Widespread distribution of archaeal reverse gyrase in thermophilic bacteria suggests a complex history of vertical inheritance and lateral gene transfers
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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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Cites
Basic local alignment search tool
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990) · Journal of Molecular Biology · doi:10.1006/jmbi.1990.9999 · Cited by 98,669 · see citing works
Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994) · Nucleic Acids Research · doi:10.1093/nar/22.22.4673 · Cited by 64,617 · see citing works
MrBayes 3: Bayesian phylogenetic inference under mixed models
Ronquist, F., & Huelsenbeck, J. P. (2003) · Bioinformatics · doi:10.1093/bioinformatics/btg180 · Cited by 28,956 · see citing works
A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood
Guindon, S., & Gascuel, O. (2003) · Systematic Biology · doi:10.1080/10635150390235520 · Cited by 16,698 · see citing works
Glacial history and colonization of Europe by the blue tit Parus caeruleus
Kvist, L., Viiri, K. M., Dias, P. C., Rytkönen, S., & Orell, M. I. (2004) · Journal of Avian Biology · doi:10.1111/j.0908-8857.2004.03297.x · Cited by 2,798 · see citing works
Nelson, K. E., Clayton, R. A., Gill, S. R., Gwinn, M. L., Dodson, R. J., Haft, D. H., Hickey, E. K., Peterson, J. D., Nelson, W. C., Ketchum, K. A., et al. (1999) · Nature · doi:10.1038/20601 · Cited by 1,493 · see citing works
Horizontal gene transfer in prokaryotes: Quantification and classification
Koonin, E. V., Makarova, K. S., & Aravind, L. (2001) · Annual Review of Microbiology · doi:10.1146/annurev.micro.55.1.709 · Cited by 1,126 · see citing works
A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont
Huber, H., Hohn, M. J., Rachel, R., Fuchs, T., Wimmer, V. C., & STETTER, K. O. (2002) · Nature · doi:10.1038/417063a · Cited by 825 · see citing works
Aminoacyl-tRNA Synthetases, the Genetic Code, and the Evolutionary Process
Woese, C. R., Olsen, G. J., Ibba, M., & Söll, D. (2000) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.64.1.202-236.2000 · Cited by 706 · see citing works
MUST, a computer package of Management Utilities for Sequences and Trees
Philippe, H. (1993) · Nucleic Acids Research · doi:10.1093/nar/21.22.5264 · Cited by 600 · see citing works
The genome of Nanoarchaeum equitans: Insights into early archaeal evolution and derived parasitism
Waters, E. R., Hohn, M. J., Ahel, I., Graham, D. E., Adams, M. D., Barnstead, M., Beeson, K. Y., Bibbs, L., Bolanos, R. A., Keller, M., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1735403100 · Cited by 512 · see citing works
The Closest BLAST Hit Is Often Not the Nearest Neighbor
Koski, L. B., & Golding, G. B. (2001) · Journal of Molecular Evolution · doi:10.1007/s002390010184 · Cited by 466 · see citing works
A Nonhyperthermophilic Common Ancestor to Extant Life Forms
Galtier, N., Tourasse, N., & Gouy, M. (1999) · Science · doi:10.1126/science.283.5399.220 · Cited by 442 · see citing works
The genome sequence of the extreme thermophile Thermus thermophilus
Henne, A., Brüggemann, H., Raasch, C., Wiezer, A., Hartsch, T., Liesegang, H., Johann, A., Lienard, T., Gohl, O., Martínez‐Arias, R., et al. (2004) · Nature Biotechnology · doi:10.1038/nbt956 · Cited by 385 · see citing works
Evidence for massive gene exchange between archaeal and bacterial hyperthermophiles
Aravind, L., Tatusov, R. L., Wolf, Y. I., Walker, D. R., & Koonin, E. V. (1998) · Trends in Genetics · doi:10.1016/s0168-9525(98)01553-4 · Cited by 333 · see citing works
Reverse gyrase—a topoisomerase which introduces positive superhelical turns into DNA
Kikuchi, A., & Asai, K. (1984) · Nature · doi:10.1038/309677a0 · Cited by 292 · see citing works
Hyperthermophiles in the history of life
STETTER, K. O. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1907 · Cited by 291 · see citing works
