Skip to main content
Log in

The linkage between reverse gyrase and hyperthermophiles: A review of their invariable association

  • Review
  • Published:
The Journal of Microbiology Aims and scope Submit manuscript

Abstract

With the discovery of reverse gyrase in 1972, from Yellowstone National Park, isolated from Sulfolobus acidocaldarius, it has been speculated as to why reverse gyrase can be found in all hyperthermophiles and just what exactly its role is in hyperthermophilic organisms. Hyperthermophiles have been defined as organisms with an optimal growth temperature of above 85°C. Reverse gyrase is responsible for the introduction of positive supercoils into closed circular DNA. This review of reverse gyrase in hyperthermophilic microorganisms summarizes the last two decades of research performed on hyperthermophiles and reverse gyrase in an effort to provide an up to date synopsis of their invariable association. From the data gathered for this review it is reasonable to hypothesize that reverse gyrase is closely tied to hyperthermophilic life.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Atomi, H., R. Matsumi, and T. Imanaka. 2004. Reverse gyrase is not a prerequisite for hyperthermophilic life. J. Bacteriol. 186, 4829–4833.

    Article  PubMed  CAS  Google Scholar 

  • Boonyaratanakornkit, B.B., L.Y. Miao, and D.S. Clark. 2007. Transcriptional responses of the deep sea hyperthermophile Methanocaldococcus jannaschii under shifting extremes of temperature and pressure. Extremophiles 11, 495–503.

    Article  PubMed  CAS  Google Scholar 

  • Brochier-Armanet, C. and P. Forterre. 2006. Widespread distribution of archaeal reverse gyrase in thermophilic bacteria suggests a complex history of vertical inheritance and lateral gene transfers. Archaea 2, 1–11.

    Article  Google Scholar 

  • Champoux, J.J. 2001. DNA topoisomerases: Structure, function and mechanism. Annu. Rev. Biochem. 70, 369–413.

    Article  PubMed  CAS  Google Scholar 

  • Charbonnier, F. and P. Forterre. 1994. Comparison of plasmid DNA topology among mesophilic and thermophilic eubacteria and archeabacteria. J. Bacteriol. 176, 1251–1259.

    PubMed  CAS  Google Scholar 

  • Charlier, D. and L. Droogmans. 2005. Microbial life at high temperature, the challenges, the strategies. Cell. Mol. Life Sci. 62, 2974–2984.

    Article  PubMed  CAS  Google Scholar 

  • Confalonieri, E., C. Elie, M. Nadal, C. De La Tour, P. Forterre, and M. Duguet. 1993. Reverse gyrase: A helicase-like domain and type I topoisomerase in the same polypeptide. Proc. Natl. Acad. Sci. USA 90, 4753–4757.

    Article  PubMed  CAS  Google Scholar 

  • Daniel, R.M. and D. Cowan. 2000. Biomolecular stability and life at high temperatures. Cell. Mol. Life Sci. 57, 250–264.

    Article  PubMed  CAS  Google Scholar 

  • De La Tour, C., C. Portemer, R. Huber, P. Forterre, and M. Duguet. 1991. Reverse gyrase in thermophilic eubacteria. J. Bacteriol. 173, 3921–3923.

    Google Scholar 

  • De La Tour, C., C. Portemer, H. Kaltoum, and M. Duguet. 1998. Reverse gyrase from the hyperthermophilic bacterium Thermotoga maritima: Properties and gene structure. J. Bacteriol. 180, 274–281.

    Google Scholar 

  • De La Tour, C., C. Portemer, M. Nadal, K.O. Stetter, P. Forterre, and M. Duguet. 1990. Reverse gyrase, a hallmark of the hyperthermophilic archeabacteria. J. Bacteriol. 172, 6803–6808.

    Google Scholar 

  • Del Toro Duany, Y., S.P. Jungblut, A.S. Schmidt, and D. Klostermeier. 2008. The reverse gyrase helicase-like domain is a nucleotide-dependent switch that is attenuated by the topoisomerase domain. Nucleic Acids Res. 36, 5882–5895.

    Article  PubMed  CAS  Google Scholar 

  • Forterre, P. 1996. A hot topic: The origin of hyperthermophiles. Cell 85, 789–792.

    Article  PubMed  CAS  Google Scholar 

  • Guipaud, O., E. Marguet, K.M. Noll, C.B. De La Tour, and P. Forterre. 1997. Both DNA gyrase and reverse gyrase are present in the hyperthermophilic bacterium Thermotoga maritima. Proc. Natl. Acad. Sci. USA 94, 10606–10611.

    Article  PubMed  CAS  Google Scholar 

  • Guy, C.P., A.I. Majernik, J.P.J. Chong, and E.L. Bolt. 2004. A novel nuclease-ATPase (Nar71) from archea is part of a proposed thermophilic DNA repair system. Nucleic Acids Res. 32, 6176–6186.

    Article  PubMed  CAS  Google Scholar 

  • Hsieh, T. and J. Plank. 2006. Reverse gyrase functions as a DNA renaturase. J. Biol. Chem. 281, 5640–5647.

    Article  PubMed  CAS  Google Scholar 

  • Imanaka, T. 2008. Adaptation strategy of thermophiles toward hyperthermophily and their molecular bases. Bull. Chem. Soc. Jpn. 81, 171–182.

