Involvement of SenC in Assembly of Cytochrome c Oxidase in Rhodobacter capsulatus

ABSTRACT SenC, a Sco1 homolog found in the purple photosynthetic bacteria, has been implicated in affecting photosynthesis and respiratory gene expression, as well as assembly of cytochrome c oxidase. In this study, we show that SenC from Rhodobacter capsulatus is involved in the assembly of a fully functional cbb3-type cytochrome c oxidase, as revealed by decreased cytochrome c oxidase activity in a senC mutant. We also show that a putative copper-binding site in SenC is required for activity and that a SenC deletion phenotype can be rescued by the addition of exogenous copper to the growth medium. In addition, we demonstrate that a SenC mutation has an indirect effect on gene expression caused by a reduction in cytochrome c oxidase activity. A model is proposed whereby a reduction in cytochrome c oxidase activity impedes the flow of electrons through the respiratory pathway, thereby affecting the oxidation/reduction state of the ubiquinone pool, leading to alterations of photosystem and respiratory gene expression.

[1]  E. Schon,et al.  Crystal Structure of Human SCO1 , 2005, Journal of Biological Chemistry.

[2]  Z. Jia,et al.  Identification of a disulfide switch in BsSco, a member of the Sco family of cytochrome c oxidase assembly proteins. , 2005, Biochemistry.

[3]  D. Winge,et al.  Specific Copper Transfer from the Cox17 Metallochaperone to Both Sco1 and Cox11 in the Assembly of Yeast Cytochrome c Oxidase* , 2004, Journal of Biological Chemistry.

[4]  S. Kaplan,et al.  Reconstitution of the Rhodobacter sphaeroides cbb3-PrrBA signal transduction pathway in vitro. , 2004, Biochemistry.

[5]  G. Rödel,et al.  Yeast SCO1 protein is required for a post-translational step in the accumulation of mitochondrial cytochrome c oxidase subunits I and II , 1990, Current Genetics.

[6]  C. Bauer,et al.  Gentic evidence for superoperonal organization of genes for photosynthesis pigments and pigment-binding proteins in Rhodobacter capsulatus , 1989, Molecular and General Genetics MGG.

[7]  G. Rödel,et al.  SCO1, a yeast nuclear gene essential for accumulation of mitochondrial cytochrome c oxidase subunit II , 1988, Molecular and General Genetics MGG.

[8]  Ivano Bertini,et al.  Solution structure of Sco1: a thioredoxin-like protein Involved in cytochrome c oxidase assembly. , 2003, Structure.

[9]  A. McEwan,et al.  PrrC from Rhodobacter sphaeroides, a homologue of eukaryotic Sco proteins, is a copper‐binding protein and may have a thiol‐disulfide oxidoreductase activity , 2002, FEBS letters.

[10]  N. Watmough,et al.  Cytochrome cbb(3) oxidase and bacterial microaerobic metabolism. , 2001, Biochemical Society transactions.

[11]  F. Daldal,et al.  The RegB/RegA two-component regulatory system controls synthesis of photosynthesis and respiratory electron transfer components in Rhodobacter capsulatus. , 2001, Journal of molecular biology.

[12]  A. Lode,et al.  The P(174)L mutation in the human hSCO1 gene affects the assembly of cytochrome c oxidase. , 2000, Biochemical and biophysical research communications.

[13]  B. Hill,et al.  Characterization of YpmQ, an Accessory Protein Required for the Expression of Cytochrome c Oxidase in Bacillus subtilis * , 2000, The Journal of Biological Chemistry.

[14]  Y. Chinenov,et al.  Cytochrome c oxidase assembly factors with a thioredoxin fold are conserved among prokaryotes and eukaryotes , 2000, Journal of Molecular Medicine.

[15]  F. Daldal,et al.  Roles of the ccoGHIS gene products in the biogenesis of the cbb(3)-type cytochrome c oxidase. , 2000, Journal of molecular biology.

[16]  S. Kaplan,et al.  From redox flow to gene regulation: role of the PrrC protein of Rhodobacter sphaeroides 2.4.1. , 2000, Biochemistry.

[17]  B. Barrell,et al.  The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences , 2000, Nature.

[18]  D. Glerum,et al.  SCO1 and SCO2 Act as High Copy Suppressors of a Mitochondrial Copper Recruitment Defect in Saccharomyces cerevisiae* , 1996, The Journal of Biological Chemistry.

[19]  H. Hennecke,et al.  Assembly and Function of the Cytochrome cbb Oxidase Subunits in Bradyrhizobium japonicum(*) , 1996, The Journal of Biological Chemistry.

[20]  C. Bauer,et al.  Cloning and characterization of senC, a gene involved in both aerobic respiration and photosynthesis gene expression in Rhodobacter capsulatus , 1995, Journal of bacteriology.

[21]  F. Daldal,et al.  Membrane-associated cytochrome cy of Rhodobacter capsulatus is an electron carrier from the cytochrome bc1 complex to the cytochrome c oxidase during respiration , 1995, Journal of bacteriology.

[22]  C. Bauer,et al.  Characterization of a light-responding trans-activator responsible for differentially controlling reaction center and light-harvesting-I gene expression in Rhodobacter capsulatus , 1994, Journal of bacteriology.

[23]  C. Slaughter,et al.  Rhodobacter capsulatus contains a novel cb-type cytochrome c oxidase without a CuA center. , 1994, Biochemistry.

[24]  C. Bauer,et al.  Nucleotide sequence and characterization of the Rhodobacter capsulatus hvrB gene: HvrB is an activator of S-adenosyl-L-homocysteine hydrolase expression and is a member of the LysR family , 1994, Journal of bacteriology.

[25]  C. Locht,et al.  Isolation and molecular characterization of a novel broad‐host‐range plasmid from Bordetella bronchiseptica with sequence similarities to plasmids from Gram‐positive organisms , 1992, Molecular microbiology.

[26]  C. Bauer,et al.  Regulatory factors controlling photosynthetic reaction center and light-harvesting gene expression in Rhodobacter capsulatus , 1992, Cell.

[27]  C. Bauer,et al.  Analysis of the Rhodobacter capsulatus puf operon. Location of the oxygen-regulated promoter region and the identification of an additional puf-encoded gene. , 1988, The Journal of biological chemistry.

[28]  H. Gest,et al.  Genetic Mutations Affecting the Respiratory Electron-Transport System of the Photosynthetic Bacterium Rhodopseudomonas capsulata , 1973, Journal of bacteriology.