Higher‐level classification of the Archaea: evolution of methanogenesis and methanogens
Bapteste, E. P., Brochier‐Armanet, C., & Boucher, Y. (2005) · Archaea · doi:10.1155/2005/859728 · Cited by 261 · see citing works
Self-citationA non-hyperthermophilic ancestor for Bacteria
Brochier‐Armanet, C., & Philippe, H. (2002) · Nature · doi:10.1038/417244a · Cited by 253 · see citing works
Self-citationA hot story from comparative genomics: reverse gyrase is the only hyperthermophile-specific protein
Forterre, P. (2002) · Trends in Genetics · doi:10.1016/s0168-9525(02)02650-1 · Cited by 228 · see citing works
Self-citationBrochier‐Armanet, C., Gribaldo, S., Zivanovic, Y., Confalonieri, F., & Forterre, P. (2005) · Genome biology · doi:10.1186/gb-2005-6-5-r42 · Cited by 168 · see citing works
Self-citationReverse Gyrase Is Not a Prerequisite for Hyperthermophilic Life
Atomi, H., Matsumi, R., & Imanaka, T. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.14.4829-4833.2004 · Cited by 146 · see citing works
DNA stability at temperatures typical for hyperthermophiles
Marguet, E., & Forterre, P. (1994) · Nucleic Acids Research · doi:10.1093/nar/22.9.1681 · Cited by 127 · see citing works
Self-citationForterre, P., de la Tour, C. B., Philippe, H., & Duguet, M. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(00)01980-6 · Cited by 126 · see citing works
Self-citationForterre, P., Brochier‐Armanet, C., & Philippe, H. (2002) · Theoretical Population Biology · doi:10.1006/tpbi.2002.1592 · Cited by 112 · see citing works
Self-citationEnvironmental signals and cell fate specification in premigratory neural crest
Dorsky, R. I., Moon, R. T., & Raible, D. W. (2000) · BioEssays · doi:10.1002/1521-1878(200008)22:8 · Cited by 111 · see citing works
Self-citationBrochier‐Armanet, C., Forterre, P., & Gribaldo, S. (2005) · BMC Evolutionary Biology · doi:10.1186/1471-2148-5-36 · Cited by 94 · see citing works
Self-citationReverse gyrase has heat-protective DNA chaperone activity independent of supercoiling
Kampmann, M. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh683 · Cited by 94 · see citing works
Comparison of plasmid DNA topology among mesophilic and thermophilic eubacteria and archaebacteria
Charbonnier, F., & Forterre, P. (1994) · Journal of Bacteriology · doi:10.1128/jb.176.5.1251-1259.1994 · Cited by 91 · see citing works
Self-citationReverse gyrase in thermophilic eubacteria
de la Tour, C. B., Portemer, C., Huber, R., Forterre, P., & Duguet, M. (1991) · Journal of Bacteriology · doi:10.1128/jb.173.12.3921-3923.1991 · Cited by 83 · see citing works
Self-citationGuipaud, O., Marguet, E., Noll, K. M., de la Tour, C. B., & Forterre, P. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.20.10606 · Cited by 72 · see citing works
Self-citationHyperthermophiles in the history of life.
STETTER, K. O. (1996) · PubMed · Cited by 71 · see citing works
Reverse Gyrase, the Two Domains Intimately Cooperate to Promote Positive Supercoiling
Déclais, A., Marsault, J., Confalonieri, F., de la Tour, C. B., & Duguet, M. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m910091199 · Cited by 70 · see citing works
Nisbet, E. G., & Fowler, C. M. R. (1996) · Nature · doi:10.1038/382404a0 · Cited by 57 · see citing works
Reverse Gyrase Recruitment to DNA after UV Light Irradiation in Sulfolobus solfataricus
Napoli, A., Valenti, A., Salerno, V., Nadal, M., Garnier, F., Rossi, M., & Ciaramella, M. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m402619200 · Cited by 55 · see citing works
Stępkowski, T., Brzeziński, K., Legocki, A. B., Jaskólski, M., & Béna, G. (2004) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2004.09.008 · Cited by 36 · see citing works
Hyperthermophiles in the History of Life
STETTER, K. O. (2007) · Novartis Foundation symposium · doi:10.1002/9780470514986.ch1 · Cited by 27 · see citing works
Flagged first, then by citations
Research works printed but not linked: 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.
