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How this complex system emerged in the course of evolution is poorly understood. Intriguingly, a single horizontal gene transfer event led to the successful establishment of bacterial gyrase in Archaea, but its emergent function remains a mystery. To better understand the challenges associated with the establishment of pervasive negative supercoiling activity, we expressed the gyrase of the bacterium Thermotoga maritima in a na\u00efve archaeon Thermococcus kodakarensis which naturally has positively supercoiled DNA. We found that the gyrase was catalytically active in T. kodakarensis leading to strong negative supercoiling of plasmid DNA which was stably maintained over at least eighty generations. An increased sensitivity of gyrase-expressing T. kodakarensis to ciprofloxacin suggested that gyrase also modulated chromosomal topology. Accordingly, global transcriptome analyses revealed large scale gene expression deregulation and identified a subset of genes responding to the negative supercoiling activity of gyrase. Surprisingly, the artificially introduced dominant negative supercoiling activity did not have a measurable effect on T. kodakarensis growth rate. Our data suggest that gyrase can become established in Thermococcales archaea without critically interfering with DNA transaction processes.<\/jats:p>","DOI":"10.1093\/nar\/gkab869","type":"journal-article","created":{"date-parts":[[2021,11,9]],"date-time":"2021-11-09T20:17:45Z","timestamp":1636489065000},"page":"12332-12347","source":"Crossref","is-referenced-by-count":13,"title":["The hyperthermophilic archaeon <i>Thermococcus kodakarensis<\/i> is resistant to pervasive negative supercoiling activity of DNA gyrase"],"prefix":"10.1093","volume":"49","author":[{"given":"Paul","family":"Villain","sequence":"first","affiliation":[{"name":"Universit\u00e9 Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 91198\u00a0Gif-sur-Yvette, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Violette","family":"da\u00a0Cunha","sequence":"additional","affiliation":[{"name":"Universit\u00e9 Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 91198\u00a0Gif-sur-Yvette, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Etienne","family":"Villain","sequence":"additional","affiliation":[{"name":"Immunology department, Institut Pasteur, Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patrick","family":"Forterre","sequence":"additional","affiliation":[{"name":"Universit\u00e9 Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 91198\u00a0Gif-sur-Yvette, France"},{"name":"Archaeal Virology Unit, Institut Pasteur, Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1680-636X","authenticated-orcid":false,"given":"Jacques","family":"Oberto","sequence":"additional","affiliation":[{"name":"Universit\u00e9 Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 91198\u00a0Gif-sur-Yvette, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ryan","family":"Catchpole","sequence":"additional","affiliation":[{"name":"Universit\u00e9 Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 91198\u00a0Gif-sur-Yvette, France"},{"name":"Department of Biochemistry and Molecular Biology, University of Georgia, Athens, GA 30602, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1944-7593","authenticated-orcid":false,"given":"Tamara","family":"Basta","sequence":"additional","affiliation":[{"name":"Universit\u00e9 Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 91198\u00a0Gif-sur-Yvette, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2021,11,10]]},"reference":[{"key":"2021120508580715200_B1","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1038\/171737a0","article-title":"Molecular structure of nucleic acids: a structure for deoxyribose nucleic acid","volume":"171","author":"Watson","year":"1953","journal-title":"Nature"},{"key":"2021120508580715200_B2","doi-asserted-by":"crossref","first-page":"7024","DOI":"10.1073\/pnas.84.20.7024","article-title":"Supercoiling of the DNA template during transcription","volume":"84","author":"Liu","year":"1987","journal-title":"Proc. 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