1887

Microbiology Society logo

Volume 143, Issue 2

The and genes: cloning and sequencing, and analysis of the potential of their products to form a haem or apo- -type cytochrome transporter Free

Abstract

Two c-type cytochrome deficient mutants of HN49 and HN53, were isolated by Tn mutagenesis and screening for failure to oxidize dimethylphenylenediamine (the Nadi test). Both were completely deficient in -type cytochromes. Genomic DNA flanking the site of Tn insertion in HN53 was cloned by marker rescue and a 3.1 kb region sequenced. Three of the genes, designated and present in this region are proposed to encode the components of a membrane transporter of the ABC (ATP-binding cassette) super-family, which is similar to a group of transporters postulated to translocate either haem or apocytochromes The Tn elements in HN49 and HN53 were shown to be inserted in and respectively. Sequence analysis suggested that both CcmB and CcmC have the potential to interact with CcmA and thus that the three gene products probably associate to form a complex with (CcmA)-CcmB-CcmC stoichiometry; it also indicated a lack of similarity between CcmB and CcmC and the membrane-integral components of transporters mediating uptake of haem or other iron complexes. Supplementation of growth media with haem did not stimulate -type cytochrome formation in HN49 or HN53, although it elevated levels of soluble haemoproteins and membrane-bound cytochromes suggesting that exogenous haem can traverse both outer and inner membranes of HN49 and HN53 accumulated apocytochrome to much lower levels than other -type cytochrome deficient mutants of but expression and translocation of an apocytochrome -alkaline phosphatase fusion protein and apocytochrome were unaffected in HN53. The results suggest that the substrate for the putative CcmABC-transporter is probably neither haem nor -type apocytochromes.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): apocytochrome , c-type cytochrome biogenesis , haem , Paracoccus denitrificans and putative ABC-transporter
Society for General Microbiology 1997
Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-143-2-563
1997-02-01
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/micro/143/2/mic-143-2-563.html?itemId=/content/journal/micro/10.1099/00221287-143-2-563&mimeType=html&fmt=ahah

References

  1. Aguilar G.R., Soberon M. 1996; Cloning And Sequence Analysis Of The Rhizobium Etli Ccma And Ccmb Genes Involved In C-Type Cytochrome Assembly.. Embl/Genbank/Ddbj Database Entry U52866.
    [Google Scholar]
  2. Alefounder P.R., Ferguson S.J. 1981; A Periplasmic Location For Methanol Dehydrogenase From Paracoccus Denitrificans: Implications For Proton Pumping By Cytochrome Aa3 . Biochem Biophys Res Commun 98:778–784
     [Google Scholar]
  3. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. 1990; Basic Local Alignment Search Tool. J Mol Biol 215:403–410
     [Google Scholar]
  4. Ames G.F.-L., Lecar H. 1992; Atp-Dependent Bacterial Transporters And Cystic Fibrosis: Analogy Between Channels And Transporters. Faseb J 6:2660–2666
     [Google Scholar]
  5. Ames G.F.-L, Mimura C.S, Holbrook S.R., Shymala V. 1992; Traffic Atpases: A Superfamily Of Transport Proteins Operating From Escherichia ColiTo Humans. Adv Enzymol 65:1–7
     [Google Scholar]
  6. Auerswald E.-A., Ludwig G, Schalle H. 1981; Structural Analysis Of Tn5. Cold Spring Harbour Symp Quant Biol 45:107–113
