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The Paracoccus Denitrificans Electron Transport System: Aspects of Organisation, Structures and Biogenesis

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Biological Electron Transfer Chains: Genetics, Composition and Mode of Operation

Part of the book series: NATO ASI Series ((ASIC,volume 512))

Abstract

The electron transport system of Paracoccus denitrificans (then known as Micrococcus denitrificans) first attracted significant interest in the 1960’s when it was shown that at least some of its components required for aerobic respiration are similar to those found in mitochondria. The identification of cytochrome c 550 as a protein with significant similarity to mitochondrial cytochrome c led to an early X-ray diffraction structure determination. However, attention was strongly focused on the P. denitrificans electron transfer chain following the publication in 1975 of a review article by John and Whatley [32] that developed the thesis that the aerobic electron transport chain of the organism is more similar to that of the mitochondrion than that found in any other bacterium. The corollary of this thesis was that P. denitrificans is related to an aerobic symbiont from which the present-day mitochondrion is derived [32]. In subsequent years a great deal has been learned about the P. denitrificans electron transport system, much of it confirming at the molecular level that many of its components are indeed closely related to, but often possessing a simpler subunit structure than, those of the mammalian mitochondrion. Furthermore, in the years since 1975 a great deal of insight into other aspects of the electron transport chain has been obtained. This brief review aims to collect together current aspects of this electron transport system. The treatment cannot be comprehensive and does not attempt to relate work with P. denitrificans to that on other bacteria. However, observations on the organism Thiosphaera pantotropha are included.

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References

  1. Alefounder, P.R. and Ferguson, S.J. (1980) The location of dissimilatory nitrite reductase and the control of dissimilatory nitrate reductase in Paracoccus denitrificans, Biochem. J. 192 231–240.

    CAS  Google Scholar 

  2. Alefounder, P.R., McCarthy, J.E.G. and Ferguson, S.J. (1981) The basis of the control of nitrate reduction by oxygen in Paracoccus denitrificans, FEMS Microbiol Lett. 12 321–326.

    Article  CAS  Google Scholar 

  3. Alefounder, P.R., Greenfield, A.J., McCarthy, J.E.G. and Ferguson, S.J. (1983) Selection and organisation of denitrifying electron transfer pathways in Paracoccus denitrificans, Biochim. Biophys. Acta 724 20–39.

    Article  CAS  Google Scholar 

  4. Bauman, B., Snozzi, M., Zehnder, A.J.B. and van der Meer, J.R. (1996) Dynamics of denitrification activity of Paracoccus denitrificans in continuous culture during aerobic-anaerobic changes, J. Bacteriol. 178 4367–4374.

    Google Scholar 

  5. Bedzyk, LA., Escudero, K.W., Gill, RE, Griffin, K.J. and Frerman, F.E. (1993) Cloning, sequencing and expression of the genes encoding subunits of Paracoccus denitrifzcans electron transfer flavoprotein, J. Biol. Chem. 268 20211–20217.

    CAS  Google Scholar 

  6. Berks, B.C. (1996) A common export pathway for proteins binding complex redox cofactors? Mol. Microbiol. 22 393–404.

    Article  CAS  Google Scholar 

  7. Berks, B.C., Richardson, D.J, Reilly, A., Willis, A.C. and Ferguson, S.J. (1995) The napABC gene cluster encoding the periplasmic nitrate reductase system of Thiosphaera pantotropha, Biochem. J. 309 983–992.

    CAS  Google Scholar 

  8. Berks, B.C., Page, M.D., Richardson, D.J., Reilly, A., Cavill, A., Outen, F. and Ferguson, S.J. (1995) Sequence analysis of subunits of the membrane-bound nitrate reductase from a denitrifying bacterium: the integral membrane subunit provides a prototype for the electron carrying arm of a redox loop, Mol. Microbiol. 15, 319–331.

    Article  CAS  Google Scholar 

  9. Berks, B.C., Ferguson, S.J, Moir, J.W.B., and Richardson, D.J. (1995) Enzymes and associated electron transport systems that catalyse their respiratory reduction of nitrogen oxides and oxyanions, Biochim. Biophys. Acta 1232 97–173.

