Skip to main content
SpringerLink
Log in

C1 metabolism inParacoccus denitrificans: Genetics ofParacoccus denitrificans

  • Mini-Review
  • Published:
Journal of Bioenergetics and Biomembranes Aims and scope Submit manuscript

Abstract

Paracoccus denitrificans is able to grow on the C1 compounds methanol and methylamine. These compounds are oxidized to formaldehyde which is subsequently oxidized via formate to carbon dioxide. Biomass is produced by carbon dioxide fixation via the ribulose biphosphate pathway. The first oxidation reaction is catalyzed by the enzymes methanol dehydrogenase and methylamine dehydrogenase, respectively. Both enzymes contain two different subunits in an α2β2 configuration. The genes encoding the subunits of methanol dehydrogenase (moxF andmoxI) have been isolated and sequenced. They are located in one operon together with two other genes (moxJ andmoxG) in the gene ordermoxFJGI. The function of themoxJ gene product is not yet known.MoxG codes for a cytochromec 551i , which functions as the electron acceptor of methanol dehydrogenase. Both methanol dehydrogenase and methylamine dehydrogenase contain PQQ as a cofactor. These so-called quinoproteins are able to catalyze redox reactions by one-electron steps. The reaction mechanism of this oxidation will be described. Electrons from the oxidation reaction are donated to the electron transport chain at the level of cytochromec. P. denitrificans is able to synthesize at least 10 differentc-type cytochromes. Five could be detected in the periplasm and five have been found in the cytoplasmic membrane. The membrane-bound cytochromec 1 and cytochromec 552 and the periplasmic-located cytochromec 550 are present under all tested growth conditions. The cytochromesc 551i andc 553i , present in the periplasm, are only induced in cells grown on methanol, methylamine, or choline. The otherc-type cytochromes are mainly detected either under oxygen limited conditions or under anaerobic conditions with nitrate as electron acceptor or under both conditions. An overview including the induction pattern of allP. denitrificans c-type cytochromes will be given. The genes encoding cytochromec 1, cytochromec 550, cytochromec 551i , and cytochromec 553i have been isolated and sequenced. By using site-directed mutagenesis these genes were mutated in the genome. The mutants thus obtained were used to study electron transport during growth on C1 compounds. This electron transport has also been studied by determining electron transfer rates inin vitro experiments. The exact pathways, however, are not yet fully understood. Electrons from methanol dehydrogenase are donated to cytochromec 551i . Further electron transport is either via cytochromec 550 or cytochromec 553i to cytochromeaa 3. However, direct electron transport from cytochromec 551i to the terminal oxidase might be possible as well. Electrons from methylamine dehydrogenase are donated to amicyanin and then via cytochromec 550 to cytochromeaa 3, but other routes are used also.P. denitrificans is studied by several groups by using a genetic approach. Several genes have already been cloned and sequenced and a lot of mutants have been isolated. The development of a host/vector system and several techniques for mutation induction that are used inP. denitrificans genetics will be described.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Al-Taho, N. M., Cornish, A., and Warner, P. J. (1990).Curr. Microbiol. 20, 153–157.

    Google Scholar 

  • Alefounder, P. R., and Ferguson, S. J. (1981).Biochem. Biophys. Res. Commun. 98, 778–784.

    Google Scholar 

  • Allen, L. N., and Hanson, R. S. (1985).J. Bacteriol. 161, 995–962.

    Google Scholar 

  • Ambler, R. P., Meyer, T. E., Kamen, M. D., Schickman, S. A., and Sawyer, L. (1981).J. Mol. Biol. 147, 351–356.

    Google Scholar 

  • Anderson, D. J., and Lidström, M. E. (1988).J. Bacteriol. 170, 2254–2262.

    Google Scholar 

  • Anthony, C. (1982). InThe Biochemistry of Methylotrophs, Academic Press, London.

    Google Scholar 

  • Anthony, C. (1988). InBacterial Energy Transduction (Anthony, C., ed.), Academic Press, London, pp. 293–316.

    Google Scholar 

  • Anthony, C., and Zatman, L. J. (1964).Biochem. J. 92, 614–621.

    Google Scholar 

  • Anthony, C., and Zatman, L. J. (1967).Biochem. J. 104, 953–959.

    Google Scholar 

  • Arfman, N., Watling, E. M., Clement, W., van Oosterwijk, R. J., de Vries, G. E., Harder, W., Attwood, M. M., and Dijkhuizen, L. (1989).Arch. Microbiol. 152, 280–288.