     [Google Scholar]
  7. Bagdasarian M., LüRz R., RüCkert B., Franklin F.C.H., Bagdasarian M.M., Frey J., Timmis K.N. 1981; Specific- Purpose Plasmid Cloning Vectors. Ii. Broad Host Range, High Copy Number Rsflolo-Derived Vectors And A Host-Vector System For Gene Cloning In Pseudomonas. . Gene 16:237–247
     [Google Scholar]
  8. Beckman D.L., Kranr R.G. 1993; Cytochromes C Biogenesis In A Photosynthetic Bacterium Requires A Periplasmic Thioredoxin- Like Protein. Proc Natl Acad Sci Usa 902179–2183
     [Google Scholar]
  9. Beckman D.L, Kranz R.G. 1992; Bacterial Cytochrome C Biogenesis. Genes Dev 6:268–283
     [Google Scholar]
  10. Burnell J.N., John P., Whatley F.R. 1975; The Reversibility Of Active Sulphate Transport In Membrane Vesicles Of Paracoccus Denitrificans. . Biochem J 150:527–536
     [Google Scholar]
  11. Crooke H., Cole J. 1995; The Biogenesis Of C-Type Cytochromes In E. Coli Requires A Membrane-Bound Protein, Dipz, With A Protein Disulphide Isomerase-Like Domain. Mol Microbiol 15:1139–1150
     [Google Scholar]
  12. Dassa E., Hofnung M. 1985; Sequence Of Gene Malg In E. Coli K12: Homologies Between Integral Membrane Components From Binding-Protein-Dependent Transport Systems. Embo J 4:2287–2293
     [Google Scholar]
  13. Dassa E., Francoz E., Dahl M., Schneider E., Werts C., Charbit A., Saurin W., Hofnung M. 1993; The Maltose B Region In Salmonella Typhimurium, Escherichia Coli And Other Entero- Bacteriaceae. Nato Asl Ser Ser A Life Sci 245:91–104
     [Google Scholar]
  14. Devereux J., Haeberli P., Smithies O. 1984; A Comprehensive Set Of Sequence Analysis Programs For The Vax. Nucleic Acids Res 12:387–395
     [Google Scholar]
  15. Ditta G., Stanfield S., Corbin D., Helinski D.R. 1980; Broad Host Range Dna Cloning Systems For Gram-Negative Bacteria: Construction Of A Gene Bank Of Rhizobium Meliloti. . Proc Natl Acad Sci Usa 777347–7351
     [Google Scholar]
  16. Dumont M.E., Corin A.F., Campbell G.A. 1994; Noncovalent Binding Of Heme Induces A Compact Apocytochrome C Structure. Biochemistry 33:7368–7378
     [Google Scholar]
  17. Fath M.J., Kolter R. 1993; Abc Transporters: Bacterial Exporters. Microbiol Rev 57:995–1017
     [Google Scholar]
  18. Fisher W.R., Taniuchi H., Anfinsen C.B. 1973; On The Role Of Heme In The Formation Of The Structure Of Cytochrome C. . J Biol Chem 248:3188–3195
     [Google Scholar]
  19. Fleischmann R.D., Adams M.D., White O. 37 Other Authors 1995; Whole-Genome Sequencing And Assembly Of Haemophilus Influenzae Rd. Science 269:496–512
     [Google Scholar]
  20. Gaballa A., Koedam N., Cornells P. 1995 Pseudomonas Fluorescens Cyt [1,2,3,4,5,6,7,8] Genes. Embl/Genbank/Ddbj Database Entry Z47979.
    [Google Scholar]
  21. Gardel C., Johnson K., Jacq A., Beckwith J. 1990; The Secd Locus Of E. Coli Codes For Two Membrane Proteins Required For Protein Export. Embo J 9:3209–3216
     [Google Scholar]
  22. Grove J., Tanapongpipat S., Thomas G., Griffiths L, Crooke H., Cole J. 1996; Escherichia Coli K-12 Genes Essential For The Synthesis Of C-Type Cytochromes And A Third Nitrate Reductase Located In The Periplasm. Mol Microbiol 19:467–481
     [Google Scholar]
  23. Haddock B.A., Schairer H.U. 1973; Electron-Transport Chains Of Escherichia Coli: Reconstitution Of Respiration In A 5- Aminolevulinic Acid-Requiring Mutant. Eur J Biochem 35:34–15
     [Google Scholar]
