A Novel Redox-Sensing Histidine Kinase That Controls Carbon Catabolite Repression in <italic toggle="yes">Azoarcus</italic> sp. CIB

ABSTRACT We have identified and characterized the AccS multidomain sensor kinase that mediates the activation of the AccR master regulator involved in carbon catabolite repression (CCR) of the anaerobic catabolism of aromatic compounds in Azoarcus sp. CIB. A truncated AccS protein that contains only...

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Autores principales:	J. Andrés Valderrama, Helena Gómez-Álvarez, Zaira Martín-Moldes, M. Álvaro Berbís, F. Javier Cañada, Gonzalo Durante-Rodríguez, Eduardo Díaz
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	catabolite repression quinones redox switch sensor kinase Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/30e0602224694fca96311536bc542b48
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spelling	oai:doaj.org-article:30e0602224694fca96311536bc542b482021-11-15T15:55:24ZA Novel Redox-Sensing Histidine Kinase That Controls Carbon Catabolite Repression in <italic toggle="yes">Azoarcus</italic> sp. CIB10.1128/mBio.00059-192150-7511https://doaj.org/article/30e0602224694fca96311536bc542b482019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00059-19https://doaj.org/toc/2150-7511ABSTRACT We have identified and characterized the AccS multidomain sensor kinase that mediates the activation of the AccR master regulator involved in carbon catabolite repression (CCR) of the anaerobic catabolism of aromatic compounds in Azoarcus sp. CIB. A truncated AccS protein that contains only the soluble C-terminal autokinase module (AccS′) accounts for the succinate-dependent CCR control. In vitro assays with purified AccS′ revealed its autophosphorylation, phosphotransfer from AccS′∼P to the Asp60 residue of AccR, and the phosphatase activity toward its phosphorylated response regulator, indicating that the equilibrium between the kinase and phosphatase activities of AccS′ may control the phosphorylation state of the AccR transcriptional regulator. Oxidized quinones, e.g., ubiquinone 0 and menadione, switched the AccS′ autokinase activity off, and three conserved Cys residues, which are not essential for catalysis, are involved in such inhibition. Thiol oxidation by quinones caused a change in the oligomeric state of the AccS′ dimer resulting in the formation of an inactive monomer. This thiol-based redox switch is tuned by the cellular energy state, which can change depending on the carbon source that the cells are using. This work expands the functional diversity of redox-sensitive sensor kinases, showing that they can control new bacterial processes such as CCR of the anaerobic catabolism of aromatic compounds. The AccSR two-component system is conserved in the genomes of some betaproteobacteria, where it might play a more general role in controlling the global metabolic state according to carbon availability. IMPORTANCE Two-component signal transduction systems comprise a sensor histidine kinase and its cognate response regulator, and some have evolved to sense and convert redox signals into regulatory outputs that allow bacteria to adapt to the altered redox environment. The work presented here expands knowledge of the functional diversity of redox-sensing kinases to control carbon catabolite repression (CCR), a phenomenon that allows the selective assimilation of a preferred compound among a mixture of several carbon sources. The newly characterized AccS sensor kinase is responsible for the phosphorylation and activation of the AccR master regulator involved in CCR of the anaerobic degradation of aromatic compounds in the betaproteobacterium Azoarcus sp. CIB. AccS seems to have a thiol-based redox switch that is modulated by the redox state of the quinone pool. The AccSR system is conserved in several betaproteobacteria, where it might play a more general role controlling their global metabolic state.J. Andrés ValderramaHelena Gómez-ÁlvarezZaira Martín-MoldesM. Álvaro BerbísF. Javier CañadaGonzalo Durante-RodríguezEduardo DíazAmerican Society for Microbiologyarticlecatabolite repressionquinonesredox switchsensor kinaseMicrobiologyQR1-502ENmBio, Vol 10, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	catabolite repression quinones redox switch sensor kinase Microbiology QR1-502