    Google Scholar 

  • Amitage, J. P., Ingham, C., and Evans, M. C. W. (1985).J. Bacteriol. 161, 967–972.

    Google Scholar 

  • Baccanini-Melandri, A., Jones, O. T. G., and Hauska, G. (1978).FEBS Lett. 86, 151–154.

    Google Scholar 

  • Bamforth, C. W., and O'Connor, M. L. (1979).J. Gen. Microbiol. 110, 143–149.

    Google Scholar 

  • Bamforth, C. W., and Quayle, J. R. (1978).Arch. Microbiol. 119, 91–97.

    Google Scholar 

  • Barth, P. T., and Grinter, N. J. (1974).J. Bacteriol. 120, 619–630.

    Google Scholar 

  • Bastien, C., Machlin, S., Zhang, Y., Donaldson, K., and Hanson, R. S. (1989).J. Bacteriol. 55, 3124–3130.

    Google Scholar 

  • Beandmore-Gray, M., O'Keeffe, D. T., and Anthony, C. (1983).J. Gen. Microbiol. 129, 923–933.

    Google Scholar 

  • Berry, E. A., and Trumpower, B. L. (1985).J. Biol. Chem. 260, 2458–2467.

    Google Scholar 

  • Beyerinck, M. W., and Minkman, D. C. J. (1910).Zentralbl. Bakteriol. Parasitenkd. Infektionskr. Hyg. Abt. Z. 25, 30–63.

    Google Scholar 

  • Biville, F., Mazodier, P., Gasser, F., Van Kleef, M. A. G. and Duine, J. A. (1988).FEMS Microbiol. Lett. 52, 53–58.

    Google Scholar 

  • Biville, F., Turlin, E., and Gasser, F. (1989).J. Gen. Microbiol. 135, 2917–2929.

    Google Scholar 

  • Bosma, G. (1989). Ph.D. Thesis, Free University Amsterdam, The Netherlands.

    Google Scholar 

  • Bosma, G., Braster, M., Stouthamer, A. H., and Van Verseveld, H. W. (1987a).Eur. J. Biochem. 165, 665–670.

    Google Scholar 

  • Bosma, G., Braster, M., Stouthamer, A. H., and Van Verseveld, H. W. (1987b).Eur. J. Biochem. 165, 657–664.

    Google Scholar 

  • Chandra, T. S., and Shethna, E. V. (1975).Antonie van Leeuwenhoek 41, 465–477.

    Google Scholar 

  • Cox, R. B., and Quayle, J. R. (1975).Biochem. J. 150, 569–571.

    Google Scholar 

  • Davidson, V. L. (1989).Biochem. J. 261, 107–111.

    Google Scholar 

  • Davidson, V. L. and Kumar, M. A. (1989).FEBS Lett. 245, 271–273.

    Google Scholar 

  • Davidson, V. L., and Neher, J. W. (1987).FEMS Microbiol. Lett. 44, 121–124.

    Google Scholar 

  • Day, D. J., Nunn, D. N., and Anthony, C. (1990).J. Gen. Microbiol. 136, 181–188.

    Google Scholar 

  • De Beer, R., Duine, J. A., Frank, J. Jzn., and Large, P. J. (1980).Biochim. Biophys. Acta 622, 370–374.

    Google Scholar 

  • De Vries, G. E. (1986).FEMS Microbiol. Rev. 39, 235–258.

    Google Scholar 

  • De Vries, G. E., Harms, N., Maurer, K., Papendrecht, A., and Stouthamer, A. H. (1988).J. Bacterial. 170, 3731–3737.

    Google Scholar 

  • De Vries, G. E., Harms, N., Hoogendijk, J., and Stouthamer, A. M. (1989).Arch. Microbiol. 152, 52–57.

    Google Scholar 

  • De Vries, G. E., Kües, U., and Stahl, U. (1990).FEMS Microbiol. Rev. 75, 57–102.

    Google Scholar 

  • Dijkhuizen, L., Timmerman, J. W. C., and Harder, W. (1979).FEMS Microbiol. Lett. 6, 53–56.

    Google Scholar 

  • Dijkstra, M., Frank, J. Jzn., and Duine, J. A. (1988a).Biochem. J. 257, 87–94.

    Google Scholar 

  • Dijkstra, M., Frank, J. Jzn., and Duine, J. A. (1988b).FEBS Lett. 227, 198–202.

