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Speculations on the origin of life and thermophily: Review of available information on reverse gyrase suggests that hyperthermophilic procaryotes are not so primitive

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Forterre, Patrick, Confalonier, Fabrice, Charbonnier, Franck, Duguet, Michel·1995·Origins of Life and Evolution of the Biosphere
DOI 10.1007/bf01581587
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Abstract

All present-day hyperthermophiles studied so far (either Bacteria or Archaea) contain a unique DNA topoisomerase, reverse gyrase, which probably helps to stabilize genomic DNA at high temperature. Herein the data relating this enzyme is reviewed and discussed from the perspective of the nature of the last detectable common ancestor and the origin of life. The sequence of the gene encoding reverse gyrase from an archaeon, Sulfolobus acidocaldarius, suggests that this enzyme contains both a helicase and a topoisomerase domains (Confalonieri et al., Proc. Natl. Acad. Sci., 1993, 90, 4735). Accordingly, it has been proposed that reversed gyrase originated by the fusion of DNA helicase and DNA topoisomerase genes. If reverse gyrase is essential for life at high temperature, its composite structure suggests that DNA helicases and topoisomerases appeared independently and first evolved in a mesophilic world. Such scenario contradicts the hypothesis that a direct link connects present day hyperthermophiles to a hot origin of life. We discuss different patterns for the early cellular evolution in which reverse gyrase appeared either before the emergence of the last common ancestor of Archaea, Bacteria and Eucarya, or in a lineage common to the two procaryotic domains. The later scenario could explain why all today hyperthermophiles are procaryotes.

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  • Reverse gyrase includes two distinct regions, homologous to a topoisomerase and a helicase, respectively.

    “The evolutionary history of reverse gyrase is well constrained because of its structure: it includes two distinct regions, homologous to a topoisomerase and a helicase, respectively (Forterre 1996;Forterre et al. 1995).”

    From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Forterre et al. 1995

  • The splitting scenario requires that reverse gyrase predated even more fundamental and essential cellular mechanisms like membrane transporters, V and F-ATPases, and elongation and initiation factors for protein synthesis.

    “The latter scenario presents a problematic evolutionary narrative, in which modern helicases and some topoisomerases are the descendants of reverse gyrase, requiring that reverse gyrase predated even more fundamental and essential cellular mechanisms like membrane transporters, V and F-ATPases, and elongation and initiation factors for protein synthesis (Forterre et al. 1995).”

    From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Forterre et al. 1995

  • Either reverse gyrase was formed by fusion of genes encoding a topoisomerase and a helicase, or topoisomerases and helicases evolved through splitting of a more ancient gene encoding reverse gyrase.

    “Either reverse gyrase was formed by the fusion of genes encoding of a topoisomerase and a helicase, or topoisomerases and helicases evolved through the splitting of a more ancient gene encoding reverse gyrase (Forterre et al. 1995).”

    From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Forterre et al. 1995

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Research works printed but not linked: 13

  1. Andera, L., Mikulik, K., and Savelyeva, N. D.: 1993, FEMS Microbial. Letters 110, 107.
  2. Collin, R. G.,. Morgan, H. W., Musgrave, D. R., and Daniel, R. M.: 1988, FEMSMicro. Letters 55, 235.
  3. Confalonieri, F., Elie, C., Nadal, M., Bouthier de la Tour, C., Forterre, P., and Duguet, M.: 1993, Proc. NatL Acad. Sci. USA 90, 4753.
  4. Forterre, P. and Elie, C.: 1993, in 'The Biochemistry of Archaea', New Comprehensive Biochemistry (Elsevier) 26, 325.
  5. Forterre, P., Marguet, E., Charbonnier, F., Mojica, F., and Bergerat, A.: 1994b, Abstract of the US/NZ Workshop on extreme thermophiles, December 8-11, Hamilton, New-Zealand.
  6. Gogarten, J. E, Kibak, H., Dittrich, E, Taiz, L., Bowman, E. J., Bowman, B. J., Manolson, M. E, Poole, R. J., Date, T., Oshima, T., Konishi, J., Denda, K., and Yoshida, M.: 1989, Proc. Natl. Acad. Sci. U.S.A. 86, 6661.
  7. Iwabe, N., Kuma, K., Hasegawa, M., Osawa, S., amd Miyata, T.: 1989, Proc. Natl. Acad. Sci. U.S.A. 86, 9355.
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Authors
Forterre, P., Confalonier, F., Charbonnier, F., & Duguet, M.
Affiliations
Université Paris-Sud (FR)
Corresponding author
Forterre, Patrick
ORCID
Forterre, Patrick
Venue
Origins of Life and Evolution of the Biosphere
Publisher
Springer Science and Business Media LLC
Published
1995-06
Volume
25
Issue
1-3
Pages
235-249
ISSN
  • 0169-6149 (ISSN-L)
  • 1573-0875
DOI
10.1007/bf01581587
OpenAlex
W2062275978
Cited by
52
References
63
Citations by year
2024: 1 · 2023: 1 · 2019: 2 · 2018: 2 · 2017: 2 · 2014: 1 · 2013: 2 · 2012: 1
FWCI
3.63
Type
journal article
Language
en
Open access
Licence
Locations
  • Origins of Life and Evolution of Biospheres (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
Keywords
reverse gyrase, hyperthermophiles, origin of life, thermophily, DNA topoisomerase, DNA helicase, gene fusion, last common ancestor, archaea, Sulfolobus acidocaldarius, prokaryotes
MeSH terms
Origin of Life, Archaea, Bacteria, DNA Topoisomerases, Type II, DNA Topoisomerases, Type I, DNA Helicases, DNA, Bacterial, Genes, Bacterial, Hot Temperature, Prokaryotic Cells, RNA, Ribosomal, 16S, RNA, Transfer, Sulfolobus acidocaldarius, Evolution, Molecular

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