Abstract
Rhodobacter capsulatus regulates many metabolic processes in response to the level of environmental oxygen and the energy state of the cell. One of the key global redox regulators of the cell's metabolic physiology is the sensor kinase RegB that controls the synthesis of numerous energy generation and utilization processes. In this study, we have succeeded in purifying full-length RegB containing six transmembrane-spanning elements. Exogenous addition of excess oxidized coenzyme Q1 is capable of inhibiting RegB autophosphorylation approximately 6-fold. However, the addition of reduced coenzyme Q1 exhibits no inhibitory effect on kinase activity. A ubiquinone-binding site, as defined by azidoquinone photo affinity cross-linking, was determined to lie within a periplasmic loop between transmembrane helices 3 and 4 that contains a fully conserved heptapeptide sequence of GGXXNPF. Mutation of the phenylalanine in this heptapeptide renders RegB constitutively active in vivo, indicating that this domain is responsible for sensing the redox state of the ubiquinone pool and subsequently controlling RegB autophosphorylation.
MeSH Terms
Amino Acid Sequence
Bacterial Proteins/antagonists & inhibitors,genetics,isolation & purification,metabolism
Binding Sites
Blotting, Northern
DNA Mutational Analysis
Molecular Sequence Data
Oxidation-Reduction
Phosphorylation
Protein Kinases/genetics,isolation & purification,metabolism
Protein Structure, Secondary
Protein Structure, Tertiary
Rhodobacter capsulatus/enzymology,genetics,metabolism
Spectrophotometry
Ubiquinone/metabolism
Chemicals
Bacterial Proteins
RegB protein, Rhodobacter
Ubiquinone
Protein Kinases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Swem Lee R
Department of Biology, Indiana University, Bloomington, Indiana 47405, USA.
Gong Xing
Yu Chang-An
Bauer Carl E
References (28)
28 references, click to expand
-
Identification of a Mr = 17,000 protein as the plastoquinone-binding protein in the cytochrome b6-f complex from spinach chloroplasts.
J Biol Chem. 1989 Jan 25;264(3):1387-92
PMID: 2912961
-
Site-directed mutagenesis by overlap extension using the polymerase chain reaction.
Gene. 1989 Apr 15;77(1):51-9
PMID: 2744487
-
Ubiquinone binding domains in bovine heart mitochondrial cytochrome b.
J Biol Chem. 1994 Jan 21;269(3):2292-8
PMID: 8294488
-
Characterization of a light-responding trans-activator responsible for differentially controlling reaction center and light-harvesting-I gene expression in Rhodobacter capsulatus.
J Bacteriol. 1994 Nov;176(22):6936-43
PMID: 7961455
-
Identification of the ubiquinol-binding site in the cytochrome bo3-ubiquinol oxidase of Escherichia coli.
J Biol Chem. 1994 Nov 18;269(46):28834-8
PMID: 7961841
-
Autophosphorylation, phosphotransfer, and DNA-binding properties of the RegB/RegA two-component regulatory system in Rhodobacter capsulatus.
J Biol Chem. 1999 Jun 4;274(23):16343-8
PMID: 10347192
-
Identification of the ubiquinone-binding domain in QPs1 of succinate-ubiquinone reductase.
J Biol Chem. 1995 Mar 17;270(11):6193-8
PMID: 7890754
-
The smallest membrane anchoring subunit (QPs3) of bovine heart mitochondrial succinate-ubiquinone reductase. Cloning, sequencing, topology, and Q-binding domain.
J Biol Chem. 1997 Jul 11;272(28):17867-72
PMID: 9211943
-
The quinone-binding site in succinate-ubiquinone reductase from Escherichia coli. Quinone-binding domain and amino acid residues involved in quinone binding.
J Biol Chem. 1998 Nov 27;273(48):31916-23
PMID: 9822661
-
Topological analysis of the membrane-localized redox-responsive sensor kinase PrrB from Rhodobacter sphaeroides 2.4.1.
J Biol Chem. 1999 Jun 11;274(24):17290-6
PMID: 10358089
-
Expression of uptake hydrogenase and molybdenum nitrogenase in Rhodobacter capsulatus is coregulated by the RegB-RegA two-component regulatory system.
J Bacteriol. 2000 May;182(10):2831-7
PMID: 10781552
-
Interaction of CbbR and RegA* transcription regulators with the Rhodobacter sphaeroides cbbIPromoter-operator region.
J Biol Chem. 2000 Jun 23;275(25):19224-30
PMID: 10748066
-
Disulfide bonds are generated by quinone reduction.
J Biol Chem. 2000 Aug 25;275(34):26082-8
PMID: 10854438
-
Quinones as the redox signal for the arc two-component system of bacteria.
Science. 2001 Jun 22;292(5525):2314-6
PMID: 11423658
-
The default state of the membrane-localized histidine kinase PrrB of Rhodobacter sphaeroides 2.4.1 is in the kinase-positive mode.
J Bacteriol. 2001 Dec;183(23):6807-14
PMID: 11698369
-
Identification of the ubiquinone-binding domain in the disulfide catalyst disulfide bond protein B.
J Biol Chem. 2002 Jan 18;277(3):1649-52
PMID: 11698406
-
Expression, purification and characterisation of full-length histidine protein kinase RegB from Rhodobacter sphaeroides.
J Mol Biol. 2002 Jul 5;320(2):201-13
PMID: 12079379
-
The unorthodox histidine kinases BvgS and EvgS are responsive to the oxidation status of a quinone electron carrier.
Eur J Biochem. 2002 Jul;269(14):3479-84
PMID: 12135487
-
The ubiquinone-binding site in NADH:ubiquinone oxidoreductase from Escherichia coli.
J Biol Chem. 2003 Jul 11;278(28):25731-7
PMID: 12730198
-
Signal transduction by the global regulator RegB is mediated by a redox-active cysteine.
EMBO J. 2003 Sep 15;22(18):4699-708
PMID: 12970182
-
RegB/RegA, a highly conserved redox-responding global two-component regulatory system.
Microbiol Mol Biol Rev. 2004 Jun;68(2):263-79
PMID: 15187184
-
Reconstitution of the Rhodobacter sphaeroides cbb3-PrrBA signal transduction pathway in vitro.
Biochemistry. 2004 Jun 22;43(24):7915-23
PMID: 15196036
-
Identification of a quinone-sensitive redox switch in the ArcB sensor kinase.
Proc Natl Acad Sci U S A. 2004 Sep 7;101(36):13318-23
PMID: 15326287
-
Growth of a photosynthetic bacterium anaerobically in darkness, supported by "oxidant-dependent" sugar fermentation.
Arch Microbiol. 1978 May 30;117(2):119-22
PMID: 678017
-
Properties of bovine heart mitochondrial cytochrome b560.
J Biol Chem. 1987 Jan 25;262(3):1137-43
PMID: 3027080
-
Interaction and identification of ubiquinone-binding proteins in ubiquinol-cytochrome c reductase by azido-ubiquinone derivatives.
J Biol Chem. 1985 Jan 25;260(2):963-73
PMID: 2981854
-
Identification of ubiquinone-binding proteins in yeast mitochondrial ubiquinol-cytochrome c reductase using an azido-ubiquinone derivative.
Biochim Biophys Acta. 1986 Mar 12;848(3):305-11
PMID: 3004577
-
Use of an azido-ubiquinone derivative to identify subunit I as the ubiquinol binding site of the cytochrome d terminal oxidase complex of Escherichia coli.
J Biol Chem. 1986 Nov 15;261(32):14987-90
PMID: 3533929