    Google Scholar 

  • Dispirito, A. A., Waechter-Brulla, D., and Lidström, M. E. (1989). InAbstracts of 6th International Symposium on Microbial growth on C1 compounds. Göttingen, Germany, p. 311.

  • Ditta, G., Stanfield, S., Corbin, D., and Helinski, D. R. (1980).Proc. Natl. Acad. Sci. USA 77, 7347–7351.

    Google Scholar 

  • Duine, J. A., Frank, J. Jzn., and De Ruiter, L. G. (1979).J. Gen. Microbiol. 115, 523–526.

    Google Scholar 

  • Duine, J. A., Frank, J. Jzn., and Verwiel, P. E. J. (1980).Eur. J. Biochem. 108, 187–192.

    Google Scholar 

  • Duine, J. A., Frank, J., and Berkhout, M. P. J. (1984).FEBS Lett. 168, 217–221.

    Google Scholar 

  • Duine, J. A., Frank, J. Jzn., and Jongejan, J. A. (1987). InAdvances in Enzymology and Related Areas of Molecular Biology (Meister, A., ed.), Vol. 59, Wiley, New York, pp. 169–212.

    Google Scholar 

  • Elliot, J. E., and Anthony, C. (1988).J. Gen. Microbiol. 134, 369–371.

    Google Scholar 

  • Ford, S., Page, M. D., and Anthony, C. (1985).J. Gen. Microbiol. 131, 2173–2182.

    Google Scholar 

  • Frank, J. Jzn., Dijkstra, M., Duine, J. A., and Balney, C. (1988).Eur. J. Biochem. 174, 331–338.

    Google Scholar 

  • Friedrich, C. G., Bowien, B., and Friedrich, B. (1979).J. Gen. Microbiol. 115, 185–192.

    Google Scholar 

  • Gennis, R. B., Casey, R. P., Azzi, A., and Ludwig, B. (1982).Eur. J. Biochem. 125, 189–195.

    Google Scholar 

  • Gerhus, E., Steinrücke, P., and Ludwig, B., (1990).J. Bacteriol. 172, 2392–2400.

    Google Scholar 

  • Gerstenberg, C., Friedrich, B., and Schlegel, H. G. (1982).Arch. Microbiol. 133, 90–96.

    Google Scholar 

  • Gray, K. A., Kraft, D. B., Husain, M., and Davidson, V. L. (1986).FEBS Lett. 207, 239–242.

    Google Scholar 

  • Gray, K. A., Davidson, V. L. and Knall, D. B. (1988).J. Biol. Chem. 263, 13987–13990.

    Google Scholar 

  • Greenwood, J. A., and Jones, C. W. (1986).J. Gen. Microbiol. 132, 1247–1256.

    Google Scholar 

  • Haltia, T., Finel, M., Harms, N., Nakari, T., Raitio, M., Wikström, M., and Saraste, M. (1989).EMBO J. 8, 3572–3579.

    Google Scholar 

  • Harms, N. (1988). Ph.D. Thesis, Free University, Amsterdam, The Netherlands.

    Google Scholar 

  • Harms, N., de Vries, G. E., Maurer, K., Veltkamp, E., and Stouthamer, A. H. (1985).J. Bacteriol. 164, 1064–1070.

    Google Scholar 

  • Harms, N., de Vries, G. E., Maurer, K., Hoogendijk, J. and Stouthamer, A. H. (1987).J. Bacteriol. 169, 3969–3975.

    Google Scholar 

  • Harms, N., Van Spanning, R. J. M., Oltmann, L. F., and Stouthamer, A. H. (1989).Antonie van Leeuwenhoek 56, 47–50.

    Google Scholar 

  • Heiss, B., Frunzke, K., and Zumft, W. G. (1989).J. Bacteriol. 171, 3288–3297.

    Google Scholar 

  • Hou, C. T. (1984). InMethylotrophs: Microbiology, Biochemistry, and Genetics. (Hou, C. I., ed.), CRC Press, Boca Raton, Florida, pp. 1–53.

    Google Scholar 

  • Husain, M., and Davidson, V. L. (1985).J. Biol. Chem. 260, 14626–14629.

    Google Scholar 

  • Husain, M., and Davidson, V. L. (1986).J. Biol. Chem. 261, 8577–8580.

    Google Scholar 

  • Husain, M., and Davidson, V. L. (1987a).J. Bacteriol. 169, 1712–1717.

    Google Scholar 

  • Husain, M., and Davidson, V. L. (1987b).Biochemistry 26, 4139–4143.