  24. Harms N., Van Spanning R.J. 1991; C1Metabolism In Paracoccus Denitrificans; Genetics Of P Denitrificans.. J Bioenerg Biomembr 23:187–210
     [Google Scholar]
  25. Harms N., De Vries G. E., Maurer K., Veltkamp E., Stouthamer A. H. 1985; Isolation And Characterisation Of Paracoccus Denitrificans Mutants With Defects In The Metabolism Of One- Carbon Compounds. J Bacteriol 164:1064–1070
     [Google Scholar]
  26. Von Heijne G. 1992; Membrane Protein Structure Prediction. Hydrophobicity Analysis And The Positive-Inside Rule. J Mol Biol 225:487–494
     [Google Scholar]
  27. Hekstra D., Tommassen J. 1993; Functional Exchangeability Of The Abc Proteins Of The Periplasmic Binding Protein-Dependent Transport Systems Ugp And Mal Of Escherichia Coli. . J Bacteriol 175:6546–6552
     [Google Scholar]
  28. Henderson D.P., Payne S.M. 1994; Characterisation Of The Vibrio Cholerae Outer Membrane Heme Transport Protein Huta: Sequence Of The Gene, Regulation Of Expression, And Homology To The Family Of Tonb-Dependent Proteins. J Bacteriol 176:3269–3277
     [Google Scholar]
  29. Higgins C.F. 1992; Abc Transporters: From Microorganisms To Man. Annu Rev Cell Biol 8:67–113
     [Google Scholar]
  30. Higgins C.F. 1995; The Abc Of Channel Regulation. Cell 82:693–696
     [Google Scholar]
  31. Higgins C.F., Hiles I.D., Salmond G.P.C, Gill D.R, Evans J. A. D. I. J.,, Holland I.B., Gray J., Buckel S.D., Bell A.W., Hermodson M.A. 1986; A Family Of Related Atp-Binding Subunits Coupled To Many Distinct Biological Processes In Bacteria. Nature 323:448–450
     [Google Scholar]
  32. Hoffman C.S., Wright A. 1985; Fusions Of Secreted Proteins To Alkaline Phosphatase: An Approach For Studying Protein Secretion. Proc Natl Acad Sci Usa 825107–5111
     [Google Scholar]
  33. Jekabsons W., Schuster W. 1995; Orf250 Encodes A Second Subunit Of A Abc-Type Heme Transporter In Oenothera Mitochondria. Mol Gen Genet 246:166–173
     [Google Scholar]
  34. Jones D.T., Taylor W.R., Thornton J.M. 1994; A Model Recognition Approach To The Prediction Of All-Helical Membrane Protein Structure And Topology. Biochemistry 33:3038–3049
     [Google Scholar]
  35. Karim A., Kaderbhai N., Evans A., Harding V., Kaderbhai M.A. 1993; Efficient Bacterial Export Of A Eukaryotic Cytoplasmic Cytochrome. Bio/Technology 11:612–618
     [Google Scholar]
  36. KöSter W., BöHm B. 1992; Point Mutations In Two Conserved Glycine Residues Within The Integral Membrane Protein Fhub Affect Iron(Iii)Hydroxamate Transport. Mol Gen Genet 232:399–407
     [Google Scholar]
  37. Kozak M. 1983; Comparison Of Initiation In Protein Synthesis In Procaryotes, Eucaryotes, And Organelles. Microbiol Rev 47:1–45
     [Google Scholar]
  38. Kranz R.G., Beckman D.L. 1995; Cytochrome Biogenesis. . In Anoxygenic Photosynthetic Bacteria Pp. 709–723 Blankenship R. E., Madigan M. T., Bauer. C. E. Edited By Amsterdam:: Kluwer;
     [Google Scholar]
  39. Leighton J., Schatz G. 1995; An Abc Transporter In The Mitochondrial Inner Membrane Is Required For Normal Growth Of Yeast. Embo ] 14:188–195
     [Google Scholar]
  40. Marrs B., Gest H. 1973; Genetic Mutations Affecting The Respiratory Electron-Transport System Of The Photosynthetic Bacterium Rhodopseudomonas Capsulata. . J Bacteriol 114:1045–1051
     [Google Scholar]
  41. Moir J.W.B. 1993 Aspects Of Electron Transport In Thiosphaera Pantotropha And Paracoccus Denitrificans. Dphil Thesis. University Of Oxford.
