Cloning and sequence analysis of the Rhizobium etli ccmA and ccmB genes involved in c-type cytochrome biogenesis

Aguilar, Germán R.; Soberón, Mário

doi:10.1016/s0378-1119(96)00534-3

Cited by 11 publications

(11 citation statements)

References 28 publications

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“…This operon has a high degree of similarity to previously described bacterial cytochrome c biogenesis genes (1,5,20,28). One of these gene products, CytA, an inner membrane protein of the ABC transporter superfamily (14,22), has been proposed to transport both heme and pyoverdine from the cytoplasm to the periplasm (14).…”

mentioning

confidence: 78%

Transcriptional regulation of the cydDC operon, encoding a heterodimeric ABC transporter required for assembly of cytochromes c and bd in Escherichia coli K-12: regulation by oxygen and alternative electron acceptors

1997

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The expression of the cydDC operon was investigated by using a chromosomal ⌽(cydD-lacZ) transcriptional fusion and primer extension analysis. A single transcriptional start site was found for cydD located 68 bp upstream of the translational start site, and Northern blot analysis confirmed that cydDC is transcribed as a polycistronic message independently of the upstream gene trxB. cydDC was highly expressed under aerobic growth conditions and during anaerobic growth with alternative electron acceptors. Aerobic expression was independent of ArcA and Fnr, but induction of cydDC by nitrate and nitrite was dependent on NarL and Fnr.Like almost all bacteria, the enteric bacterium Escherichia coli has to cope with constantly changing conditions in the environment to optimize its growth rate and yield. E. coli adapts to fluctuations in oxygen supply by using two wellcharacterized membrane-bound terminal oxidases for aerobic respiration, cytochromes boЈ and bd (15). One of these oxidases, cytochrome bd, is expressed maximally at low aeration (7% air saturation) as determined by cydA-lacZ activity, but at 0% air saturation of the growth medium, the level of this oxidase is decreased to 60% of its maximum expression (44). ArcA was shown to be a positive regulator of cydAB expression under these conditions, but Fnr functioned as a repressor (44). It has also been shown that cytochrome bd is induced when E. coli is grown under alkaline or other unfavorable growth conditions (3, 6, 9).In addition to the structural genes cydA and cydB, which encode the two subunits of the oxidase, two further genes, cydD and cydC, encoding a heterodimeric ATP-binding cassette (ABC-type) transporter, are required for a functional cytochrome bd in E. coli (16,(30)(31)(32). Mutants defective in cydD or cydC are sensitive to hydrogen peroxide and are unable to exit stationary phase and resume aerobic growth at high temperatures (11, 37). However, recent studies (19, 36) have suggested that it is the lack of a functional cytochrome bd caused by mutations in cydD or cydC that leads to the observed phenotypes of stationary-phase mortality and sensitivity to oxidative stress.Mutations in cydDC do not influence the transcription of cydAB or the assembly of CydA or CydB polypeptides into the membrane (4). The oxidase polypeptides are assembled but lack the distinctive chlorin heme d and presumably hemes b 595 and b 558 (30). Periplasmic cytochromes (i.e., cytochrome c and cytochrome b 562 ) are also significantly reduced in cydDC mutants (18,30). At present, neither the function of nor the substrate for the CydDC ABC transporter is known. The goal of the present work was to understand how expression of the cydDC operon is regulated and to define a role for this transporter in the growth physiology of E. coli. We report here the use of a chromosomal operon fusion to study cydDC expression under various conditions of oxygen supply and in the presence of alternative electron acceptors.