    Google Scholar 

  • Husain, M., Davidson, V. L., and Smith, A. J. (1986).Biochemistry 25, 2431–2436.

    Google Scholar 

  • Ishii, Y., Hase, T., Fukumori, Y., Matsubara, H., and Tobari, J. (1983).J. Biochem. (Tokyo).93, 107–119.

    Google Scholar 

  • Janssen, D. B., Kenning, S., and Witholt, B. (1987).J. Gen. Microbiol. 133, 85–92.

    Google Scholar 

  • Jones, C. W., Greenwood, J. A., Burton, S. M., Santos, H., and Turner, D. L. (1987).J. Gen. Microbiol. 133, 1511–1519.

    Google Scholar 

  • Köstler, M., and Kleiner, D. (1989).FEMS Microbiol. Lett. 65, 1–4.

    Google Scholar 

  • Kuo, L. M., Davies, H. C., and Smith, L. (1985).Biochim. Biophys. Acta 809, 388–395.

    Google Scholar 

  • Kurowski, B., and Ludwig, B. (1987).J. Biol. Chem. 262, 13805–13811.

    Google Scholar 

  • Lawton, S. A., and Anthony, C. (1985).Biochem. J. 228, 719–726.

    Google Scholar 

  • Machlin, S. M., and Hanson, R. S. (1988).J. Bacteriol. 170, 4739–4747.

    Google Scholar 

  • Machlin, S. M., Tam, P. E., Bastien, C. A., and Hanson, R. S. (1988).J. Bacteriol. 170, 141–148.

    Google Scholar 

  • Marison, I. W., and Attwood, M. M. (1980).J. Gen. Microbiol. 117, 305–313.

    Google Scholar 

  • Martinkus, K., Kennelly, P. J., Rea, T., and Timkovich, R. (1980).Arch. Biochem. Biophys. 199, 465–472.

    Google Scholar 

  • Matsumoto, T. (1978).Biochim. Biophys. Acta 552, 291–302.

    Google Scholar 

  • McIntire, W. S., and Stults, J. T. (1986).Biochem. Biophys. Res. Commun. 141, 562–568.

    Google Scholar 

  • McNerney, T., and O'Connor, M. L. (1980).Appl. Environ. Microbiol. 40, 370–375.

    Google Scholar 

  • McWhirter, R. B., and Klapper, M. H. (1989). InPQQ and Quinoproteins (Jongejan, J. A., and Duine, J. A., eds.), Kluwer Academic Publishers, Dordrecht, Boston, London, pp. 259–268.

    Google Scholar 

  • Meyer, R., Laux, R., Boch, G., Hinds, M., Bayly, R., and Shapiro, J. A. (1982).J. Bacteriol. 164, 446–455.

    Google Scholar 

  • Meyer, W. G. (1990). Ph.D. Thesis, University of Groningen, The Netherlands.

    Google Scholar 

  • Nokhal, T.-H., and Schlegel, H. G. (1983).Int. J. Syst. Bacteriol. 33, 26–37.

    Google Scholar 

  • Nunn, D. N., and Anthony, C. (1988).Biochem. J. 256, 673–676.

    Google Scholar 

  • Nunn, D. N., and Lidström, M. E. (1986a).J. Bacteriol. 166, 581–590.

    Google Scholar 

  • Nunn, D. N., and Lidström, M. E. (1986b).J. Bacteriol. 166, 591–597.

    Google Scholar 

  • Nunn, D. N., Day, D., and Anthony, C. (1989).Biochem. J. 260, 857–862.

    Google Scholar 

  • O'Connor, M. L., and Hanson, R. S. (1977).J. Gen. Microbiol. 101, 327–332.

    Google Scholar 

  • O'Keeffe, D. T. and Anthony, C. (1980).Biochem. J. 192, 411–419.

    Google Scholar 

  • Ohta, S., and Tobari, J. (1981).J. Biochem. (Tokyo).90, 215–224.

    Google Scholar 

  • Page, M. D., and Anthony, C. (1986).J. Gen. Microbiol. 132, 1553–1563.

    Google Scholar 

  • Paraskeva, C. (1979).J. Bacteriol. 139, 1062–1064.

    Google Scholar 

  • Quayle, J. R. (1961).Annu. Rev. Microbiol. 15, 119–162.

    Google Scholar 

  • Raitio, M., Tuulikki, J., and Saraste, M. (1987).EMBO J. 6, 2825–2833.

