The Journal of Membrane Biology

, Volume 8, Issue 1, pp 45–62 | Cite as

Cation transport and electrogenesis byStreptococcus faecalis

II. Proton and sodium extrusion
  • F. M. Harold
  • D. Papineau


Glycolyzing cells ofStreptococcus faecalis 9790 accumulate large amounts of lipid-soluble cations such as dimethyldibenzylammonium (DDA+). We showed in the preceding paper that uptake of DDA+ occurs in response to an electrical potential, interior negative, which arises by extrusion of H+ and Na+. The experiments described here deal with the mechanism of electrogenesis. Evidence is presented to indicate that extrusion of protons is an electrogenic, energy-linked process which can proceed against the electrochemical gradient for H+. Proton extrusion is blocked by dicyclohexylcarbodiimide (DCCD), an inhibitor of the membrane-bound ATPase ofS. faecalis. However, in a mutant whose ATPase is resistant to DCCD, proton extrusion is also resistant to the inhibitor. We conclude from these results that the membrane-bound ATPase is involved in proton extrusion. Extrusion of sodium can also occur against the electrochemical gradient, but we find no evidence for the existence of an electrogenic sodium pump. It rather appears, from studies with ionophorous agents and inhibitors of the ATPase, that the cells extrude Na+ in exchange for H+; the H+ is then extruded by the proton pump. Evidence is presented for an influx of H+ coupled to the efflux of Na+.

Among the mutants known to be defective in K+ accumulation one class is deficient in proton extrusion and another lacks the Na+/H+ exchange. Thus, proton extrusion and Na+/H+ antiport are essential elements in K+ accumulation.


Sodium Human Physiology Electrical Potential Proton Pump Essential Element 
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.


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  1. Abrams, A., Smith, J. B., Baron, C. 1972. Carbodiimide-resistant membrane ATPase. I. Studies of the mechanism of resistance.J. Biol. Chem. (In press.) Google Scholar
  2. Chesbro, W. R., Evans, J. B. 1960. Hydroxyl ion dependent release of amino acids from enterococci.J. Bacteriol. 79:682.Google Scholar
  3. Epstein, W., Kim, B. S. 1971. Potassium transport loci inEscherichia coli K 12.J. Bacteriol. 108:639.Google Scholar
  4. Greville, G. D. 1969. A scrutiny of Mitchell's chemiosmotic hypothesis of respiratory chain and photosynthetic phosphorylation.Curr. Topics Bioenergetics 3:1.Google Scholar
  5. Grinius, L. L., Jasaitis, A. A., Kadziauskas, Yu. P., Liberman, E. A., Skulachev, V. P., Topali, V. P., Tsofina, L. M., Vladimirova, M. A. 1970. Conversion of biomembrane-produced energy into electric form: I. Submitochondrial particles.Biochim. Biophys. Acta 216:1.Google Scholar
  6. Harold, F. M. 1970. Antimicrobial agents and membrane function.Advanc. Microbial Physiol. 4:45.Google Scholar
  7. Harold, F. M., Baarda, J. R., Baron, C., Abrams, A. 1969. Inhibition of membrane-bound adenosine triphosphatase and cation transport inStreptococcus faecalis by N,N′-dicyclohexylcarbodiimide.J. Biol. Chem. 244:2261.Google Scholar
  8. Harold, F. M., Baarda, J. R., Pavlasova, E. 1970a. Extrusion of sodium and hydrogen ions as the primary process in potassium ion accumulation byStreptococcus faecalis.J. Bacteriol. 101:152.Google Scholar
  9. Harold, F. M., Papineau, D. Cation transport and electrogenesis byStreptococcus faecalis. I. The membrane potential.J. Membrane Biol. 8:27.Google Scholar
  10. Harold, F. M., Pavlasova, E., Baarda, J. R. 1970b. A transmembrane pH gradient inStreptococcus faecalis: origin, and dissipation by proton conductors and dicyclohexyl-carbodiimide.Biochim. Biophys. Acta 196:235.Google Scholar
  11. Isaev, P. I., Liberman, E. A., Samuilov, V. D., Skulachev, V. P., Tsofina, L. M. 1970. Conversion of biomembrane produced energy into electric form. III. Chromatophores ofRhodospirillum rubrum.Biochim. Biophys. Acta 216:22.Google Scholar
  12. Liberman, E. A., Skulachev, V. P. 1970. Conversion of biomembrane-produced energy into electric form. IV. General discussion.Biochim. Biophys. Acta 216:30.Google Scholar
  13. Mitchell, P. 1966. Chemiosmotic coupling in oxidative and photosynthetic phosphorylation.Biol. Rev. 41:445.Google Scholar
  14. Mitchell, P. 1967. Proton-translocation phosphorylation in mitochondria, chloroplasts and bacteria: natural fuel cells and solar cells.Fed. Proc. 26:1370.Google Scholar
  15. Mitchell, P. 1968. Chemiosmotic Coupling and Energy Transduction. Glynn Research, Bodmin, Cornwall.Google Scholar
  16. Mitchell, P. 1970. Membranes of cells and organelles: morphology, transport and metabolism.In: Organization and Control in Prokaryotic and Eukaryotic Cells. XXth Symposium of the Society for General Microbiology. H. P. Charles and B. C. J. G. Knight, editors. p. 121. Cambridge University Press.Google Scholar
  17. Mitchell, P., Moyle, J. 1968. Proton translocation coupled to ATP hydrolysis in rat liver mitochondria.Europ. J. Biochem. 4:530.Google Scholar
  18. Mitchell, P., Moyle, J. 1969. Translocation of some anions, cations and acids in rat liver mitochondria.Europ. J. Biochem. 9:149.Google Scholar
  19. Mueller, P., Rudin, D. O. 1970. Translocators in bimolecular lipid membranes: their role in dissipative and conservative bioenergy transductions.Curr. Topics Bioenergetics 3:157.Google Scholar
  20. Pressman, B. C. 1968. Ionophorous antibiotics as models of biological transport.Fed. Proc. 27:1283.Google Scholar
  21. Schnebli, H. P., Vatter, A. E., Abrams, A. 1970. Membrane adenosine triphosphatase fromStreptococcus faecalis: molecular weight, subunit structure and amino acid composition.J. Biol. Chem. 245:1122.Google Scholar
  22. Scholes, P., Mitchell, P., Moyle, J. 1969. The polarity of proton translocation in some photosynthetic microorganisms.Europ. J. Biochem. 8:450.Google Scholar
  23. Schultz, S. G., Solomon, A. K. 1961. Cation transport inEscherichia coli. I. Intracellular Na and K concentrations and net Na movement.J. Gen. Physiol. 45:355.Google Scholar
  24. Slater, E. C. 1971. The coupling between energy-yielding and energy-utilizing reactions in mitochondria.Quart. Rev. Biophys. 4:35.Google Scholar
  25. Zarlengo, M. H., Schultz, S. G. 1966. Cation transport and metabolism inStreptococcus faecalis.Biochim. Biophys. Acta 126:308.Google Scholar

Copyright information

© Springer-Verlag New York Inc. 1972

Authors and Affiliations

  • F. M. Harold
    • 1
    • 2
  • D. Papineau
    • 1
    • 2
  1. 1.Division of ResearchNational Jewish Hospital and Research CenterDenver
  2. 2.Department of MicrobiologyUniversity of Colorado Medical CenterDenver

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