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mentioning

confidence: 78%

Transcriptional regulation of the cydDC operon, encoding a heterodimeric ABC transporter required for assembly of cytochromes c and bd in Escherichia coli K-12: regulation by oxygen and alternative electron acceptors

1997

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“…CcmB, together with CcmA, seems to be a subunit of an ATP-binding cassette (ABC) transporter involved in cytochrome c biogenesis (Thony-Meyer, 2003). The B. japonicum and R. etli CycW/CcmB proteins are thought to be involved in haem translocation required for the synthesis of mature c-type cytochromes, and for symbiotic nitrogen fixation (Aguilar & Soberon, 1996;Ramseier et al, 1989Ramseier et al, , 1991.…”

Section: Isolation Of S Meliloti Nadi " Mutants and Localization Of mentioning

confidence: 99%

Pleiotropic effects of mutations that alter the Sinorhizobium meliloti cytochrome c respiratory system

et al. 2007

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“…In addition, E. coli and Haemophilus influenzae nrfEG are also thought to be involved specifically in the attachment of haem to a cysteine–lysine motif on an apocyt (Grove et al ., 1996). Various homologues of these genes have also been reported through mutagenesis studies in other Gram‐negative bacteria such as Paracoccus denitrificans (Page and Ferguson, 1995; Page, 1997; Page et al ., 1997a; Pearce et al ., 1998), Rhizobia (Delgado et al ., 1995; Aguilar and Soberón, 1996; Fabianek et al ., 1997; Tabche et al ., 1998) and Pseudomonas aeruginosa (Page et al ., 1997b). Counterparts of several components of system I have also been encountered in archae such as Archaeoglobus fulgidus (Klenk et al ., 1997), as well as in nuclear ( Arabidopsis thaliana ) (Sadowski et al ., 1996) and mitochondrial [ Marchantia sp.…”

Section: Introductionmentioning

confidence: 99%

Novel Rhodobacter capsulatus genes required for the biogenesis of various c‐type cytochromes

Deshmukh

Brasseur

Daldal

2000

Molecular Microbiology

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Following chemical mutagenesis and screening for the inability to grow by photosynthesis and the absence of cyt cbb3 oxidase activity, two c‐type cytochrome (cyt)‐deficient mutants, 771 and K2, of Rhodobacter capsulatus were isolated. Both mutants were completely deficient in all known c‐type cyts, and could not be complemented by the previously known cyt c biogenesis genes of R. capsulatus. Complementation of 771 and K2 with a wild‐type chromosomal library led to the identification of two novel genes, cycJ and ccdA respectively. The cycJ is highly homologous to ccmE/cycJ, encountered in various Gram‐negative species. Unlike in other species, where cycJ is a part of an operon essential for cyt c biogenesis, in R. capsulatus, it is located immediately downstream from argC, involved in arginine biosynthesis. Mutation of its universally conserved histidine residue, which is critical for its proposed haem chaperoning role, to an alanine led to loss of its function. All R. capsulatus cycJ mutants studied so far excrete copious amounts of coproporphyrin and protoporphyrin when grown on enriched media, suggesting that its product is also a component of the haem delivery branch of cyt c biogenesis in this species. In contrast, the R. capsulatus ccdA was homologous to the cyt c biogenesis gene ccdA, found in the Gram‐positive bacterium Bacillus subtilis, and to the central region of dipZ, encoding a protein disulphide reductase required for cyt c biogenesis in Escherichia coli. Membrane topology of CcdA was established in R. capsulatus using ccdA ::phoA and ccdA ::lacZ gene fusions. The deduced topology revealed that the two conserved cysteine residues of CcdA are, as predicted, membrane embedded. Mutagenesis of these cysteines showed that both are required for the function of CcdA in cyt c biogenesis. This study demonstrated for the first time that CcdA homologues are also required for cyt c biogenesis in some Gram‐negative bacteria such as R. capsulatus.

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Cloning and sequence analysis of the Rhizobium etli ccmA and ccmB genes involved in c-type cytochrome biogenesis

Cited by 11 publications

References 28 publications

Transcriptional regulation of the cydDC operon, encoding a heterodimeric ABC transporter required for assembly of cytochromes c and bd in Escherichia coli K-12: regulation by oxygen and alternative electron acceptors

Transcriptional regulation of the cydDC operon, encoding a heterodimeric ABC transporter required for assembly of cytochromes c and bd in Escherichia coli K-12: regulation by oxygen and alternative electron acceptors

Pleiotropic effects of mutations that alter the Sinorhizobium meliloti cytochrome c respiratory system

Novel Rhodobacter capsulatus genes required for the biogenesis of various c‐type cytochromes

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