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

The source waters of acid-sulphate-chloride (ASC) geothermal springs located in Norris Geyser Basin, Yellow-stone National Park contain several reduced chemical species, including H-2, H-2 S, 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 (similar to 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), t(1/2) = 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 similar to 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 H-2 oxidizers. The use of H-2, 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.