    Article  Google Scholar 

  10. Berks, B.C., Richardson, D.J., Page, M.D. and Ferguson, S.J. (1996) An alternative model for haem ligation in nitrate reductase and analogous respiratory cytochrome b complexes (response to the Microcorrespondence by van der Oost et al.), Mol. Microbiol. 22 195–196.

    Article  CAS  Google Scholar 

  11. Boyington, J.C., Gladyshev, V.N., Khangulov, S.V., Stadtman, T.C. and Sun, P.D. (1997) Crystal structure of formate dehydrogenase H: Catalysis involving Mo, molybdopterin, selenocysteine, and an Fe4S4 cluster, Science 275 1305–1308.

    Article  CAS  Google Scholar 

  12. Carr, G.J. and Ferguson, S.J. (1990) The nitric oxide reductase of Paracoccus denitrificans, Biochem. J. 269, 423–429.

    CAS  Google Scholar 

  13. Chen, L., Durley, R., Poliks, B.J., Hamada, K., Chen, Z., Mathews, F.S., Davidson, V.L., Satow, Y., Huizinga, E., Vellieux, F.M.D. and Hol, W.G.J. (1992) Crystal structure of an electron-transfer complex between methylamine dehydrogenase and amicyanin, Biochemistry 31 4959–4964.

    Article  CAS  Google Scholar 

  14. Chen, L., Durley, R.C.E., Mathews, F.S., and Davidson, V.L. (1994) Structure of an electron-transfer complex; methylamine dehydrogenase, amicyanin and cytochrome c 551, Science 264 86–90.

    Article  CAS  Google Scholar 

  15. De Gier, J.W.L., Lubben, M., Reijnders, W.N.M., Westerhoff, H.V., Tipker, C.A., Slotboom, D.J., and van Spanning, R.J.M. (1994) The terminal oxidases of Paracoccus denitnficans, Mol. Microbiol. 13183–186.

    Article  Google Scholar 

  16. De Gier, J.W.L., van der Oost, J., Harms, N., Stouthamer, A.H. and van Spanning, R.J.M. (1995) The oxidation of methylamine inParacoccus denitrificans, Eur. J. Biochem. 229148–154.

    Article  Google Scholar 

  17. De Gier, J.W.L., Schepper, M., Reijnders, W.N.M., Westerhoff, H.V., Tipker, C.A., Slotboom, D.J., van Spanning, R.J.M. and van der Oost, J. (1996) Structural and functional analysis of aa 3-type and cbb 3-type cytochrome c oxidases of Paracoccus denitrificans reveals significant differences in proton-pump design, Mol. Microbiol. 20,1247–1260.

    Article  Google Scholar 

  18. Dickins, M.A., Dhawan, T., Gunsalus, R.P., Schroeder, L, and Cecchini, G. (1996) Cloning, sequencing and expression of the succinate-ubiquinone oxidoreductase (SdhCDAB) operon from Paracoccus denitrificans. EMBL database entry PDU31902.

    Google Scholar 

  19. Ferguson, S.J. (1982) Aspects of the control and organization of bacterial electon transport, Biochem. Soc. Trans. 10,198–200.

    CAS  Google Scholar 

  20. Ferguson, S.J. (1991) The functions and synthesis of bacterial c-type cytochromes with particular reference to Paracoccus denitnficans and Rhodobacter capsulatus. Biochim. Biophys. Acta 105817–20.

    Article  CAS  Google Scholar 

  21. Fujiwara, T. and Fukumori, Y. (1996) Cytochrome cb-type nitric oxide reductase with cytochrome c oxidase activity from Paracoccus denitrzftcans ATCC 35512, J. Bacterio. 1781866–1871.

    CAS  Google Scholar 

  22. Füöp, V., Moir, J.W.B., Ferguson, S.J. and Hajdu, J. (1995) The anatomy of a bifunctional enzyme: Structural basis for reduction of oxygen to water and synthesis of nitric oxide by cytochrome cd 1 , Cell 81 369–377.

