Cytochromes c(550), c(552), and c(1) in the electron transport network of Paracoccus denitrificans: redundant or subtly different in function?
Paracoccus denitrificans strains with mutations in the genes encoding the cytochrome c(550), c(552), or c(1) 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 bc(1) complex reduced nitrite, which is cytotoxic and accumulated in the medium. The cytochrome c(550)-deficient mutant did denitrify provided copper was present. The cytochrome c(552) 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 bc(1) complex is the electron acceptor of the Q-pool and of amicyanin. It is also the electron donor to cytochromes c(550) and c(552) and to the cbb(3)-type oxidase. Cytochrome c(552) is an electron acceptor both of the cytochrome bc(1) complex and of amicyanin, as well as a dedicated electron donor to the aa(3)-type oxidase. Cytochrome c(550) can accept electrons from the cytochrome bc(1) 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.
Otten
M F
MF
Department of Molecular Cell Physiology, Faculty of Biology, BioCentrum Amsterdam, Free University, 1081 HV Amsterdam, The Netherlands.
van der Oost
J
J
Reijnders
W N
WN
Westerhoff
H V
HV
Ludwig
B
B
Van Spanning
R J
RJ
D001426:Bacterial Proteins / Q000378:metabolism; D003300:Copper; D003574:Cytochrome c Group / Q000235:genetics / Q000378:metabolism*; D003575:Cytochromes c1 / Q000235:genetics / Q000378:metabolism*; D004579:Electron Transport; D003576:Electron Transport Complex IV / Q000378:metabolism; D007700:Kinetics; D008954:Models, Biological; D009154:Mutation; D009572:Nitrite Reductases / Q000378:metabolism*; D009573:Nitrites / Q000378:metabolism; D010101:Oxygen Consumption; D010231:Paracoccus denitrificans / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D011809:Quinones / Q000378:metabolism; D013053:Spectrophotometry
D001426:Bacterial Proteins; D003574:Cytochrome c Group; D009573:Nitrites; D011809:Quinones; C083951:cytochrome c553; C017079:mauC protein, Methylobacterium extorquens; D003300:Copper; D003575:Cytochromes c1; C022302:cytochrome C-552; C031732:cytochrome C-550; D009572:Nitrite Reductases; D003576:Electron Transport Complex IV