Cited by
Sorted by citations
Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world
Koonin, E., & Wolf, Y. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn668 · Cited by 722 · see citing works
All tangled up: how cells direct, manage and exploit topoisomerase function
Vos, S. M., Tretter, E. M., Thurtle-Schmidt, B. H., & Berger, J. M. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3228 · Cited by 655 · see citing works
DNA topoisomerases: harnessing and constraining energy to govern chromosome topology
Schoeffler, A. J., & Berger, J. M. (2008) · Quarterly Reviews of Biophysics · doi:10.1017/s003358350800468x · Cited by 490 · see citing works
Spang, A., Hatzenpichler, R., Brochier‐Armanet, C., Rattei, T., Tischler, P., Spieck, E., Streit, W. R., Stahl, D. A., Wagner, M., & Schleper, C. (2010) · Trends in Microbiology · doi:10.1016/j.tim.2010.06.003 · Cited by 452 · see citing works
Self-citationOrigin and evolution of DNA topoisomerases
Forterre, P., Gribaldo, S., Gadelle, D., & Serre, M.-C. (2007) · Biochimie · doi:10.1016/j.biochi.2006.12.009 · Cited by 344 · see citing works
Self-citationNunoura, T., Takaki, Y., Kakuta, J., Nishi, S., Sugahara, J., Kazama, H., Chee, G.-J., Hattori, M., Kanai, A., Atomi, H., et al. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq1228 · Cited by 291 · see citing works
Chemistry of Abiotic Nucleotide Synthesis
Yadav, M., Kumar, R., & Krishnamurthy, R. (2020) · Chemical Reviews · doi:10.1021/acs.chemrev.9b00546 · Cited by 225 · see citing works
Forterre, P., & Gadelle, D. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp032 · Cited by 190 · see citing works
Self-citationThe universal tree of life: an update
Forterre, P. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00717 · Cited by 186 · see citing works
Self-citationCampbell, 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., et al. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000362 · Cited by 143 · see citing works
The essential genome of the crenarchaeal model Sulfolobus islandicus
Zhang, C., Phillips, A. P. R., Wipfler, R. L., Olsen, G. J., & Whitaker, R. J. (2018) · Nature Communications · doi:10.1038/s41467-018-07379-4 · Cited by 123 · see citing works
Takeuchi, N., Kaneko, K., & Koonin, E. V. (2014) · G3 Genes|Genomes|Genetics · doi:10.1534/g3.113.009845 · Cited by 125 · see citing works
Lateral Gene Transfer from the Dead
Szöllősi, G. J., Tannier, É., Lartillot, N., & Daubin, V. (2013) · Systematic Biology · doi:10.1093/sysbio/syt003 · Cited by 124 · see citing works
Horizontal Gene Transfer and the History of LifePreprint
Daubin, V., & Szöllősi, G. J. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018036 · Cited by 123 · see citing works
The Common Ancestor of Archaea and Eukarya Was Not an Archaeon
Forterre, P. (2013) · Archaea · doi:10.1155/2013/372396 · Cited by 112 · see citing works
Self-citationBacterial gene import and mesophilic adaptation in archaea
López‐García, P., Zivanovic, Y., Deschamps, P., & Moreira, D. (2015) · Nature Reviews Microbiology · doi:10.1038/nrmicro3485 · Cited by 112 · see citing works
Abby, S. S., Melcher, M., Kerou, M., Krupovìč, M., Stieglmeier, M., Rossel, C., Pfeifer, K., & Schleper, C. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.00028 · Cited by 89 · see citing works
Major players on the microbial stage: why archaea are important
Jarrell, K. F., Walters, A. D., Bochiwal, C., Borgia, J. M., Dickinson, T., & Chong, J. P. J. (2011) · Microbiology · doi:10.1099/mic.0.047837-0 · Cited by 74 · see citing works
Cavalier‐Smith, T., & Chao, E. E. Y. (2020) · PROTOPLASMA · doi:10.1007/s00709-019-01442-7 · Cited by 68 · see citing works