    Article  Google Scholar 

  23. George, C.L. and Ferguson, S.J. (1987) Immunochemical probing of the structure and cofactor of NADH dehydrogenase from Paracoccus denitrificans,Biochem J. 244 661–668.

    CAS  Google Scholar 

  24. George, C.L., Ferguson, S.J., Cleeter, M.W.J. and Ragan, C.I. (1986) Structural relationships between NADH dehydrogenases of Paracoccus denitrificans and bovine heart mitochondria as revealed by immunological cross-reactivities, FEBS Len. 198135–139.

    Article  CAS  Google Scholar 

  25. George, C.L. and Ferguson, S.J. (1984) Immunochemical identification of a two-subunit NADHubiquinone oxidoreductase from Paracoccus denitnficans, Eur. J. Biochem. 143 567–573.

    Article  CAS  Google Scholar 

  26. Gilmour, R., Goodhew, C.F. and Pettigrew, G.W. (1991) Cytochrome c’ of Paracoccus denitnficans, Biochim. Biophys. Acta 1059, 233–238.

    Article  CAS  Google Scholar 

  27. Goodhew, C.F., Wilson, I.B.H., Hunter, D.J.B. and Pettigrew, G.W. (1990) The cellular location and specificity of bacterial cytochrome c peroxidases, Biochem. J. 271 707–712.

    CAS  Google Scholar 

  28. Goodhew, C.F., Pettigrew, G.W., Devreese, B., van Beeumen, J., Van Spanning R.J.M., Baker, S.C., Saunders, N., Ferguson, S.J. and Thompson, LP. (1996) The cytochromes c550 of Paracoccus denitnficans and Thiosphaera pantotropha: a need for the re-evaluation of the history of Paracoccus cultures, FEMS Microbiol. Lett. 137 95–101.

    Article  CAS  Google Scholar 

  29. Grisch, P. and de Vries, S. (1997) Purification and initial kinetic and spectroscopic characterization of NO reductase from Paracoccus denitnficans, Biochim. Biophys. Acta 1318 202–216.

    Article  Google Scholar 

  30. Hoeren, F.U., Berks, B.C., Ferguson, S.J. and McCarthy, J.E.G. (1993) Sequence and expression of the gene encoding the respiratory nitrous-oxide reductase from Paracoccus denitrificans. New and conserved structural and regulatory motifs, Eur.J.Biochem. 218 49–57.

    Article  CAS  Google Scholar 

  31. Iwata, S., Ostermeier, C., Ludwig, B. and Michel, H. (1995) Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitnficans, Nature 376 660–669.

    Article  CAS  Google Scholar 

  32. John, P. and Whatley, F.R. (1975) Paracoccus denitrificans and the evolutionary origin of the mitochondrion. Nature 254 495–498.

    Article  CAS  Google Scholar 

  33. Long, A. and Anthony, C. (1991) Characterization of the periplasmic cytochromes c of Paracoccus denitriftcans: identification of the electron acceptor for methanol dehydrogenase, and description of a novel cytochrome c heterodimer, J. Gen. Microbiol. 137 415–425.

    CAS  Google Scholar 

  34. Machová, L and Kucera, I. (1991) Evidence for the role of soluble cytochrome c in the dissimilatory reduction of nitrite and nitrous oxide by cells of Paracoccus denitnficans, Biochim. Biophys. Acta. 1058, 256–260.

    Article  Google Scholar 

  35. Moir, J.W.B. and Ferguson, S.J. (1993) Spontaneous mutation of Thiosphaera pantotropha enabling growth on methanol correlates with synthesis of a 26 kDa c-type cytochrome, FEMS Microbiol. Lett. 113, 321–326.

    Article  CAS  Google Scholar 

  36. Moir, J.W.B. and Ferguson, S.J. (1994) Properties of a Paracoccus denitrificans mutant deleted in cytochrome c 550 indicate that a copper protein can substitute for this cytochrome in electron transport to nitrite, nitric oxide and nitrous oxide, Microbiology 140 389–397.