    [Google Scholar]
  42. Oda K., Yamato K., Ohta E., Nakamura Y., Takmura M., Nozato N., Kohchi T., Ogura Y., Kanegae T., Akashi K, Ohyama K. 1992; Gene Organisation Deduced From The Complete Sequence Of Liverwort Marchantia Polymorpha Mitochondrial Dna. A Primitive Form Of Plant Mitochondrial Genome.. Mol Biol 223:1–7
     [Google Scholar]
  43. Page M.D., Ferguson S.J. 1989; A Bacterial C-Type Cytochrome Can Be Translocated To The Periplasm As An Apo Form; The Biosynthesis Of Cytochrome Cd1 (Nitrite Reductase) From Paracoccus Denitrificans. . Mol Microbiol 3:653–661
     [Google Scholar]
  44. Page M.D., Ferguson S.J. 1990; Apo Forms Of Cytochrome C550 And Cytochrome Cd1 Are Translocated To The Periplasm Of Paracoccus Denitrificans In The Absence Of Haem Incorporation Caused By Either Mutation Or Inhibition Of Haem Synthesis. Mol Microbiol 4:1181–1192
     [Google Scholar]
  45. Page M.D., Ferguson S.J. 1994; Differential Reduction In Periplasmic And Membrane-Bound C-Type Cytochrome Contents In A Paracoccus Denitrificans Mutant Partially Deficient In 5- Aminolevulinate Synthase. J Bacteriol 176:5919–5928
     [Google Scholar]
  46. Page M.D., Ferguson S.J. 1995; Cloning And Sequence Analysis Of The Cych Gene From Paracoccus Denitrificans: The CychGene Product Is Required For Assembly Of All C-Type Cytochromes, Including Cytochrome C1. . Mol Microbiol 15:307–318
     [Google Scholar]
  47. Persson B., Argos P. 1994; Prediction Of Transmembrane Segments In Proteins Utilising Multiple Sequence Alignments. J Mol Biol 237:182–192
     [Google Scholar]
  48. Petronilli V., Ames G.F.-L. 1991; Binding Protein-Independent Histidine Permease Mutants: Uncoupling Of Atp Hydrolysis From Transmembrane Signalling. J Biol Chem 266:16293–16296
     [Google Scholar]
  49. Poole R.K., Hatch L., Cleeter M.W.J., Gibson F., Cox G.B., Wu G. 1993; Cytochrome Bd Biosynthesis In Escherichia Coli:The Sequences Of The Cydc And Cydd Genes Suggest That They Encode The Components Of An Abc Membrane Transporter. Mol Microbiol 10:421–430
     [Google Scholar]
  50. Poole R.K., Gibson F., Wu G. 1994; The Cydd Gene Product, Component Of A Heterodimeric Abc Transporter, Is Required For Assembly Of Periplasmic Cytochrome C And Of Cytochrome Bd In Escherichia Coli. . Fems Microbiol Lett 117:217–224
     [Google Scholar]
  51. Ramseier T., Winteler H.V., Hennecke H. 1991; Discovery And Sequence Analysis Of Bacterial Genes Involved In The Biogenesis Of C-Type Cytochromes. J Biol Chem 266:7793–7803
     [Google Scholar]
  52. Reizer J., Reizer A., Saier M.H. Jr 1992; A New Subfamily Of Bacterial Abc-Transport Systems Catalyzing Export Of Drugs And Carbohydrates. Protein Sci 1:1326–1332
     [Google Scholar]
  53. Richterich P., Lakey N., Gryan G., Jaehn L., Mintz L., Robison K., Church G.M. 1993; Centisome 49 Region Of E. Coli K-12 Bhb2600.. Embl/Genbank/Ddbj Database Entry U00008.
    [Google Scholar]
  54. Sambongi Y., Ferguson S. J. 1994A; Synthesis Of Holo Paracoccus Denitrificans Cytochrome C550Requires Targeting To The Periplasm Whereas That Of Holo Hydrogenobacter Thermophilus Cytochrome C552 Does Not. Implications For C-Type Cytochrome Biogenesis. Febs Lett 340:65–70
     [Google Scholar]
  55. Sambongi Y., Ferguson S. J. 1994B; Specific Thiol Compounds Complement Deficiency In C-Type Cytochrome Biogenesis In Escherichia Coli Carrying A Mutation In A Membrane-Bound Disulphide-Isomerase-Like Protein. Febs Lett 353:235–240
     [Google Scholar]
  56. Sambrook J., Fritsch E.F., Maniatis T. 1989 Molecular Cloning: A Laboratory Manual,, 2. Cold Spring Harbor, Ny:: Cold Spring Harbor Laboratory.;
     [Google Scholar]
  57. Schuster W. 1994; The Highly Edited Orf206 In OenotheraMitochondria May Encode A Component Of A Heme Transporter Involved In Cytochrome C Biogenesis. Plant Mol Biol 25:33–42
