Bioenergetic mechanism for nisin resistance, induced by the acid tolerance response of Listeria monocytogenes.
This study examined the bioenergetics of Listeria monocytogenes, induced to an acid tolerance response (ATR). Changes in bioenergetic parameters were consistent with the increased resistance of ATR-induced (ATR(+)) cells to the antimicrobial peptide nisin. These changes may also explain the increased resistance of L. monocytogenes to other lethal factors. ATR(+) cells had lower transmembrane pH (DeltapH) and electric potential (Deltapsi) than the control (ATR(-)) cells. The decreased proton motive force (PMF) of ATR(+) cells increased their resistance to nisin, the action of which is enhanced by energized membranes. Paradoxically, the intracellular ATP levels of the PMF-depleted ATR(+) cells were approximately 7-fold higher than those in ATR(-) cells. This suggested a role for the F(o)F(1) ATPase enzyme complex, which converts the energy of ATP hydrolysis to PMF. Inhibition of the F(o)F(1) ATPase enzyme complex by N'-N'-1,3-dicyclohexylcarbodiimide increased ATP levels in ATR(-) but not in ATR(+) cells, where ATPase activity was already low. Spectrometric analyses (surface-enhanced laser desorption ionization-time of flight mass spectrometry) suggested that in ATR(+) listeriae, the downregulation of the proton-translocating c subunit of the F(o)F(1) ATPase was responsible for the decreased ATPase activity, thereby sparing vital ATP. These data suggest that regulation of F(o)F(1) ATPase plays an important role in the acid tolerance response of L. monocytogenes and in its induced resistance to nisin.
Bonnet
Marcelo
M
Department of Food Science, Rutgers, The State University of New Jersey, 65 Dudley Rd., New Brunswick, NJ 08901, USA.
Rafi
Mohamed M
MM
Chikindas
Michael L
ML
Montville
Thomas J
TJ
D000900:Anti-Bacterial Agents / Q000494:pharmacology*; D024881:Drug Resistance, Bacterial; D004734:Energy Metabolism; D018869:Heat-Shock Response; D006863:Hydrogen-Ion Concentration; D008089:Listeria monocytogenes / Q000187:drug effects / Q000502:physiology*; D008564:Membrane Potentials; D009561:Nisin / Q000494:pharmacology*; D006180:Proton-Translocating ATPases / Q000378:metabolism
D000900:Anti-Bacterial Agents; D009561:Nisin; D006180:Proton-Translocating ATPases