    Article  CAS  Google Scholar 

  37. Mou, J.W.B., Richardson, D.J. and Ferguson, S.J. (1995) The expression of redox proteins of denitrification in Thiosphaera pantotropha grown with oxygen, nitrate and nitrous oxide as electron acceptors, Arch. Microbiol. 164, 43–49.

    Article  Google Scholar 

  38. Moir, J.W.B., Wehrfritz, J-M., Spiro, S. and Richardson, D.J. (1996) The biochemical characterization of a novel non-harne iron hydroxylamine oxidase from Paracoccus denitrificans GB17, Biochem. J. 319, 823–827.

    CAS  Google Scholar 

  39. Moir, J.W.B., Grossman, L.C., Spiro, S. and Richardson, D.J. (1996) The purification of ammonia monooxygenase from Paracoccus denitrificans, FEBS Lett. 387, 71–74.

    Article  CAS  Google Scholar 

  40. Page, M.D. and Ferguson, S.J. (1989) A bacterial c-type cytochrome can be translocated to the periplasm as an apo form; the biosynthesis of cytochrome cd 1 (nitrite reductase) from Paracoccus denitrificans, Mol. Microbiol 3653–661.

    Article  CAS  Google Scholar 

  41. Page, M.D. and Ferguson, S.J. (1990) Apo forms of cytochrome c 550 and cytochrome cd 1 are translocated to the periplasm of Paracoccus denitrificans in the absence of haem incorporation caused by either mutation of inhibition of haem synthesis, Mol. Microbiol. 41181–1192.

    Article  CAS  Google Scholar 

  42. Page, M.D. and Ferguson, S.J. (1993) Mutants of Methylobacterium extorquens and Paracoccus denitrificans deficient in c-type cytochrome biogenesis synthesise the methylamine dehydrogenase polypeptides but cannot assemble the tryptophan-tryptophylquinone group, Eur. J. Biochem 218 711–717.

    Article  CAS  Google Scholar 

  43. Page, M.D. and Ferguson, S.J. (1995) Cloning and sequence analysis of the cycH gene from Paracoccus denitrificans; the cycH gene product is required for assembly of all c-type cytochromes, including cytochrome cl, Mol. Microbiol. 41181–1192.

    Google Scholar 

  44. Page, M.D., Pearce, D.A., Norris, H.A.C. and Ferguson, S.J. (1997) 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 143 563–576.

    Article  CAS  Google Scholar 

  45. Page, M.D. and Ferguson, S.J. (1997) Paracoccus denitrificans CcmG is a periplasmic protein-disulphide oxidoreductase required for c- and aa 3-type cytochrome biogenesis; evidence for a reductase role in vivo, Mol. Microbiol. 24 977–990.

    Article  CAS  Google Scholar 

  46. Parsonage, D., Greenfield, A.J. and Ferguson, S.J. (1985) The high affinity of Paracoccus denitrificans cells for nitrate as an electron acceptor. Analysis of possible mechanisms of nitrate and nitrite movement across the plasma membrane and the basis for inhibition by added nitrite of oxidase activity in permeabilised cells, Biochim. Biophys. Acta 807 81–95.

    Article  CAS  Google Scholar 

  47. Pennoyer, J.D., Ohnishi, T. and Trumpower, B.L. (1988) Purification and properties of succinateubiquinone oxidoreductase complex from Paracoccus denitrificans, Biochim. Biophys. Acta 935 195–207.

    Article  CAS  Google Scholar 

  48. Ras, J., Reijnders, W.N.M., van Spanning, R.J.M., Harms, N., Oltmann, L.F. and Stouthamer, A.H. (1991) Isolation sequencing and mutagenesis of the gene encoding cytochrome c 553i of Paracoccus denitrificans and characterization of the mutant strain, J. Bacteriol. 173 6971–6979.

