Is the Na+-Activated NADH-Quinone-Acceptor Oxidoreductase in Marine Bacteria and Moderate Halophiles a Primary Electrogenic Na+ Pump?

  • Robert A. MacLeod
Part of the NATO ASI Series book series (NSSA, volume 201)


Tokuda and Unemoto observed that a concentration of the protonophore carbonyl cyanide m-chlorophenylhydrazone (CCCP) which completely collapsed the membrane potential of the marine bacterium Vibrio alginolyticus 138-2 and the moderate halophile Vibrio costicola at pH 7 only partially and transiently collapsed it at pH 8.5. They also found that a concentration of CCCP which inhibited Na+ extrusion from and Na+ dependent amino acid uptake by V. alginolyticus 138-2 at pH 7.0 did not do so at pH 8.5. To explain these observations they proposed the existence of a primary electrogenic Na+ extrusion system which was uncoupler resistant and functioned best at alkaline pH. The organisms examined have been shown to have a Na+-activated NADH:quinone-acceptor oxidoreductase with a pH optimum at 8. Since mutants of V. alginolyticus 138-2 lacking this enzyme were sensitive to CCCP at pH 8.5, it was concluded that the enzyme functions as the proposed electrogenic Na+ pump. Hamaide et al., however, demonstrated Na+/H+ antiport activity at pH 8.5 inV. costicola which was sensitive to the protonophores CCCP and 3,3’,4’,4-tetrachlorosalicylanilide (TCS). MacLeod et al. found that CCCP inhibited Na+-dependent amino acid uptake into a number of marine bacteria and V. costicola at pH 8.5 if the concentration was increased sufficiently while TCS was almost as inhibitory in this capacity at pH 8.5 as at 7. Relatively low concentrations of TCS collapsed the membrane potential of V. alginolyticus 118 at pH 8.5 and prevented Na+ extrusion from the cells. These findings suggested that NADH oxidation at pH 8.5 in this organism and V. costicola leads to the extrusion of protons which in turn cause Na+ to be pumped out of the cells via a Na+/H+ antiporter. Reasons for the differences in the conclusions reached are discussed.


Marine Bacterium Proton Motive Force NADH Oxidation NADH Oxidase Carbonyl Cyanide 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. [1]
    J. L. Reichelt and P. Baumann, Arch. Microbiol.97: 329 (1974)PubMedCrossRefGoogle Scholar
  2. [2]
    G. R. Drapeau and R. A. MacLeod, Biochem. Biophys. Res. Comm.12: 111 (1963)CrossRefGoogle Scholar
  3. [3]
    R. Droniuk, P. T. S. Wong, G. Wisse and R. A. MacLeod, Appl. Environ. Microbiol.53: 1487 (1987)PubMedGoogle Scholar
  4. [4]
    Y. Kakinuma and T. Unemoto, J. Bacteriol.163: 1293 (1985)PubMedGoogle Scholar
  5. [5]
    H. M. Hassan and R. A. MacLeod, J. Bacteriol.121: 160 (1975)PubMedGoogle Scholar
  6. [6]
    T. Unemoto, M. Hayashi and M. Hayashi, J. Biochem. (Tokyo)82: 1389 (1977)Google Scholar
  7. [7]
    G. Khanna, L. DeVoe, L. Brown, D. F. Niven and R. A. MacLeod, J. Bacteriol.157: 59 (1984)PubMedGoogle Scholar
  8. [8]
    G. D. Sprott, J. P. Drozdowski, E. L. Martin and R. A. MacLeod, Can. J. Microbiol.21: 43 (1975)PubMedCrossRefGoogle Scholar
  9. [9]
    J. Thompson and R. A. MacLeod J. Biol. Chem. 248: 7106 (1973)Google Scholar
  10. [10]
    T. Unemoto and M. Hayashi, J. Biochem. (Tokyo)85: 1461 (1979)Google Scholar
  11. [11]
    H. Tokuda and T. Unemoto, Biochem. Biophys. Res. Comm.102: 265 (1981)PubMedCrossRefGoogle Scholar
  12. [12]
    H. Tokuda, Biochem. Biophys. Res. Comm.114: 113 (1983)PubMedCrossRefGoogle Scholar
  13. [13]
    H. Tokuda and T. Unemoto, J. Biol. Chem.259: 7785 (1984)PubMedGoogle Scholar
  14. [14]
    H. Tokuda and T. Unemoto, J. Bacteriol.156: 636 (1983)PubMedGoogle Scholar
  15. [15]
    T. Tsuchiya and S. Shinoda J. Bacterial. 162: 794 (1985)Google Scholar
  16. [16]
    S. Ken-Dror, R. Preger and Y. Avi-Dor, Arch. Biochim. Biophys.244: 122 (1986)CrossRefGoogle Scholar
  17. [17]
    P. A. Dibrov, V. S. Kostyrko, R. L. Lazarova, V. P. Skulachev and I. A. Smirnova, Biochim. Biophys. Acta850: 449 (1986)PubMedCrossRefGoogle Scholar
  18. [18]
    P. Dimroth and A. Thomer, Arch. Microbiol.151: 439 (1989)PubMedCrossRefGoogle Scholar
  19. [19]
    V. Müller, C. Winner and G. Gottschalk, Eur. J. Biochem.178: 519 (1988)PubMedCrossRefGoogle Scholar
  20. [20]
    F. Hamaide, D. J. Kushner and G. D. Sprott, J. Bacteriol.161: 681 (1985)PubMedGoogle Scholar
  21. [21]
    T. A. Krulwich, Biochim. Biophys. Acta726: 245 (1983)PubMedCrossRefGoogle Scholar
  22. [22]
    F. Hamaide, G. D. Sprott, and D. J. Kushner, Biochim. Biophys. Acta766: 77 (1984)PubMedCrossRefGoogle Scholar
  23. [23]
    R. A. MacLeod, G. A. Wisse and F. L. Stejskal, J. Bacteriol.170: 4330 (1988)PubMedGoogle Scholar
  24. [24]
    H. Tokuda, Methods Enzymol. 125: 520 (1986)PubMedCrossRefGoogle Scholar
  25. [25]
    S. G. A. McLaughlin and J. P. Dilger, Physiol. Rev.60: 825 (1980)PubMedGoogle Scholar
  26. [26]
    H. Tokuda and T. Unemoto, J. Biol. Chem.257: 10007 (1982)PubMedGoogle Scholar
  27. [27]
    U. Hopfer, A. L. Lehninger and W. J. Lennarz, J. Membr. Biol.3: 142 (1970)CrossRefGoogle Scholar
  28. [28]
    R. J. Lewis, E. Kaback and T. A. Krulwich, J. Gen. Microbiol.128: 427 (1982)Google Scholar
  29. [29]
    A. A. Guffanti and T. A. Krulwich, J. Biol. Chem.263: 14748 (1988)PubMedGoogle Scholar
  30. [30]
    R. J. P. Williams, FEBS Lett. 85: 9 (1978)PubMedCrossRefGoogle Scholar
  31. [31]
    F. Hamaide, D. J. Kushner and G. D. Sprott, J. Bacteriol.156: 537 (1983)PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1991

Authors and Affiliations

  • Robert A. MacLeod
    • 1
  1. 1.Department of Microbiology Macdonald CollegeMcGill UniversitySte Anne de BellevueCanada

Personalised recommendations