The Evolution of Reverse Gyrase Suggests a Nonhyperthermophilic Last Universal Common Ancestor
Catchpole, R. J., & Forterre, P. (2019) · Molecular Biology and Evolution · doi:10.1093/molbev/msz180 · Cited by 66 · see citing works
Self-citationOrita, I., Futatsuishi, R., Adachi, K., Ohira, T., Kaneko, A., Minowa, K., Suzuki, M. M., Tamura, T., Nakamura, S., Imanaka, T., et al. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky1313 · Cited by 65 · see citing works
Reverse gyrase—recent advances and current mechanistic understanding of positive DNA supercoiling
Lulchev, P., & Klostermeier, D. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku589 · Cited by 61 · see citing works
How hyperthermophiles adapt to change their lives: DNA exchange in extreme conditions
van Wolferen, M., Ajon, M., Driessen, A. J. M., & Albers, S. (2013) · Extremophiles · doi:10.1007/s00792-013-0552-6 · Cited by 57 · see citing works
Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor
Cantine, M. D., & Fournier, G. P. (2018) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-017-9542-5 · Cited by 54 · see citing works
The origin of modern terrestrial life
Forterre, P., & Gribaldo, S. (2007) · HFSP journal · doi:10.2976/1.2759103 · Cited by 54 · see citing works
Self-citationBerkemer, S. J., & McGlynn, S. E. (2020) · Molecular Biology and Evolution · doi:10.1093/molbev/msaa089 · Cited by 52 · see citing works
Reverse gyrase and genome stability in hyperthermophilic organisms
Perugino, G., Valenti, A., D’Amaro, A., Rossi, M., & Ciaramella, M. (2009) · Biochemical Society Transactions · doi:10.1042/bst0370069 · Cited by 50 · see citing works
Insights into thermoadaptation and the evolution of mesophily from the bacterial phylum Thermotogae
Pollo, S. M. J., Zhaxybayeva, O., & Nesbø, C. L. (2015) · Canadian Journal of Microbiology · doi:10.1139/cjm-2015-0073 · Cited by 46 · see citing works
The linkage between reverse gyrase and hyperthermophiles: A review of their invariable association
Heine, M., & Chandra, S. (2009) · The Journal of Microbiology · doi:10.1007/s12275-009-0019-8 · Cited by 46 · see citing works
Meyer, J. L., & Huber, J. A. (2013) · The ISME Journal · doi:10.1038/ismej.2013.206 · Cited by 45 · see citing works
Li, L., Liu, Z., Meng, D., Liu, X., Li, X., Zhang, M., Tao, J., Gu, Y., Zhong, S., & Yin, H. (2018) · Applied and Environmental Microbiology · doi:10.1128/aem.02153-18 · Cited by 45 · see citing works
Helical Chirality: a Link between Local Interactions and Global Topology in DNA
Timsit, Y., & Várnai, P. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009326 · Cited by 43 · see citing works
The legacy of Carl Woese and Wolfram Zillig: from phylogeny to landmark discoveries
Albers, S., Forterre, P., Prangishvili, D. A., & Schleper, C. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro3124 · Cited by 43 · see citing works
Self-citationNishida, H., Beppu, T., & Uéda, K. (2011) · Genomics · doi:10.1016/j.ygeno.2011.08.001 · Cited by 40 · see citing works
Yang, L., Tang, S., Huang, Y., & Zhi, X. (2015) · Genome Biology and Evolution · doi:10.1093/gbe/evv232 · Cited by 36 · see citing works
Phylogenetic systematics of microorganisms inhabiting thermal environments
Lebedinsky, A. V., Chernyh, N. A., & Bonch-Osmolovskaya, E. A. (2007) · Biochemistry (Moscow) · doi:10.1134/s0006297907120048 · Cited by 33 · see citing works
Inhibition of translesion DNA polymerase by archaeal reverse gyrase
Valenti, A., Perugino, G., Nohmi, T., Rossi, M., & Ciaramella, M. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp386 · Cited by 33 · see citing works