    CAS  Google Scholar 

  49. Ras, J., Hazelaar, M.J., Robertson, L.A., Kuenen, J.G., van Spanning, R.J.M., Harms, N., Oltmann, L.F. and Stouthamer, A.H. (1995) Methanol oxidation in a spontaneous mutant of Thiosphaera pantotropha with a methanol-positive phenotype is catalysed by a dye-linked ethanol dehydrogenase, FEMS Microbiol. Lett. 127 159–164.

    Article  CAS  Google Scholar 

  50. Richardson, D.J. and Ferguson, S.J. (1992) The influence of carbon substrate on the activity of the periplasmic nitrate reductase in aerobically grown Thiosphaera pantotropha, Arch. Microbiol. 157 535–537.

    CAS  Google Scholar 

  51. Richardson, D.J. and Ferguson, S.J. (1995) Competition between hydrogen peroxide and nitrate for electrons from the respiratory chains of Thiosphaera pantotropha and Rhodobacter capsulatus, FEMS Microbiol. Lett. 132 125–129.

    Article  CAS  Google Scholar 

  52. Richter, O-M. IL, Tao, J., Turba, A. and Ludwig, B. (1994) A cytochrome ba 3 oxidase functions as a quinol oxidase in Paracoccus denitrificans, J. Biol. Chem. 269 23079–23086.

    CAS  Google Scholar 

  53. Sears H.J., Ferguson, S.J., Richardson, D.J. and Spiro, S. (1993) The identification of a periplasmic nitrate reductase in Paracoccus denitrificans, FEMS Microbiol. Lett. 113 107–112.

    Article  CAS  Google Scholar 

  54. Smith, L. and Davies, H.C. (1991) The reactions of the oxidase and reductases of Paracoccus denitrificans with cytochromes c, J. Bioenergetics and Biomembranes 23 303–319.

    Article  CAS  Google Scholar 

  55. Stoll, R., Page, M.D., Sambongi, Y. and Ferguson, S.J. (1996) Cytochrome c 550 expression in Paracoccus denitrificans strongly depends on growth condition: Identification of promoter region for cycA by transcription start analysis, Microbiology 142 2577–2585.

    Article  CAS  Google Scholar 

  56. Stouthamer, A.H. (1992) Metabolic pathways in Paracoccus denitrificans and closely related bacteria in relation to phylogeny of prokaryotes, Antonie van Leeuwenhoek 61 1–33.

    Article  CAS  Google Scholar 

  57. Talcum, S., Yano, T. and Yagi, T. (1996) Structural studies of the proton translocating NADH ubiquinone oxidoreductase (NDH-1) of Paracoccus denitnficans: Identity. property and stoichiometry of the peripheral subunits, Biochemistry 35 9120–9127.

    Article  Google Scholar 

  58. Turba, A., Jetzek, M. and Ludwig, B. (1995) Purification of Paracoccus denitnficans cytochrome c 552 and sequence analysis of the gene, Eur. J. Biochem. 231 259–265.

    CAS  Google Scholar 

  59. van der Oost, J., Nederkoom, P.H., Stouthamer, A.H., Westerhoff, H.V., van Spanning, R.J.M. (1996) An alternative model for haem ligation in nitrate reductase and analogous respiratory cytochrome b complexes, Molecular Microbiology 22193–195.

    Article  Google Scholar 

  60. van Spanning, RJ.M., Wansell, C, Harms, N., Oltman, L.F. and Stouthamer, A. (1990) Mutagenesis of the gene encoding cytochrome c 550 of Paracoccus denitrificans and analysis of the resultant physiological effects, J. Bacteriol. 172 986–996. A correction to the amino acid sequence of cytochrome c 550 reported in this paper can be found in J. Bacteriol. 172 3534.

    Google Scholar 

  61. van Spanning, R.J.M., Wansell, C.W., Reijnders, W.N.M., Oltmann, L.F. and Stouthamer, A.H. (1990) Mutagenesis of the gene encoding amicyanin of Paracoccus denitrificans and the resultant effect on methylamine oxidation, FEBS Lett. 275 217–220.

