On the mode of action of the bacteriocin butyricin 7423. Effects on membrane potential and potassium-ion accumulation in Clostridium pasteurianum

Eur J Biochem. 1982 Sep;127(1):105-16. doi: 10.1111/j.1432-1033.1982.tb06843.x.

Abstract

1. The apparent transmembrane bulk-phase electrical potential (delta psi) of Clostridium pasteurianum was determined from the distribution ratio of the membrane-permeable cation butyltriphenylphosphonium (BuPh3P+). In glycolysing cells the highest value of delta psi, calculated on the assumption that there was no energy-dependent binding of BuPh3P+ to the organisms, was recorded in media containing only 2-3 mM K+ ions and, even so, was only 100-110 mV. 2. Efrapeptin, a BF1-directed inhibitor of the membrane H+-ATPase of Cl. pasteurianum, abolished the membrane potential (delta psi) and caused complete efflux of actively-transported K+ ions. Thus protonmotive hydrolysis of ATP generated by substrate level phosphorylation is the sole means of membrane energisation in this anaerobe. 3. At low (sublethal) concentrations, butyricin 7423 stimulated K+ efflux from Cl. pasteurianum without measurably affecting its membrane potential. At lethal and supralethal concentrations of this bacteriocin, both delta psi and active K+ uptake were abolished. 4. Whilst the addition of valinomycin to cells of Cl. pasteurianum suspended in media of low K+ concentration generated a diffusion potential to which BuPh3P+ would respond, addition of butyricin 7423 in place of valinomycin caused no such effect. Also, unlike valinomycin, butyricin 7423 did not increase the rate of K+ efflux from non-glycolysing cells of Cl. pasteurianum. Valinomycin stimulated, but butyricin 7423 inhibited, the uptake of 86Rb+ ions by glycolysing cells of Cl. pasteurianum. 5. A mutant strain of Cl. pasteurianum (viz. strain DC3) which possessed a H+-ATPase with diminished sensitivity both to N,N'-dicyclohexylcarbodiimide and to butyricin 7423, exhibited a negligible decrease in delta psi and in K+ accumulation ratio in response to concentrations of butyricin 7423 that were bactericidal to the wild-type, parent organism. Even so, the bactericidal action of butyricin 7423 on Cl. pasteurianum is not adequately explained by its ability in vitro to inhibit the membrane H+-ATPase of this organism. 6. Bactericidal concentrations of butyricin 7423 neither provoked efflux of Na+ ions from Cl. pasteurianum nor exhibited any protonophorous activity. However, at artificially high concentration, butyricin 7423 catalysed the passage of Na+ ions as well as of K+ ions through multilayer lipid membranes. 7. As a non-protonophorous uncoupler, butyricin 7423 appears to act in a similar manner to that of the membrane-active colicins. Yet no evidence was obtained that butyricin 7423 at its minimum lethal concentration might form a gated ion channel in the cytoplasmic membrane of the target cell, or act as a classic ionophore.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphatases / physiology
  • Bacterial Proteins / pharmacology*
  • Bacteriocins / pharmacology*
  • Cell Membrane / enzymology
  • Cell Membrane Permeability / drug effects
  • Chemical Phenomena
  • Chemistry
  • Clostridium / drug effects*
  • Clostridium / metabolism
  • Glycolysis / drug effects
  • Membrane Potentials / drug effects
  • Potassium / metabolism*

Substances

  • Bacterial Proteins
  • Bacteriocins
  • butyricin 7423
  • Adenosine Triphosphatases
  • Potassium