    Google Scholar 

  • Raitio, M., Pispa, J. M., Metso, T., and Saraste, M. (1990).FEBS Lett. 261, 431–435.

    Google Scholar 

  • Rodinov, Yu. V., and Zakharova, E. V. (1980).Biokhimiya 45, 854–863.

    Google Scholar 

  • Roitsch, T., and Stolp, H. (1986).Arch. Microbiol. 144, 245–247.

    Google Scholar 

  • Sahm, H. M., Cox, R. B., and Quayle, J. R. (1976).J. Gen. Microbiol. 94, 313–332.

    Google Scholar 

  • Salisbury, S. A., Forrest, H. S., Cruse, W. B. T., and Kennard, O. (1979).Nature (London)280, 843–844.

    Google Scholar 

  • Schmidhauser, T. J., and Helinski, D. R. (1905).J. Bacteriol. 164, 446–455.

    Google Scholar 

  • Shirai, S., Matsumoto, T., and Tobari, J. (1978).J. Biochem. 83, 1599–1607.

    Google Scholar 

  • Spence, D. W., and Barr, G. C. (1981).FEMS Microbiol. Lett. 12, 159–161.

    Google Scholar 

  • Steinrücke, P., Steffens, G. C. M., Panskus, G., Buse, G., and Ludwig, B. (1987).Eur. J. Biochem. 167, 431–439.

    Google Scholar 

  • Stephens, R. L., Haygood, M. G., and Lidström, M. E. (1988).J. Bacteriol. 170, 2063–2069.

    Google Scholar 

  • Timkovich, R., Dickenson, R. E., and Margoliash, E. (1976).J. Biol. Chem. 251, 2197–2206.

    Google Scholar 

  • Van der Meer, R. E., Jongejan, J. A., and Duine, J. A. (1987).FEBS Lett. 221, 299–304.

    Google Scholar 

  • Van Spanning, R. J. M., Wansell, C., Harms, N., Oltmann, L. F., and Stouthamer, A. H. (1989). InAbstracts of the 6th Int. Symp. on Microbial Growth on C1 Compounds, Göttingen, Germany, p. 340.

  • Van Spanning, R. J. M., Wansell, C., Harms, N., Oltmann, L. F., and Stouthamer, A. H. (1990).J. Bacteriol. 172, 986–996.

    Google Scholar 

  • Van Verseveld, H. W., and Stouthamer, A. H. (1978a).Arch. Microbiol. 118, 13–20.

    Google Scholar 

  • Van Verseveld, H. W., and Stouthamer, A. H. (1978b).Arch. Microbiol. 118, 21–26.

    Google Scholar 

  • Van Verseveld, H. W., Boon, J. P., and Stouthamer, A. H. (1979).Arch. Microbiol. 121, 213–223.

    Google Scholar 

  • Van Verseveld, H. W., Krab, K., and Stouthamer, A. H. (1981).Biochim. Biophys. Acta 635, 525–534.

    Google Scholar 

  • Van Wielink, J. E., Frank, J. Jzn., and Duine, J. A. (1989). InPQQ and Quinoproteins (Jongejan, J. A., and Duine, J. A., eds.), Kluwer Academic Publishers, Dordrecht, Boston, London, pp. 269–278.

    Google Scholar 

  • Vellieux, F. M. D., Huitema, F., Groendijk, H., Kalk, K. H., Frank, J. Jzn., Jongejan, J. A., Duine, J. A., Petratos, K., Drenth, J., and Hol, W. G. J. (1989).EMBO J. 8, 2171–2178.

    Google Scholar 

  • Weaver, G. A., and Lidström, M. E. (1985).J. Gen. Microbiol. 131, 2183–2197.

    Google Scholar 

  • Willison, J. C., and John, P. (1979).J. Gen. Microbiol. 115, 443–450.

    Google Scholar 

  • Willison, J. C., Haddock, B., and Boxer, D. H. (1981).FEMS Microbiol. Lett. 10, 249–255.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology, Biological Laboratory, Vrije Universiteit, De Boelelaan 1087, 1081 HV, Amsterdam, The Netherlands

    N. Harms & R. J. M. van Spanning

Authors
  1. N. Harms
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. J. M. van Spanning
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Harms, N., van Spanning, R.J.M. C1 metabolism inParacoccus denitrificans: Genetics ofParacoccus denitrificans . J Bioenerg Biomembr 23, 187–210 (1991). https://doi.org/10.1007/BF00762217

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00762217

Key Words

Search

Navigation