spellingShingle	catabolite repression quinones redox switch sensor kinase Microbiology QR1-502 J. Andrés Valderrama Helena Gómez-Álvarez Zaira Martín-Moldes M. Álvaro Berbís F. Javier Cañada Gonzalo Durante-Rodríguez Eduardo Díaz A Novel Redox-Sensing Histidine Kinase That Controls Carbon Catabolite Repression in <italic toggle="yes">Azoarcus</italic> sp. CIB
description	ABSTRACT We have identified and characterized the AccS multidomain sensor kinase that mediates the activation of the AccR master regulator involved in carbon catabolite repression (CCR) of the anaerobic catabolism of aromatic compounds in Azoarcus sp. CIB. A truncated AccS protein that contains only the soluble C-terminal autokinase module (AccS′) accounts for the succinate-dependent CCR control. In vitro assays with purified AccS′ revealed its autophosphorylation, phosphotransfer from AccS′∼P to the Asp60 residue of AccR, and the phosphatase activity toward its phosphorylated response regulator, indicating that the equilibrium between the kinase and phosphatase activities of AccS′ may control the phosphorylation state of the AccR transcriptional regulator. Oxidized quinones, e.g., ubiquinone 0 and menadione, switched the AccS′ autokinase activity off, and three conserved Cys residues, which are not essential for catalysis, are involved in such inhibition. Thiol oxidation by quinones caused a change in the oligomeric state of the AccS′ dimer resulting in the formation of an inactive monomer. This thiol-based redox switch is tuned by the cellular energy state, which can change depending on the carbon source that the cells are using. This work expands the functional diversity of redox-sensitive sensor kinases, showing that they can control new bacterial processes such as CCR of the anaerobic catabolism of aromatic compounds. The AccSR two-component system is conserved in the genomes of some betaproteobacteria, where it might play a more general role in controlling the global metabolic state according to carbon availability. IMPORTANCE Two-component signal transduction systems comprise a sensor histidine kinase and its cognate response regulator, and some have evolved to sense and convert redox signals into regulatory outputs that allow bacteria to adapt to the altered redox environment. The work presented here expands knowledge of the functional diversity of redox-sensing kinases to control carbon catabolite repression (CCR), a phenomenon that allows the selective assimilation of a preferred compound among a mixture of several carbon sources. The newly characterized AccS sensor kinase is responsible for the phosphorylation and activation of the AccR master regulator involved in CCR of the anaerobic degradation of aromatic compounds in the betaproteobacterium Azoarcus sp. CIB. AccS seems to have a thiol-based redox switch that is modulated by the redox state of the quinone pool. The AccSR system is conserved in several betaproteobacteria, where it might play a more general role controlling their global metabolic state.
format	article
author	J. Andrés Valderrama Helena Gómez-Álvarez Zaira Martín-Moldes M. Álvaro Berbís F. Javier Cañada Gonzalo Durante-Rodríguez Eduardo Díaz
author_facet	J. Andrés Valderrama Helena Gómez-Álvarez Zaira Martín-Moldes M. Álvaro Berbís F. Javier Cañada Gonzalo Durante-Rodríguez Eduardo Díaz
author_sort	J. Andrés Valderrama
title	A Novel Redox-Sensing Histidine Kinase That Controls Carbon Catabolite Repression in <italic toggle="yes">Azoarcus</italic> sp. CIB
title_short	A Novel Redox-Sensing Histidine Kinase That Controls Carbon Catabolite Repression in <italic toggle="yes">Azoarcus</italic> sp. CIB
title_full	A Novel Redox-Sensing Histidine Kinase That Controls Carbon Catabolite Repression in <italic toggle="yes">Azoarcus</italic> sp. CIB
title_fullStr	A Novel Redox-Sensing Histidine Kinase That Controls Carbon Catabolite Repression in <italic toggle="yes">Azoarcus</italic> sp. CIB
title_full_unstemmed	A Novel Redox-Sensing Histidine Kinase That Controls Carbon Catabolite Repression in <italic toggle="yes">Azoarcus</italic> sp. CIB
title_sort	novel redox-sensing histidine kinase that controls carbon catabolite repression in <italic toggle="yes">azoarcus</italic> sp. cib
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/30e0602224694fca96311536bc542b48
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A Novel Redox-Sensing Histidine Kinase That Controls Carbon Catabolite Repression in <italic toggle="yes">Azoarcus</italic> sp. CIB

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