    Article  CAS  Google Scholar 

  • Kampmann, M. and D. Stock. 2004. Reverse gyrase has heat-protective DNA chaperone activity independent of supercoiling. Nucleic Acids Res. 32, 3537–3545.

    Article  PubMed  CAS  Google Scholar 

  • Klinger, C., M. Roßbach, R. Howe, and M. Kaufmann. 2003. Thermophile-specific proteins: the gene product of aq_1292 from Aquifex aeolicus is an NTPase. BMC Biochem. 4, 1471–2091.

    Article  Google Scholar 

  • Kozyavkin, S., R. Krah, M. Gellert, K.O. Stetter, J.A. Lake, and A.I. Slesarev. 1994. A reverse gyrase with an unusual structure. J. Biol. Chem. 269, 11081–11089.

    PubMed  CAS  Google Scholar 

  • Krah, R., M. O’Dea, and M. Gellert. 1997. Reverse gyrase from Methanopyrus kandleri. J. Biol. Chem. 272, 13986–13990.

    Article  PubMed  CAS  Google Scholar 

  • Lebedinsky, A.V., N.A. Chernyh, and E.A. Bonch-Osmolovskaya. 2007. Phylogenetic systematics of microorganisms inhabiting thermal environments. Biochemistry 72, 1299–1312.

    PubMed  CAS  Google Scholar 

  • Lopez-Garcia, P. and P. Forterre. 1997. DNA topology in hyperthermophilic archaea: reference states and their variation with growth phase, growth temperature and temperature stresses. Mol. Microbiol. 23, 1267–1279.

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Garcia, P. and P. Forterre. 1999. Control of DNA topology during thermal stress in hyperthermophilic archea: DNA topoisomerase levels, activities and induced thermotolerance during heat and cold shock in Sulfolobus. Mol. Microbiol. 33, 766–777.

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Garcia, P., P. Forterre, J. Van Der Oost, and G. Erauso. 2000. Plasmid pGS5 from the hyperthermophilic archaeon Archaeoglobus profundus is negatively supercoiled. J. Bacteriol. 182, 4998–5000.

    Article  PubMed  CAS  Google Scholar 

  • Lowe, S.E., M.K. Jian, and J.G. Zeikus. 1993. Biology, ecology, and biotechnological applications of anaerobic bacteria adapted to environmental stresses in temperature, pH, salinity, or substrates. Microbiol. Rev. 57, 451–509.

    PubMed  CAS  Google Scholar 

  • Madigan, M. 2000 Extremophilic bacteria and microbial diversity. Ann. Missouri Bot. Gard. 87, 3–12.

    Article  Google Scholar 

  • Musgrave, D., X. Zhang, and M. Dinger. 2002. Archaeal genome organization and stress responses: Implications for the origin and evolution of cellular life. Astrobiology 2, 241–253.

    Article  PubMed  CAS  Google Scholar 

  • Omelchenko, M.V., Y.I. Wolf, E.K. Gaidamakova, V.Y. Matrosova, A. Vasilenko, M. Zhai, M.J. Daly, E.V. Koonin, and K.S. Makarova. 2005. Comparative genomics of Thermus thermophilus and Deinococcus radiodurans: divergent routes of adaptation to thermophily and radiation resistance. BMC Evol. Biol. 5, 1–22.

    Article  CAS  Google Scholar 

  • Takai, K., K. Nakamura, T. Toki, U. Tsunogai, M. Miyazaki, J. Miyazaki, H. Hirayama, S. Nakagawa, T. Nunoura, and K. Horikoshi. 2008. Cell proliferation at 122°C and isotypically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation. Proc. Natl. Acad. Sci. USA 105, 10949–10954.

    Article  PubMed  CAS  Google Scholar 

  • Takami, H., Y. Takaki, G.J. Chee, S. Nishi, S. Shimamura, H. Suzuki, S. Matsui, and I. Uchiyama. 2004. Thermoadaptation trait revealed by the genome sequence of thermophilic Geobacillus kaustophilus. Nucleic Acids Res. 32, 6292–6303.

    Article  PubMed  CAS  Google Scholar 

  • Unsworth, L., J. Van Der Oost, and S. Koutsopoulos. 2007. Hyperthermophilic enzymes — stability, activity and implementation strageties for high temperature applications. FEBS Lett. 274, 4044–4056.

    CAS  Google Scholar 

  • Valenti, A., G. Perugino, A. D’Amaro, A. Cacace, A. Napoli, M. Rossi, and M. Ciaramella. 2008. Dissection of reverse gyrase activities: insight into the evolution of a thermostable molecular machine. Nucleic Acids Res. 36, 4587–4597.

    Article  PubMed  CAS  Google Scholar 

  • Vieille, C. and G.J. Zeikus. 2001. Hyperthermophilic enzymes: Sources, uses and molecular mechanisms for thermostability. Microbiol. Mol. Biol. 65, 1–43.

    Article  CAS  Google Scholar 

  • Zierenberg, R.A., M.W.W. Adams, and A.J. Arp. 2000. Life in extreme environments: Hydrothermal vents. Proc. Natl. Acad. Sci. USA 97, 12961–12962.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sathees B. C. Chandra.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Heine, M., Chandra, S.B.C. The linkage between reverse gyrase and hyperthermophiles: A review of their invariable association. J Microbiol. 47, 229–234 (2009). https://doi.org/10.1007/s12275-009-0019-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-009-0019-8

Keywords

Navigation