Metagenomes from high-temperature chemotrophic systems reveal geochemical controls on microbial community structure and function

William P. Inskeep, Douglas B. Rusch, Zackary J. Jay, Markus J. Herrgard, Mark A. Kozubal, Toby H. Richardson, Richard E. Macur, Natsuko Hamamura, Ryan de M. Jennings, Bruce W. Fouke, Anna Louise Reysenbach, Frank Roberto, Mark Young, Ariel Schwartz, Eric S. Boyd, Jonathan H. Badger, Eric J. Mathur, Alice C. Ortmann, Mary Bateson, Gill GeeseyMarvin Frazier

Research output: Contribution to journalArticle

127 Citations (Scopus)

Abstract

The Yellowstone caldera contains the most numerous and diverse geothermal systems on Earth, yielding an extensive array of unique high-temperature environments that host a variety of deeply-rooted and understudied Archaea, Bacteria and Eukarya. The combination of extreme temperature and chemical conditions encountered in geothermal environments often results in considerably less microbial diversity than other terrestrial habitats and offers a tremendous opportunity for studying the structure and function of indigenous microbial communities and for establishing linkages between putative metabolisms and element cycling. Metagenome sequence (14-15,000 Sanger reads per site) was obtained for five hightemperature (>65°C) chemotrophic microbial communities sampled from geothermal springs (or pools) in Yellowstone National Park (YNP) that exhibit a wide range in geochemistry including pH, dissolved sulfide, dissolved oxygen and ferrous iron. Metagenome data revealed significant differences in the predominant phyla associated with each of these geochemical environments. Novel members of the Sulfolobales are dominant in low pH environments, while other Crenarchaeota including distantly-related Thermoproteales and Desulfurococcales populations dominate in suboxic sulfidic sediments. Several novel archaeal groups are well represented in an acidic (pH 3) Fe-oxyhydroxide mat, where a higher O 2 influx is accompanied with an increase in archaeal diversity. The presence or absence of genes and pathways important in S oxidation-reduction, H 2 -oxidation, and aerobic respiration (terminal oxidation) provide insight regarding the metabolic strategies of indigenous organisms present in geothermal systems. Multiple-pathway and protein-specific functional analysis of metagenome sequence data corroborated results from phylogenetic analyses and clearly demonstrate major differences in metabolic potential across sites. The distribution of functional genes involved in electron transport is consistent with the hypothesis that geochemical parameters (e.g., pH, sulfide, Fe, O 2 ) control microbial community structure and function in YNP geothermal springs.

Original languageEnglish
Article numbere9773
JournalPloS one
Volume5
Issue number3
DOIs
Publication statusPublished - Dec 1 2010

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Geothermal springs
Metagenome
Sulfides
microbial communities
community structure
Genes
Hot Springs
Oxidation
Functional analysis
hot springs
Temperature
Geochemistry
oxidation
Dissolved oxygen
sulfides
Desulfurococcales
Metabolism
Thermoproteales
Sulfolobales
national parks

All Science Journal Classification (ASJC) codes

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Inskeep, W. P., Rusch, D. B., Jay, Z. J., Herrgard, M. J., Kozubal, M. A., Richardson, T. H., ... Frazier, M. (2010). Metagenomes from high-temperature chemotrophic systems reveal geochemical controls on microbial community structure and function. PloS one, 5(3), [e9773]. https://doi.org/10.1371/journal.pone.0009773

Metagenomes from high-temperature chemotrophic systems reveal geochemical controls on microbial community structure and function. / Inskeep, William P.; Rusch, Douglas B.; Jay, Zackary J.; Herrgard, Markus J.; Kozubal, Mark A.; Richardson, Toby H.; Macur, Richard E.; Hamamura, Natsuko; Jennings, Ryan de M.; Fouke, Bruce W.; Reysenbach, Anna Louise; Roberto, Frank; Young, Mark; Schwartz, Ariel; Boyd, Eric S.; Badger, Jonathan H.; Mathur, Eric J.; Ortmann, Alice C.; Bateson, Mary; Geesey, Gill; Frazier, Marvin.

In: PloS one, Vol. 5, No. 3, e9773, 01.12.2010.

Research output: Contribution to journalArticle

Inskeep, WP, Rusch, DB, Jay, ZJ, Herrgard, MJ, Kozubal, MA, Richardson, TH, Macur, RE, Hamamura, N, Jennings, RDM, Fouke, BW, Reysenbach, AL, Roberto, F, Young, M, Schwartz, A, Boyd, ES, Badger, JH, Mathur, EJ, Ortmann, AC, Bateson, M, Geesey, G & Frazier, M 2010, 'Metagenomes from high-temperature chemotrophic systems reveal geochemical controls on microbial community structure and function', PloS one, vol. 5, no. 3, e9773. https://doi.org/10.1371/journal.pone.0009773
Inskeep, William P. ; Rusch, Douglas B. ; Jay, Zackary J. ; Herrgard, Markus J. ; Kozubal, Mark A. ; Richardson, Toby H. ; Macur, Richard E. ; Hamamura, Natsuko ; Jennings, Ryan de M. ; Fouke, Bruce W. ; Reysenbach, Anna Louise ; Roberto, Frank ; Young, Mark ; Schwartz, Ariel ; Boyd, Eric S. ; Badger, Jonathan H. ; Mathur, Eric J. ; Ortmann, Alice C. ; Bateson, Mary ; Geesey, Gill ; Frazier, Marvin. / Metagenomes from high-temperature chemotrophic systems reveal geochemical controls on microbial community structure and function. In: PloS one. 2010 ; Vol. 5, No. 3.
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