Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Alvarez, Laura, G. Quintáns, Nieves, Blesa, Alba, Baquedano, Ignacio, Mencía, Mario, Bricio, Carlos, Berenguer, José
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5748679/
https://www.ncbi.nlm.nih.gov/pubmed/29194386
http://dx.doi.org/10.3390/genes8120361
_version_ 1783289447741128704
author Alvarez, Laura
G. Quintáns, Nieves
Blesa, Alba
Baquedano, Ignacio
Mencía, Mario
Bricio, Carlos
Berenguer, José
author_facet Alvarez, Laura
G. Quintáns, Nieves
Blesa, Alba
Baquedano, Ignacio
Mencía, Mario
Bricio, Carlos
Berenguer, José
author_sort Alvarez, Laura
collection PubMed
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.
format Online
Article
Text
id pubmed-5748679
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-57486792018-01-07 Hierarchical Control of Nitrite Respiration by Transcription Factors Encoded within Mobile Gene Clusters of Thermus thermophilus Alvarez, Laura G. Quintáns, Nieves Blesa, Alba Baquedano, Ignacio Mencía, Mario Bricio, Carlos Berenguer, José Genes (Basel) Article 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. MDPI 2017-12-01 /pmc/articles/PMC5748679/ /pubmed/29194386 http://dx.doi.org/10.3390/genes8120361 Text en © 2017 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Alvarez, Laura
G. Quintáns, Nieves
Blesa, Alba
Baquedano, Ignacio
Mencía, Mario
Bricio, Carlos
Berenguer, José
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
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_short 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
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5748679/
https://www.ncbi.nlm.nih.gov/pubmed/29194386
http://dx.doi.org/10.3390/genes8120361
work_keys_str_mv AT alvarezlaura hierarchicalcontrolofnitriterespirationbytranscriptionfactorsencodedwithinmobilegeneclustersofthermusthermophilus
AT gquintansnieves hierarchicalcontrolofnitriterespirationbytranscriptionfactorsencodedwithinmobilegeneclustersofthermusthermophilus
AT blesaalba hierarchicalcontrolofnitriterespirationbytranscriptionfactorsencodedwithinmobilegeneclustersofthermusthermophilus
AT baquedanoignacio hierarchicalcontrolofnitriterespirationbytranscriptionfactorsencodedwithinmobilegeneclustersofthermusthermophilus
AT menciamario hierarchicalcontrolofnitriterespirationbytranscriptionfactorsencodedwithinmobilegeneclustersofthermusthermophilus
AT briciocarlos hierarchicalcontrolofnitriterespirationbytranscriptionfactorsencodedwithinmobilegeneclustersofthermusthermophilus
AT berenguerjose hierarchicalcontrolofnitriterespirationbytranscriptionfactorsencodedwithinmobilegeneclustersofthermusthermophilus