    Article  Google Scholar 

  62. van Spanning, RJ.M., Wansell, C.W., de Boer, T., Hazelaar, M.J., Anazawa, IL, Harms, N., Oltmann, L.F. and Stouthamer, A.H. (1991) Isolation and characterization of the moxJ,moxG, moxI, and moxR genes of Paracoccus denitrificans: inactivation of moxJ,moxG, and moxR and the resultant effect on methylotrophic growth, J. Bacteriol. 173 6948–6961.

    Google Scholar 

  63. van Spanning, RJ.M., Wansell, C.W., Reijnders, W.N.M., Harms, N., Ras, J., Oltmann, L.F. and Stouthamer, A.H. (1991) A method for introduction of unmarked mutations in the genre of Paracoccus denitrificans: Construction of strains with multiple mutations in the genes encoding periplasmic cytochromes c 550, c 553i, and c 553i J. Bacteriol. 173 6962–6970.

    Google Scholar 

  64. van Spanning, RJ.M., de Boer, A.P.N., Reijnders, W.N.M., De Gier, J.W.L., Delorme, C.O., Stouthamer, A.H., Westerhoff, H.V., Harms, N. and van der Oost, J. (1995) Regulation of oxidative phosphorylation; the flexible respiratory network of Paracoccus denitrificans, J. Bioenergetics and Biomembranes 27 499–512.

    Article  Google Scholar 

  65. van Spanning, R.J.M., de Boer, A.P.N., Reijnders, W.N.M., Westerhoff, ILV., Stouthamer, A.H. and van der Oost, J. (1997) FnrP and NNR of Paracoccus denitrificans are both members of the FNR family of transcriptional activators but have distinct roles in respiratory adaptation in response to oxygen limitation, Mol. Microbiol. 23 893–907.

    Article  Google Scholar 

  66. Williams, P.A., Fülöp, V., Leung, Y-C., Chan, C., Moir, J.W.B., Howlett, G., Ferguson, S.J., Radford, S.E. and Hajdu, J. (1995) Pseudospecific docking surfaces on electon transfer proteins as illustrated by pseudoazurin, cytochrome c 550 and cytochrome cd 1 nitrite reductase, Nature Structural Biology 2 975–982.

    Article  CAS  Google Scholar 

  67. Wodra, C., Kosta, S., Egert, M., Kelly, D.P. and Friedrich, C.G. (1994) Identification and sequence analysis of the soxB gene essential for sulfur oxidation of Paracoccus denitrificans GB17. J. Bacteriol. 176 6188–6191.

    Google Scholar 

  68. Yano, T., Sled, V.D., Ohnishi, T. and Yagi, T. (1996) Expression and characterisation of the flavoprotein subcomplex composed of 50-kDa (NQO1) and 25-kDa (NQO2) subunits of the proton-translocating NADH-quinone oxidoreductase of Paracoccus denitrificans, J. Biol. Chem. 271 5907–5913.

    Article  CAS  Google Scholar 

  69. Zickermann, L, Anemuller, S., Richter, O.H., Tautu, O.S., Link, T.A. and Ludwig, B. (1996) Biochemical and spectroscopic properties of the four subunit quinol oxidase (cytochrome ba 3) from Paracoccus denitrificans, Biochim. Biophys. Acta 1277 93–102.

    Article  CAS  Google Scholar 

  70. Zickermann, L, Tautu, O.S., Link, T.A., Korn, M., Ludwig, B. and Richter, O-M.H. (1997) Expression studies on the ba 3 quinol oxidase from Paracoccus denitrificans - a bb 3 variant is enzymatically inactive, Eur. J. Biochem. 246, 618–624.

    Article  CAS  Google Scholar 

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Ferguson, S.J. (1998). The Paracoccus Denitrificans Electron Transport System: Aspects of Organisation, Structures and Biogenesis. In: Canters, G.W., Vijgenboom, E. (eds) Biological Electron Transfer Chains: Genetics, Composition and Mode of Operation. NATO ASI Series, vol 512. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-5133-7_6

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