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Journal of Bacteriology, December 2001, p. 7017-7026, Vol. 183, No. 24
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.24.7017-7026.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Cytochromes c550, c552, and c1 in the Electron Transport Network of Paracoccus denitrificans: Redundant or Subtly Different in Function?

Marijke F. Otten,1 John van der Oost,2 Willem N. M. Reijnders,1 Hans V. Westerhoff,1,3 Bernd Ludwig,4 and Rob J. M. Van Spanning1,*

Department of Molecular Cell Physiology, Faculty of Biology, BioCentrum Amsterdam, Free University, 1081 HV Amsterdam,1 Department of Microbiology, Wageningen University, 6703 CT Wageningen,2 and Department of Mathematical Biochemistry, Swammerdam Institute of Life Sciences, BioCentrum Amsterdam, University of Amsterdam, 1018 TV Amsterdam,3 The Netherlands, and Biozentrum der Universitaet, D-60439 Frankfurt, Germany4

Received 24 July 2001/Accepted 19 September 2001

Paracoccus denitrificans strains with mutations in the genes encoding the cytochrome c550, c552, or c1 and in combinations of these genes were constructed, and their growth characteristics were determined. Each mutant was able to grow heterotrophically with succinate as the carbon and free-energy source, although their specific growth rates and maximum cell numbers fell variably behind those of the wild type. Maximum cell numbers and rates of growth were also reduced when these strains were grown with methylamine as the sole free-energy source, with the triple cytochrome c mutant failing to grow on this substrate. Under anaerobic conditions in the presence of nitrate, none of the mutant strains lacking the cytochrome bc1 complex reduced nitrite, which is cytotoxic and accumulated in the medium. The cytochrome c550-deficient mutant did denitrify provided copper was present. The cytochrome c552 mutation had no apparent effect on the denitrifying potential of the mutant cells. The studies show that the cytochromes c have multiple tasks in electron transfer. The cytochrome bc1 complex is the electron acceptor of the Q-pool and of amicyanin. It is also the electron donor to cytochromes c550 and c552 and to the cbb3-type oxidase. Cytochrome c552 is an electron acceptor both of the cytochrome bc1 complex and of amicyanin, as well as a dedicated electron donor to the aa3-type oxidase. Cytochrome c550 can accept electrons from the cytochrome bc1 complex and from amicyanin, whereas it is also the electron donor to both cytochrome c oxidases and to at least the nitrite reductase during denitrification. Deletion of the c-type cytochromes also affected the concentrations of remaining cytochromes c, suggesting that the organism is plastic in that it adjusts its infrastructure in response to signals derived from changed electron transfer routes.


* Corresponding author. Mailing address: Department of Molecular Cell Physiology, Faculty of Biology, Free University, De Boelelaan 1087, 1081 HV Amsterdam, The Netherlands. Phone: 31-20-4447179. Fax: 31-20-4447229. E-mail: spanning{at}bio.vu.nl.


Journal of Bacteriology, December 2001, p. 7017-7026, Vol. 183, No. 24
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.24.7017-7026.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Pearson, I. V., Page, M. D., van Spanning, R. J. M., Ferguson, S. J. (2003). A Mutant of Paracoccus denitrificans with Disrupted Genes Coding for Cytochrome c550 and Pseudoazurin Establishes These Two Proteins as the In Vivo Electron Donors to Cytochrome cd1 Nitrite Reductase. J. Bacteriol. 185: 6308-6315 [Abstract] [Full Text]