Gonçalves, L. G., Borges, N., Serra, F., Fernandes, P., Dopazo, H., & Santos, H. (2011) · Environmental Microbiology · doi:10.1111/j.1462-2920.2011.02621.x · Cited by 32 · see citing works
Valenti, A., Perugino, G., D’Amaro, A., Cacace, A., Napoli, A., Rossi, M., & Ciaramella, M. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn418 · Cited by 30 · see citing works
Forterre, P., Krupovìč, M., Raymann, K., & Soler, N. (2014) · Microbiology Spectrum · doi:10.1128/microbiolspec.plas-0027-2014 · Cited by 30 · see citing works
Self-citationGenome-wide identification of SF1 and SF2 helicases from archaea
Chamieh, H., Ibrahim, H. S., & Kozah, J. (2015) · Gene · doi:10.1016/j.gene.2015.10.007 · Cited by 29 · see citing works
Unravelling the mechanisms of Type 1A topoisomerases using single-molecule approaches
Spakman, D., Bakx, J. A. M., Biebricher, A. S., Peterman, E. J. G., Wuite, G. J. L., & King, G. A. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab239 · Cited by 27 · see citing works
DNA Self-Assembly: From Chirality to Evolution
Timsit, Y. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms14048252 · Cited by 28 · see citing works
The split genes of Nanoarchaeum equitans are an ancestral character
Giulio, M. D. (2008) · Gene · doi:10.1016/j.gene.2008.06.010 · Cited by 28 · see citing works
TopR2, the Second Reverse Gyrase of Sulfolobus solfataricus, Exhibits Unusual Properties
Bizard, A. H., Garnier, F., & Nadal, M. (2011) · Journal of Molecular Biology · doi:10.1016/j.jmb.2011.03.030 · Cited by 27 · see citing works
Positive supercoiling in thermophiles and mesophiles: of the good and evil
Valenti, A., Perugino, G., Rossi, M., & Ciaramella, M. (2011) · Biochemical Society Transactions · doi:10.1042/bst0390058 · Cited by 26 · see citing works
Separate and Combined Biochemical Activities of the Subunits of a Naturally Split Reverse Gyrase
Capp, C., Qian, Y., Sage, H. J., Huber, H., & Hsieh, T. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.173989 · Cited by 25 · see citing works
In vivo and in vitro protein imaging in thermophilic archaea by exploiting a novel protein tag
Visone, V., Han, W., Perugino, G., del Monaco, G., She, Q., Rossi, M., Valenti, A., & Ciaramella, M. (2017) · PLoS ONE · doi:10.1371/journal.pone.0185791 · Cited by 25 · see citing works
The Last Universal Common Ancestor of Ribosome-Encoding Organisms: Portrait of LUCA
Forterre, P. (2024) · Journal of Molecular Evolution · doi:10.1007/s00239-024-10186-9 · Cited by 26 · see citing works
Self-citationGaining and losing the thermophilic adaptation in prokaryotes
Puigbò, P., Pasamontes, A., & Garcı́a-Vallvé, S. (2007) · Trends in Genetics · doi:10.1016/j.tig.2007.10.005 · Cited by 24 · see citing works
Jamroze, A., Perugino, G., Valenti, A., Rashid, N., Rossi, M., Akhtar, M., & Ciaramella, M. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.517649 · Cited by 23 · see citing works
Horizontal gene transfer of zinc and non-zinc forms of bacterial ribosomal protein S4
Chen, K., Roberts, E., & Luthey-Schulten, Z. A. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-179 · Cited by 23 · see citing works
Visone, V., Vettone, A., Serpe, M., Valenti, A., Perugino, G., Rossi, M., & Ciaramella, M. (2014) · International Journal of Molecular Sciences · doi:10.3390/ijms150917162 · Cited by 22 · see citing works
The Molecular Determinants of Thermoadaptation:Methanococcalesas a Case Study
Lecocq, M., Groussin, M., Gouy, M., & Brochier‐Armanet, C. (2020) · Molecular Biology and Evolution · doi:10.1093/molbev/msaa312 · Cited by 22 · see citing works
