986) Sulfur chemistry in these zones can be dynamic, with concentrations of hydrogen sulfide and derivatives of sulfide oxidation (e.g., thiosulfate) varying temporally and in proximity to vent sites (Gru et al, 1998; Mullaugh et al, 2008; Waite et al, 2008; Gartman et al, 2011). The dynamic nature of hydrothermal vents exposes organisms to fluctuating concentrations of diverse reductants and oxidants (Shank et al, 1998), and may drive variation in the metabolism and growth dynamics of symbiotic partners (Duperron et al, 2007; Dubilier et al, 2008; Robidart et al, 2011)
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