Hierarchical control of nitrite respiration by transcription factors encoded within mobile gene clusters of Thermus thermophilus

Denitrification in Thermus thermophilus is encoded by the nitrate respiration conjugative element (NCE) and nitrite and nitric oxide respiration (nic) gene clusters. A tight coordination of each cluster’s expression is required to maximize anaerobic growth, and to avoid toxicity by intermediates, es...

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Detalles Bibliográficos
Autores: Álvarez, Laura, Quintáns, Nieves G., Blesa, Alba, Baquedano, Ignacio, Mencía, Mario, Bricio, Carlos, Berenguer, José
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2017
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/166070
Acceso en línea:http://hdl.handle.net/10261/166070
Access Level:acceso abierto
Palabra clave:Nitrite respiration
Regulation
Denitrification
Thermus thermophilus
Thermophiles
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spelling Hierarchical control of nitrite respiration by transcription factors encoded within mobile gene clusters of Thermus thermophilusÁlvarez, LauraQuintáns, Nieves G.Blesa, AlbaBaquedano, IgnacioMencía, MarioBricio, CarlosBerenguer, JoséNitrite respirationRegulationDenitrificationThermus thermophilusThermophilesDenitrification in Thermus thermophilus is encoded by the nitrate respiration conjugative element (NCE) and nitrite and nitric oxide respiration (nic) gene clusters. A tight coordination of each cluster’s expression is required to maximize anaerobic growth, and to avoid toxicity by intermediates, especially nitric oxides (NO). Here, we study the control of the nitrite reductases (Nir) and NO reductases (Nor) upon horizontal acquisition of the NCE and nic clusters by a formerly aerobic host. Expression of the nic promoters PnirS, PnirJ, and PnorC, depends on the oxygen sensor DnrS and on the DnrT protein, both NCE-encoded. NsrR, a nic-encoded transcription factor with an iron–sulfur cluster, is also involved in Nir and Nor control. Deletion of nsrR decreased PnorC and PnirJ transcription, and activated PnirS under denitrification conditions, exhibiting a dual regulatory role never described before for members of the NsrR family. On the basis of these results, a regulatory hierarchy is proposed, in which under anoxia, there is a pre-activation of the nic promoters by DnrS and DnrT, and then NsrR leads to Nor induction and Nir repression, likely as a second stage of regulation that would require NO detection, thus avoiding accumulation of toxic levels of NO. The whole system appears to work in remarkable coordination to function only when the relevant nitrogen species are present inside the cell.Spanish Ministry of Economy and Competitiveness, and grant No. 685474 from the H2020 research and innovation program, respectively, of the European Union. An institutional grant from Fundación Ramón Areces to the Centro de Biología Molecular Severo Ochoa (CBMSO)Peer ReviewedMultidisciplinary Digital Publishing InstituteConsejo Superior de Investigaciones Científicas (España)Ministerio de Economía y Competitividad (España)Fundación Ramón ArecesConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2018201820172018info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versionPublisher's versioninfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/166070reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)InglésSíinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/1660702026-05-22T06:33:51Z
dc.title.none.fl_str_mv Hierarchical control of nitrite respiration by transcription factors encoded within mobile gene clusters of Thermus thermophilus
title Hierarchical control of nitrite respiration by transcription factors encoded within mobile gene clusters of Thermus thermophilus
spellingShingle Hierarchical control of nitrite respiration by transcription factors encoded within mobile gene clusters of Thermus thermophilus
Álvarez, Laura
Nitrite respiration
Regulation
Denitrification
Thermus thermophilus
Thermophiles
title_short Hierarchical control of nitrite respiration by transcription factors encoded within mobile gene clusters of Thermus thermophilus
title_full Hierarchical control of nitrite respiration by transcription factors encoded within mobile gene clusters of Thermus thermophilus
title_fullStr Hierarchical control of nitrite respiration by transcription factors encoded within mobile gene clusters of Thermus thermophilus
title_full_unstemmed Hierarchical control of nitrite respiration by transcription factors encoded within mobile gene clusters of Thermus thermophilus
title_sort Hierarchical control of nitrite respiration by transcription factors encoded within mobile gene clusters of Thermus thermophilus
dc.creator.none.fl_str_mv Álvarez, Laura
Quintáns, Nieves G.
Blesa, Alba
Baquedano, Ignacio
Mencía, Mario
Bricio, Carlos
Berenguer, José
author Álvarez, Laura
author_facet Álvarez, Laura
Quintáns, Nieves G.
Blesa, Alba
Baquedano, Ignacio
Mencía, Mario
Bricio, Carlos
Berenguer, José
author_role author
author2 Quintáns, Nieves G.
Blesa, Alba
Baquedano, Ignacio
Mencía, Mario
Bricio, Carlos
Berenguer, José
author2_role author
author
author
author
author
author
dc.contributor.none.fl_str_mv Consejo Superior de Investigaciones Científicas (España)
Ministerio de Economía y Competitividad (España)
Fundación Ramón Areces
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Nitrite respiration
Regulation
Denitrification
Thermus thermophilus
Thermophiles
topic Nitrite respiration
Regulation
Denitrification
Thermus thermophilus
Thermophiles
description Denitrification in Thermus thermophilus is encoded by the nitrate respiration conjugative element (NCE) and nitrite and nitric oxide respiration (nic) gene clusters. A tight coordination of each cluster’s expression is required to maximize anaerobic growth, and to avoid toxicity by intermediates, especially nitric oxides (NO). Here, we study the control of the nitrite reductases (Nir) and NO reductases (Nor) upon horizontal acquisition of the NCE and nic clusters by a formerly aerobic host. Expression of the nic promoters PnirS, PnirJ, and PnorC, depends on the oxygen sensor DnrS and on the DnrT protein, both NCE-encoded. NsrR, a nic-encoded transcription factor with an iron–sulfur cluster, is also involved in Nir and Nor control. Deletion of nsrR decreased PnorC and PnirJ transcription, and activated PnirS under denitrification conditions, exhibiting a dual regulatory role never described before for members of the NsrR family. On the basis of these results, a regulatory hierarchy is proposed, in which under anoxia, there is a pre-activation of the nic promoters by DnrS and DnrT, and then NsrR leads to Nor induction and Nir repression, likely as a second stage of regulation that would require NO detection, thus avoiding accumulation of toxic levels of NO. The whole system appears to work in remarkable coordination to function only when the relevant nitrogen species are present inside the cell.
publishDate 2017
dc.date.none.fl_str_mv 2017
2018
2018
2018
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
Publisher's version
info:eu-repo/semantics/publishedVersion
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/166070
url http://hdl.handle.net/10261/166070
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Multidisciplinary Digital Publishing Institute
publisher.none.fl_str_mv Multidisciplinary Digital Publishing Institute
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,811543

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