Linking geochemical processes with microbial community analysis: successional dynamics in an arsenic‐rich, acid‐sulphate‐chloride geothermal spring

Abstract

The source waters of acid‐sulphate‐chloride (ASC) geothermal springs located in Norris Geyser Basin, Yellowstone National Park contain several reduced chemical species, including H2, H2S, As(III), and Fe(II), which may serve as electron donors driving chemolithotrophic metabolism. Microorganisms thriving in these environments must also cope with high temperatures, low pH (∼3), and high concentrations of sulphide, As(III), and boron. The goal of the current study was to correlate the temporal and spatial distribution of bacterial and archaeal populations with changes in temperature and geochemical energy gradients occurring throughout a newly formed (redirected) outflow channel of an ASC spring. A suite of complimentary analyses including aqueous geochemistry, microscopy, solid phase identification, and 16S rDNA sequence distribution were used to correlate the appearance of specific microbial populations with biogeochemical processes mediating S, Fe, and As cycling and subsequent biomineralization of As(V)‐rich hydrous ferric oxide (HFO) mats. Rapid As(III) oxidation (maximum first order rate constants ranged from 4 to 5 min−1, t1/2 = 0.17 − 0.14 min) was correlated with the appearance of Hydrogenobaculum and Thiomonas–like populations, whereas the biogenesis of As(V)‐rich HFO microbial mats (mole ratios of As:Fe ∼0.7) was correlated with the appearance of Metallosphaera, Acidimicrobium, and Thiomonas–like populations. Several 16S sequences detected near the source were closely related to sequences of chemolithotrophic hyperthermophilic populations including Stygiolobus and Hydrogenobaculum organisms that are known H2 oxidizers. The use of H2, reduced S(–II,0), Fe(II) and perhaps As(III) by different organisms represented throughout the outflow channel was supported by thermodynamic calculations, confirming highly exergonic redox couples with these electron donors. Results from this work demonstrated that chemical energy gradients play an important role in establishing distinct community structure as a function of distance from geothermal spring discharge.

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

“…are genetically similar (average sequence divergence of 0.0087%) and thus may correspond to the 12 shared phylotypes that migrated to nearly the same position in (17,41,43,44,47). In Dragon Spring, as well as other acidic springs, representatives of this genus have been proposed to obtain their cell carbon through CO 2 fixation (22,23,25,34,46). They have also been shown to physically attach to sulfur (36).…”

Carbon Dioxide Fixation by Metallosphaera yellowstonensis and Acidothermophilic Iron-Oxidizing Microbial Communities from Yellowstone National Park

“…These data are consistent with the hypothesis that M. yellowstonensis and Hydrogenobaculum spp. serve founding roles in the development of Fe(III)-oxide mats and community succession (23,40). Now that the incorporation of inorganic carbon by members of these communities has been firmly established, more detailed trophic cascades and metabolite interactions may be resolvable by using stable-isotope probing coupled with metabolomic and/or proteomic analyses.…”

“…Mature Fe(III)-oxide mats of a 0.5-to 1-cm thickness contain relatively low levels of Hydrogenobaculum-like organisms (2 to 10% of random shotgun sequences). However, these bacteria are important colonizers during the formation of Fe mats (23) and are often found in communities that contain Fe(II)-oxidizing members of the order Sulfolobales, such as Metallosphaera yellowstonensis (17).…”

Hydrogen Peroxide Cycling in High-Temperature Acidic Geothermal Springs and Potential Implications for Oxidative Stress Response

“…The rod-shaped bacteria Hydrogenobaculum spp. initiate biofilm attachment, and the iron-oxidizing archaea Metallosphaera yellowstonensis (strain MK1) are responsible for the oxidation of Fe(II) and subsequent accretion of Fe(III)-oxides (Macur et al, 2004;Kozubal et al, 2008;Takacs-Vesbach et al, 2013;Jennings et al, 2014;Beam et al, 2016). Oxygen is a key driver of microbial growth and subsequent mat morphology (Kempes et al, 2014), and its diffusion into the mat is the rate-limiting factor for Fe(III)-oxide mat formation (Beam et al, 2016).…”