Hydrogen and bioenergetics in the Yellowstone geothermal ecosystem - PubMed (original) (raw)
Hydrogen and bioenergetics in the Yellowstone geothermal ecosystem
John R Spear et al. Proc Natl Acad Sci U S A. 2005.
Abstract
The geochemical energy budgets for high-temperature microbial ecosystems such as occur at Yellowstone National Park have been unclear. To address the relative contributions of different geochemistries to the energy demands of these ecosystems, we draw together three lines of inference. We studied the phylogenetic compositions of high-temperature (>70 degrees C) communities in Yellowstone hot springs with distinct chemistries, conducted parallel chemical analyses, and carried out thermodynamic modeling. Results of extensive molecular analyses, taken with previous results, show that most microbial biomass in these systems, as reflected by rRNA gene abundance, is comprised of organisms of the kinds that derive energy for primary productivity from the oxidation of molecular hydrogen, H2. The apparent dominance by H2-metabolizing organisms indicates that H2 is the main source of energy for primary production in the Yellowstone high-temperature ecosystem. Hydrogen concentrations in the hot springs were measured and found to range up to >300 nM, consistent with this hypothesis. Thermodynamic modeling with environmental concentrations of potential energy sources also is consistent with the proposed microaerophilic, hydrogen-based energy economy for this geothermal ecosystem, even in the presence of high concentrations of sulfide.
Figures
Fig. 1.
Site locations. A map of Yellowstone National Park shows locations of hydrogen measurements indicated by site number (Tables 1 and 2). Boxed numbers identify sites with associated phylogenetic analyses.
Fig. 2.
Cumulative rRNA gene analyses. (A) Distribution of sequences by phylogenetic group as identified with
arb
. Universal PCR primers (515F and 1391R) were used with environmental DNA templates from five hot springs, and resultant sequences were compiled for the assemblage. Five percent of the sequences are from one potentially new candidate bacterial division encountered in this study. (B) Distribution of archaeal sequences in three hot springs with two archaeal-specific PCR primer pairs. The majority, 77% of the sequences, are identified as crenarchaeotes. Eighteen percent fall within Euryarchaeota, and 5% fall within Korarchaeota. OPA-2, OPA-4, and OPA-Like represent environmental DNA sequences from a previous study of Obsidian Pool (16); FCG-1 represents sequences from marine/hydrothermal vent benthic archaea; and SEGMEG-1 represents sequences from deep South African mines.
Fig. 3.
Bacterial rRNA gene clone libraries. Bacterial sequences (
arb
phylogenetic assignment) for five previously unexamined hot springs are shown as pie charts. At least two PCR primer pairs and as many as eight (Obsidian Pool Prime) were used to determine the compositions for each hot spring.
Fig. 4.
Low- and high-sulfide communities compilation. (A) The phylogenetic distribution of rRNA gene sequences obtained from the two low-sulfide springs of this study (West Thumb Pool and Obsidian Pool Prime) combined with the five low-sulfide springs studied by Blank et al. in ref. (Octopus Spring, Queens Laundry, Eclipse Geyser, Spindle Spring, and Boulder Spring). (B) The phylogenetic distribution of rRNA gene sequences obtained from the three high-sulfide springs in this study (Cinder Pool, Washburn Spring 1, and Washburn Spring 3).
Fig. 5.
Results of thermodynamic models. Shown are the amounts of energy available from O2-consuming metabolic reactions, expressed in terms of available energy per mole of limiting O2 for comparative purposes. The available energy is shown for a range of hypothetical O2 concentrations because accurate O2 concentrations in hot waters are difficult to assess.
Comment in
- Hydrogen and energy flow as "sensed" by molecular genetics.
Nealson KH. Nealson KH. Proc Natl Acad Sci U S A. 2005 Mar 15;102(11):3889-90. doi: 10.1073/pnas.0500211102. Epub 2005 Mar 7. Proc Natl Acad Sci U S A. 2005. PMID: 15753283 Free PMC article. No abstract available.
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References
- Madigan, M. T., Martinko, J. M. & Parker, J. (2003) Brock Biology of Microorganisms (Prentice Hall, Upper Saddle River, NJ).
- Brock, T. D. (1967) Science 158, 1012-1019. - PubMed
- Brock, T. D. (1978) Thermophilic Microorganisms and Life at High Temperatures (Springer, New York).
- Jannasch, H. W. (1985) Proc. R. Soc. London Ser. B. 225, 277-297.
- Jannasch, H. W. & Mottl, M. J. (1985) Science 229, 717-725. - PubMed
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