Correlation of bioenergetic parameters with cell death in Listeria monocytogenes cells exposed to nisin

Abstract

In Listeria monocytogenes, nisin induced ATP efflux, reduced the intracellular ATP concentration within 1 min, and dissipated the proton motive force within 2 min. Efilux accounted for only 20% of the ATP depletion, suggesting that ATP hydrolysis also occurred. ATP efflux depended on nisin concentration and followed saturation kinetics. These results suggest that nisin breaches the membrane permeability barrier in a manner more consistent with pore formation than with a nonspecific detergent-like membrane destabilization.

Bacteriocin inhibition of two glucose transport systems in Listeria monocytogenes

“…The decrease in intracellular ATP and concomitant increase in extracellular ATP observed when L. monocytogenes cells were treated with nisin indicate that intact ATP is leaking from the cells. These results are similar to the findings of Abee et al (1994a) and Winkowski et al (1994) although the efflux in these studies (× 100%) was much greater than the 40% reported for nisin Z and 20% reported for nisin A. Cells treated with pediocin JD and leuconosin S had less efflux of intact ATP (1·5% and 41·1% of initial levels, respectively) although an almost total depletion of intracellular ATP did occur.…”

“…Such interaction of monomers results in pore formation within the membrane . While either model is consistent with the membrane disruption and loss of PMF observed in bacteriocin-sensitive cells, evidence of saturation kinetics and bacteriocin inhibition mechanisms, such as leakage of intracellular ATP and other large molecules, favour the poration complex model (Winkowski et al 1994;Montville et al 1995). Although it has been shown that bacteriocins dissipate PMF in sensitive cells, other inhibitory effects probably occur which are either a result of PMF dissipation or independent of any effect on PMF.…”

“…In contrast, the lower efflux of ATP and P i from leuconosin S-(Class IV bacteriocin) treated cells and efflux of P i from pediocin JD-(Class IIa) treated cells indicate a different or more transient type of pore formation than that found with nisin. It appears that ATP is hydrolysed in L. monocytogenes Scott A cells treated with pediocin JD or leuconosin S. This may be in an attempt to maintain a PMF, as suggested by the Montville groups (Winkowski et al 1994;Chen and Montville 1995), or due to a shift in the equilibrium between ATP and ADP ¦ P i from loss of P i , as suggested by Abee et al (1994a).…”

“…Naturally produced by many Gram-positive bacteria, bacteriocins are small antimicrobial peptides that have an inhibitory effect on other, usually closely related, species of bacteria. Leuconosin S, nisins A and Z and pediocin JD are among the bacteriocins reported to inhibit the growth of L. monocytogenes (Bruno et al 1992;Christensen and Hutkins 1992;Lewus et al 1992;Bruno and Montville 1993;Abee et al 1994a;Winkowski et al 1994). Although exact mechanisms of inhibition are not entirely known, it is generally accepted that bacteriocins inhibit growth of sensitive bacteria by disrupting the integrity of the cell membrane.…”

“…© 1998 The Society for Applied Microbiology Christensen and Hutkins 1992;Bruno and Montville 1993;Venema et al 1993;Abee et al 1994b; Montville and Bruno 1994;Winkowski et al 1994;Montville et al 1995). In addition to dissipation of PMF, bacteriocins are reported to deplete intracellular adenosine triphosphate (ATP), either through leakage or hydrolysis, and to cause efflux of intracellular inorganic phosphate (P i ) (Abee et al 1994a;Abee et al 1994b;Winkowski et al 1994;Chen and Montville 1995). Some bacteriocins also inhibit uptake and induce efflux of nutrients such as amino acids and sugars (van Belkum et al 1991;Venema et al 1993;Christensen and Hutkins 1994).…”