     [Google Scholar]
  58. Simon R., Priefer U., PüHler A. 1983; A Broad Host Range Mobilization System For In Vivo Genetic Engineering: Transposon Mutagenesis In Gram-Negative Bacteria. Bio/Technology 1:37–5
     [Google Scholar]
  59. Sockett R.E., Armitage J.P. 1991; Isolation, Characterisation And Complementation Of A Paralysed Flagellar Mutant Of Rhodobacter Sphaeroides Ws8.. J Bacteriol 173:2786–2790
     [Google Scholar]
  60. Staudenmaier H., Van Hove B., Yaraghi Z., Braun V. 1989; Nucleotide Sequences Of The Fecbcde Genes And Locations Of The Proteins Suggest A Periplasmic-Binding-Protein-Dependent Transport Mechanism For Iron (Iii) Dicitrate In Escherichia Coli. . J Bacteriol 171:2626–2633
     [Google Scholar]
  61. Steinrücke P., Ludwig B. 1993; Genetics Of Paracoccus Denitrificans. . Fems Microbiol Rev 104:83–118
     [Google Scholar]
  62. Stojijkovic I., Hantke K. 1994; Transport Of Haemin Across The Cytoplasmic Membrane Through A Haemin-Specific Periplasmic- Binding-Protein-Dependent Transport System In Yersinia Entero- Colitica. . Mol Microbiol 13:7719–7732
     [Google Scholar]
  63. Stoll R., Page M.D., Sambongi Y., Ferguson S.J. 1996; Cytochrome C550 Expression In Paracoccus Denitrificans Strongly Depends On Growth Condition; Identification Of Promoter Region For Cyca By Transcription Start Analysis. Microbiology 142:2577–2585
     [Google Scholar]
  64. ThɂNy-Meyer L., Ritz D., Hennecke H. 1994; Cytochrome CBiogenesis In Bacteria: A Possible Pathway Begins To Emerge. Mol Microbiol 12:1–9
     [Google Scholar]
  65. ThɂNy-Meyer L., Fischer F., KüNzier P., Ritz D., Hennecke H. 1995; Escherichia Coli Genes Required For C-Type Cytochrome Maturation. J Bacteriol 177:4321–4326
     [Google Scholar]
  66. ThɂNy-Meyer L., Kunzier P., Hennecke H. 1996; Requirements For Maturation Of Bradyrhizobium Japonicum Cytochrome C550 In Escherichia Coli. . Eur J Biochem 235:754–761
     [Google Scholar]
  67. Van Verseveld H.W., Krab K. 1981; Proton Pump Coupled To Cytochrome C Oxidase In Paracoccus Denitrificans. . Biochim Biophys Acta 635:525–534
     [Google Scholar]
  68. Viebrock A., Zumft W.G. 1987; Physical Mapping Of Transposon Tn5 Insertions Defines A Gene Cluster Functional In Nitrous Oxide Respiration By Pseudomonas Stutzeri. . J Bacteriol 169:4577–4580
     [Google Scholar]
  69. De Vries G.E., Harms N., Hoogedijk J.J., Stouthamer A.H. 1989; Isolation And Characterisation Of Paracoccus Denitrificans Mutants With Increased Conjugation Frequencies And Pleiotropic Loss Of A (Ngatcn) Dna-Modifying Property. Arch Microbiol 152:52–57
     [Google Scholar]
  70. Walker J.E., Saraste M., Runswick M.J., Gay N.J. 1982; Distantly Related Sequences In The α- And β-Subunits Of Atp Synthase, Myosin, Kinases And Other Atp-Requiring Enzymes And A Common Nucleotide Binding Fold. Embo J 1:945–951
     [Google Scholar]
  71. Willison. J.C, John P. 1979; Mutants Of Paracoccus Denitrificans Deficient In C-Type Cytochromes. J Gen Microbiol 115:443–450
     [Google Scholar]
  72. Yanisch-Perron C, Vieira J., Messing J. 1985; Improved M13 Phage Cloning Vectors And Host Strains: Nucleotide Sequences Of The M13Mpl8 And Puc19 Vectors. Gene 33:103–119
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-143-2-563
Loading
The Paracoccus denitrificans ccmA, B and C genes: cloning and sequencing, and analysis of the potential of their products to form a haem or apo- c-type cytochrome transporter
Microbiology 143, 563 (1997); https://doi.org/10.1099/00221287-143-2-563
/content/journal/micro/10.1099/00221287-143-2-563
/content/journal/micro/10.1099/00221287-143-2-563
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error