Adaptations to submarine hydrothermal environments exemplified by the genome of Nautilia profundicola

Barbara J. Campbell, Julie L. Smith, Thomas E. Hanson, Martin G. Klotz, Lisa Y. Stein, Charles K. Lee, Dongying Wu, Jeffrey M. Robinson, Hoda M. Khouri, Jonathan A Eisen, S. Craig Cary

Research output: Contribution to journalArticle

76 Scopus citations

Abstract

Submarine hydrothermal vents are model systems for the Archaean Earth environment, and some sites maintain conditions that may have favored the formation and evolution of cellular life. Vents are typified by rapid fluctuations in temperature and redox potential that impose a strong selective pressure on resident microbial communities. Nautilia profundicola strain Am-H is a moderately thermophilic, deeply-branching Epsilonproteobacterium found free-living at hydrothermal vents and is a member of the microbial mass on the dorsal surface of vent polychaete, Alvinella pompejana. Analysis of the 1.7-Mbp genome of N. profundicola uncovered adaptations to the vent environment - some unique and some shared with other Epsilonproteobacterial genomes. The major findings included: (1) a diverse suite of hydrogenases coupled to a relatively simple electron transport chain, (2) numerous stress response systems, (3) a novel predicted nitrate assimilation pathway with hydroxylamine as a key intermediate, and (4) a gene (rgy) encoding the hallmark protein for hyperthermophilic growth, reverse gyrase. Additional experiments indicated that expression of rgy in strain Am-H was induced over 100-fold with a 20°C increase above the optimal growth temperature of this bacterium and that closely related rgy genes are present and expressed in bacterial communities residing in geographically distinct thermophilic environments. N. profundicola, therefore, is a model Epsilonproteobacterium that contains all the genes necessary for life in the extreme conditions widely believed to reflect those in the Archaean biosphere - anaerobic, sulfur, H2- and CO 2-rich, with fluctuating redox potentials and temperatures. In addition, reverse gyrase appears to be an important and common adaptation for mesophiles and moderate thermophiles that inhabit ecological niches characterized by rapid and frequent temperature fluctuations and, as such, can no longer be considered a unique feature of hyperthermophiles.

Original languageEnglish (US)
Article numbere1000362
JournalPLoS Genetics
Volume5
Issue number2
DOIs
StatePublished - Feb 2009

ASJC Scopus subject areas

  • Genetics
  • Molecular Biology
  • Ecology, Evolution, Behavior and Systematics
  • Cancer Research
  • Genetics(clinical)

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    Campbell, B. J., Smith, J. L., Hanson, T. E., Klotz, M. G., Stein, L. Y., Lee, C. K., Wu, D., Robinson, J. M., Khouri, H. M., Eisen, J. A., & Cary, S. C. (2009). Adaptations to submarine hydrothermal environments exemplified by the genome of Nautilia profundicola. PLoS Genetics, 5(2), [e1000362]. https://doi.org/10.1371/journal.pgen.1000362