Self-citationAlpha‐Bazin, B., Gorlas, A., Lagorce, A., Joulié, D., Boyer, J.-B., Dutertre, M., Gaillard, J., Lopes, A., Zivanovic, Y., Dedieu, A., et al. (2020) · Journal of Proteomics · doi:10.1016/j.jprot.2020.104044 · Cited by 21 · see citing works
Brumm, P. J., Gowda, K., Robb, F. T., & Mead, D. A. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01979 · Cited by 20 · see citing works
Wang, L., Wang, J., & Jing, C. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00471 · Cited by 20 · see citing works
Blesa, A., Sánchez‐Costa, M., Sacristán-Horcajada, E., la Fuente, S. G., Peiró‐Pastor, R., & Berenguer, J. (2019) · Microorganisms · doi:10.3390/microorganisms7010025 · Cited by 19 · see citing works
Horizontal Gene Transfers with or without Cell Fusions in All Categories of the Living Matter
Sinkovics, J. G. (2011) · Advances in experimental medicine and biology · doi:10.1007/978-94-007-0782-5_2 · Cited by 19 · see citing works
Lebedinsky, A. V., Mardanov, A. V., Kublanov, I. V., Gumerov, V. M., Beletsky, A. V., Perevalova, A. A., Bidzhieva, S. K., Bonch-Osmolovskaya, E. A., Георгиевич, С. К., & Ravin, N. V. (2013) · Extremophiles · doi:10.1007/s00792-013-0616-7 · Cited by 18 · see citing works
Vettone, A., Perugino, G., Rossi, M., Valenti, A., & Ciaramella, M. (2014) · Extremophiles · doi:10.1007/s00792-014-0662-9 · Cited by 18 · see citing works
Genomic attributes of thermophilic and hyperthermophilic bacteria and archaea
Verma, D., Kumar, V., & Satyanarayana, T. (2022) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-022-03327-z · Cited by 19 · see citing works
Horizontal Gene Transfer in Thermus spp.
Blesa, A., Averhoff, B., & Berenguer, J. (2018) · Current Issues in Molecular Biology · doi:10.21775/cimb.029.023 · Cited by 17 · see citing works
Jungblut, S. P., & Klostermeier, D. (2007) · Journal of Molecular Biology · doi:10.1016/j.jmb.2007.05.031 · Cited by 17 · see citing works
Akram, F., Haq, I. U., Shah, F. I., Aqeel, A., Ahmed, Z., Mir, A. S., Qureshi, S. S., & Raja, S. I. (2022) · Bioorganic Chemistry · doi:10.1016/j.bioorg.2022.105942 · Cited by 15 · see citing works
Introduction and Historical Perspective
Forterre, P. (2011) · Cancer drug discovery and develogment/Cancer drug discovery and development · doi:10.1007/978-1-4614-0323-4_1 · Cited by 11 · see citing works
Self-citationCouturier, M., Bizard, A. H., Garnier, F., & Nadal, M. (2014) · BMC Molecular Biology · doi:10.1186/1471-2199-15-18 · Cited by 11 · see citing works
Horizontal Gene Transfer in Microbial Ecosystems
Brochier‐Armanet, C., & Moreira, D. (2014) · Springer eBooks · doi:10.1007/978-94-017-9118-2_12 · Cited by 11 · see citing works
Self-citationLi, J., Liu, J., Zhou, J. B., & Xiang, H. (2011) · Extremophiles · doi:10.1007/s00792-011-0356-5 · Cited by 11 · see citing works
Increase of positive supercoiling in a hyperthermophilic archaeon after UV irradiation
Gorlas, A., Catchpole, R. J., Marguet, E., & Forterre, P. (2018) · Extremophiles · doi:10.1007/s00792-018-1068-x · Cited by 10 · see citing works
Self-citationZhi, X., Yao, J., Li, H., Huang, Y., & Li, W. (2014) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2014.02.015 · Cited by 10 · see citing works
Torsional stress in DNA limits collaboration among reverse gyrase molecules
Ogawa, T., Sutoh, K., Kikuchi, A., & Kinosita, K. (2016) · FEBS Journal · doi:10.1111/febs.13675 · Cited by 8 · see citing works
Detection of Biochemical Pathways by Probabilistic Matching of Phyletic Vectors
Li, H., Kristensen, D. M., Coleman, M. K., & Mushegian, A. R. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005326 · Cited by 8 · see citing works
Microbes Thriving in Extreme Environments: How Do They Do It?
