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Archaea, 2:83–93
© 2006 Heron Publishing—Victoria, Canada
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Widespread distribution of archaeal reverse gyrase in thermophilic bacteria suggests a complex history of vertical inheritance and lateral gene transfers

Céline Brochier-Armanet (1, 3) and Patrick Forterre (2, 4)

1. EA 3781 EGEE (Evolution Génome Environnement), Université de Provence Aix-Marseille I, Centre Saint-Charles, 3 Place Victor Hugo 13331, Marseille Cedex 3, France / 2. Institut de Génétique et Microbiologie, UMR CNRS 8621, Université Paris-Sud, 91405 Orsay, France / 3. Corresponding Author ([email protected]) / 4. Unité Biologie Moléculaire du Gène chez les Extremophiles, Institut Pasteur, 25 rue du Dr Roux, 75724 Paris Cedex 15, France / Received September 21, 2005; accepted accepted May 26, 2006; published online August 18, 2006


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.

Keywords: adaptation, Archaea, evolution, genome context, HGT, hyperthermophily, plasmid, thermophily, Thermus thermophilus .

ISSN 1472-3654 (Online) ISSN 1472-3646 (Print) Copyright © 2002–2007 Heron Publishing