Cited by 97Genomics and Phylogenetic StudiesMicrobial Community Ecology and PhysiologyBacterial Genetics and Biotechnology

Widespread distribution of archaeal reverse gyrase in thermophilic bacteria suggests a complex history of vertical inheritance and lateral gene transfers

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Brochier-Armanet, Céline, Forterre, Patrick·2007·Archaea

Abstract

Reverse gyrase, an enzyme of uncertain funtion, is present in all hyperthermophilic archaea and bacteria. Previous phylogenetic studies have suggested that the gene for reverse gyrase has an archaeal origin and was transferred laterally (LGT) to the ancestors of the two bacterial hyperthermophilic phyla, Thermotogales and Aquificales. Here, we performed an in‐depth analysis of the evolutionary history of reverse gyrase in light of genomic progress. We found genes coding for reverse gyrase in the genomes of several thermophilic bacteria that belong to phyla other than Aquificales and Thermotogales. Several of these bacteria are not, strictly speaking, hyperthermophiles because their reported optimal growth temperatures are below 80 °C. Furthermore, we detected a reverse gyrase gene in the sequence of the large plasmid of Thermus thermophilus strain HB8, suggesting a possible mechanism of transfer to the T. thermophilus strain HB8 involving plasmids and transposases. The archaeal part of the reverse gyrase tree is congruent with recent phylogenies of the archaeal domain based on ribosomal proteins or RNA polymerase subunits. Although poorly resolved, the complete reverse gyrase phylogeny suggests an ancient acquisition of the gene by bacteria via one or two LGT events, followed by its secondary distribution by LGT within bacteria. Finally, several genes of archaeal origin located in proximity to the reverse gyrase gene in bacterial genomes have bacterial homologues mostly in thermophiles or hyperthermophiles, raising the possibility that they were co‐transferred with the reverse gyrase gene. Our new analysis of the reverse gyrase history strengthens the hypothesis that the acquisition of reverse gyrase may have been a crucial evolutionary step in the adaptation of bacteria to high‐temperature environments. However, it also questions the role of this enzyme in thermophilic bacteria and the selective advantage its presence could provide.

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  • Reverse gyrase appears to have evolved in Archaea and spread into Bacteria through horizontal gene transfer.

    “This scenario is further borne out by the observation that reverse gyrase appears to have evolved in Archaea and spread into Bacteria through horizontal gene transfer (HGT) (Brochier-Armanet and Forterre 2006).”

    From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Brochier-Armanet and Forterre 2006

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  1. Stetter, K.O. 1989. Extremely thermophilic chemolithoautotrophic archaebacteria. In Autotrophic Bacteria. Eds. H.G. Schlegel and B. Bowien. Science Tech. Publishers and Springer-Verlag, Berlin, pp 167-171.

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Authors
Brochier-Armanet, C., & Forterre, P.
Affiliations
Université Paris-Sud (FR)
Venue
Archaea
Publisher
Wiley
Published
2006-05-26
Volume
2
Issue
2
Pages
83-93
ISSN
  • 1472-3646 (ISSN-L)
  • 1472-3654
OpenAlex
W2078610498
Cited by
97
References
37
Citations by year
2026: 1 · 2025: 2 · 2024: 6 · 2022: 2 · 2021: 1 · 2020: 5 · 2019: 4 · 2018: 8 · 2017: 6 · 2016: 3 · 2015: 6 · 2014: 9 · 2013: 9
FWCI
2.72
Type
journal article
Language
en
Open access
Locations
  • Archaea (publishedVersion, cc-by)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords
reverse gyrase, hyperthermophilic bacteria, horizontal gene transfer, Thermus thermophilus, plasmid transfer, transposase, thermophilic adaptation, gene evolution, archaeal phylogeny, Thermotogales, Aquificales
MeSH terms
Amino Acid Sequence, Archaea, Bacteria, Bacterial Proteins, DNA Topoisomerases, Type I, Molecular Sequence Data, Phylogeny, Sequence Alignment, Thermus thermophilus, Evolution, Molecular, Archaeal Proteins, Gene Transfer, Horizontal

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