Jha, P. (2014) · International Journal of Applied Sciences and Biotechnology · doi:10.3126/ijasbt.v2i4.10543 · Cited by 7 · see citing works
Hooper, S. D., Anderson, I., Pati, A., Dalevi, D., Mavromatis, K., & Kyrpides, N. C. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp075 · Cited by 7 · see citing works
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Noll, K. M., & Thirangoon, K. (2009) · Methods in molecular biology · doi:10.1007/978-1-60327-853-9_18 · Cited by 7 · see citing works
Assembling networks of microbial genomes using linear programming
Holloway, C., & Beiko, R. G. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-360 · Cited by 5 · see citing works
Egel, R. (2017) · Preprints.org · doi:10.20944/preprints201710.0153.v1 · Cited by 5 · see citing works
Untangling bacterial DNA topoisomerases functions
Borde, C., Bruno, L., & Espéli, O. (2024) · Biochemical Society Transactions · doi:10.1042/bst20240089 · Cited by 4 · see citing works
Life in a multi-extreme environment: Thermococcales living in deep sea hydrothermal vents
Zhao, W., & Xiang, X. I. A. O. (2017) · Scientia Sinica Vitae · doi:10.1360/n052017-00056 · Cited by 4 · see citing works
Complete Genome Sequence of Pseudoxanthomonas taiwanensis AL17 and its Potential Genes
Afifah, D. N., Brigiyanti, L. N., Widhiastuty, M. P., Restiawaty, E., & Akhmaloka, A. (2024) · Journal of Pure and Applied Microbiology · doi:10.22207/jpam.18.4.33 · Cited by 2 · see citing works
Forterre, P., Krupovìč, M., Raymann, K., & Soler, N. (2015) · ASM Press eBooks · doi:10.1128/9781555818982.ch20 · Cited by 2 · see citing works
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Wani, A. K., Dhanjal, D. S., Chopra, C., & Singh, R. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-98394-5.00004-3 · Cited by 1 · see citing works
Depletion of CpG dinucleotides in bacterial genomes may represent an adaptation to high temperatures
Forni, D., Pozzoli, U., Mozzi, A., Cagliani, R., & Sironi, M. (2024) · NAR Genomics and Bioinformatics · doi:10.1093/nargab/lqae088 · Cited by 1 · see citing works
González-Siso, M.-I. (2019) · MDPI eBooks · doi:10.3390/books978-3-03897-817-6 · Cited by 1 · see citing works
Forterre, P. (2025) · Wiley eBooks · doi:10.1002/9781394351848.ch3 · Cited by 1 · see citing works
Self-citationPollo, S. M. J. (2014) · ERA: Education and Research Archive (University of Alberta) · doi:10.7939/r34s1d
Computational genomics of hyperthermophiles
van de Werken, H. J. G. (2008) · doi:10.18174/16325
Structure and Function of Helicases in Archaea the Third Domain of Life
Huang, Q.-H., Ahmad, S., Zhai, B., & Shen, Y.-L. (2019) · Helicases from All Domains of Life · doi:10.1016/b978-0-12-814685-9.00002-6
Forterre, P., Cunha, V. D., & Gaïa, M. (2018) · Wiley eBooks · doi:10.1002/9780470015902.a0001525.pub3 · Cited by 1 · see citing works
Self-citationStolz, A. (2017) · Springer eBooks · doi:10.1007/978-3-662-55595-8_2
Wäber, N. B., & Hartmann, R. K. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-809633-8.20783-8
Industrial Marvels of Extreme Microbial Adaptations
Priscilla, R. A., & Saleena, L. M. (2024) · Springer eBooks · doi:10.1007/978-981-97-6270-5_31
Evolution of Archaea and Their Taxonomy
Forterre, P. (2025) · doi:10.1002/9781394351848.ch2
Self-citationLv, Z., Wang, Y., & Wang, Y. (2026) · The Innovation Life · doi:10.59717/j.xinn-life.2026.100235
- Authors
- Brochier-Armanet, C., & Forterre, P.
- Affiliations
- Université Paris-Sud (FR)
- ORCID
- Forterre, Patrick
- Venue
- Archaea
- Publisher
- Wiley
- Published
- 2006-05-26
- Volume
- 2
- Issue
- 2
- Pages
- 83-93
- ISSN
- 1472-3646 (ISSN-L)
- 1472-3654
- PMC
- PMC2686386
- 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
- hybrid
- doi.org
- Licence
- 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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