Relative Importance of H ₂ and H ₂ S as Energy Sources for Primary Production in Geothermal Springs

Abstract

Geothermal waters contain numerous potential electron donors capable of supporting chemolithotrophybased primary production. Thermodynamic predictions of energy yields for specific electron donor and acceptor pairs in such systems are available, although direct assessments of these predictions are rare. This study assessed the relative importance of dissolved H 2 and H 2 S as energy sources for the support of chemolithotrophic metabolism in an acidic geothermal spring in Yellowstone National Park. H 2 S and H 2 concentration gradients were observed in the outflow channel, and vertical H 2 S and O 2 gradients were evident within the microbial mat. H 2 S levels and microbial consumption rates were approximately three orders of magnitude greater than those of H 2 . Hydrogenobaculum-like organisms dominated the bacterial component of the microbial community, and isolates representing three distinct 16S rRNA gene phylotypes (phylotype ‫؍‬ 100% identity) were isolated and characterized. Within a phylotype, O 2 requirements varied, as did energy source utilization: some isolates could grow only with H 2 S, some only with H 2 , while others could utilize either as an energy source. These metabolic phenotypes were consistent with in situ geochemical conditions measured using aqueous chemical analysis and in-field measurements made by using gas chromatography and microelectrodes. Pure-culture experiments with an isolate that could utilize H 2 S and H 2 and that represented the dominant phylotype (70% of the PCR clones) showed that H 2 S and H 2 were used simultaneously, without evidence of induction or catabolite repression, and at relative rate differences comparable to those measured in ex situ field assays. Under in situ-relevant concentrations, growth of this isolate with H 2 S was better than that with H 2 . The major conclusions drawn from this study are that phylogeny may not necessarily be reliable for predicting physiology and that H 2 S can dominate over H 2 as an energy source in terms of availability, apparent in situ consumption rates, and growth-supporting energy.Thermophiles dominate the deepest and shortest branches of the Bacteria and Archaea domains in the tree of life, suggesting that they are likely ancestors of Earth's contemporary microbial populations (8,35). Consequently, these organisms have attracted considerable attention due to interest in the origin of enzymes and metabolic pathways that are thought to have evolved from such organisms. Chemolithotrophic metabolism is foundational to primary productivity in geothermal environments where temperatures exceed the limit of photosynthesis. The bioenergetics of such systems have been examined from the perspective of theoretical energy yield as a way of discussing the relative importance of the various electron donors and acceptors that could support primary productivity (3)(4)(5)22). Other studies have sought to link the inferred physiology of microbial populations with the predicted energy yields obtainable from the inorganic constituents present (4...

An oligarchic microbial assemblage in the anoxic bottom waters of a volcanic subglacial lake

“…At [H 2 ]40.1 nM, H 2 oxidation is more exergonic per O 2 molecule than sulfide oxidation (based on data in Bach and Edwards (2003)). The presence of H 2 -oxidizing clades has been correlated with the free energy of this reaction (Spear et al, 2005), but its importance vis-a`-vis sulfide oxidation is probably controlled by the H 2 affinities and uptake kinetics of guild members (D'Imperio et al, 2008). We speculate that hydrogen-oxidizing bacteria (possibly including Ralstonia sp.)…”

CO 2 Uptake and Fixation by a Thermoacidophilic Microbial Community Attached to Precipitated Sulfur in a Geothermal Spring

“…In addition, submerged substrata at the spring's source are blanketed by precipitates of elemental sulfur (S°), hereafter referred to as S o floc (23). Inventories of bacterial and archaeal 16S rRNA genes recovered from S o floc collected from the source of Dragon Spring indicate the presence of Crenarchaeota and Aquificae (4,15). The latter are related to chemolithoautotrophic Hydrogenobaculum spp., representatives of which have recently been isolated from the spring (15).…”

“…Inventories of bacterial and archaeal 16S rRNA genes recovered from S o floc collected from the source of Dragon Spring indicate the presence of Crenarchaeota and Aquificae (4,15). The latter are related to chemolithoautotrophic Hydrogenobaculum spp., representatives of which have recently been isolated from the spring (15). In the present study, we demonstrate uptake and fixation of CO 2 at a temperature of 73°C by a Hydrogenobaculum-dominated microbial community associated with S o floc collected from the source of Dragon Spring.…”

“…The pH of the water is ϳ3.1, and the temperature of the water at the source fluctuates from 65 to 78°C, which is well above the upper temperature limit for photosynthesis under acidic conditions. Potential electron donors for chemolithoautotrophic growth in the source water include hydrogen (H 2 ) and sulfide (S 2Ϫ ) at concentrations of 13 nM and 65 M, respectively (15). In addition, submerged substrata at the spring's source are blanketed by precipitates of elemental sulfur (S°), hereafter referred to as S o floc (23).…”

“…Evidence for chemosynthesis in these environments is based on the recovery of 16S rRNA gene sequences that are affiliated with cultivated representatives of the phyla Aquificae and Crenarchaeota, many of which are capable of CO 2 fixation via the oxidation of hydrogen (H 2 ) and/or sulfide (HS Ϫ ) (15,17,21,24,26,28,41,46). Surprisingly, CO 2 fixation has yet to be demonstrated in situ in YNP hot spring environments (acidic or alkaline) where temperatures exceed the limits of photosynthesis and where primary production is thought to be driven by chemoautotrophic metabolism (14,15,28,29).Dragon Spring, an acid-sulfate-chloride (ASC) spring located in the Norris Geyser Basin of YNP, is a likely habitat for chemoautotrophic primary production. The pH of the water is ϳ3.1, and the temperature of the water at the source fluctuates from 65 to 78°C, which is well above the upper temperature limit for photosynthesis under acidic conditions.…”