Fitness costs associated with class IIa bacteriocin resistance in Listeria monocytogenes B73

Abstract

I NG S. 1998. In order to assess the potential for the spread of class IIa bacteriocin resistance in natural populations of Listeria monocytogenes, the fitness costs associated with resistance to leucocins A, B and E and sakacin A in L. monocytogenes B73 in the absence of bacteriocin were examined. The resistant phenotype had a lower growth rate (and thus relative fitness) than the sensitive phenotype in monoculture experiments. Furthermore, resistant phenotypes were unable to invade populations of the sensitive strain, even at frequencies of 10 −1 or higher, when grown in co-culture. These results held true for resistant strains that had been exposed to bacteriocin for 25 successive growth cycles. It was concluded that the class IIa bacteriocin-resistant phenotype of L. monocytogenes B73 is unlikely to become stable in natural populations based on this evidence. Due to the possibility of variations in the frequencies of spontaneous mutation and fitness among Listeria strains, however, the extrapolation of these results to the species as a whole should not be made. INTRODUCTIONthe class IIa group is apparent, while bacteriocins belonging to other classes are not protected against (Rekhif et al. 1994). Bacteriocins are proteinaceous anti-competitor toxins, pro-The ecology of resistance to antimicrobial compounds has duced by bacteria, that act against the same or closely related been investigated with respect to many commonly used traspecies (Jack et al. 1995 ; Nes et al. 1996). The class II ditional antibiotics, such as tetracycline, because of the medibacteriocins are a subset of these compounds, which are cal significance of the spread of such resistance (Johnson and characteristically small, heat-stable, cationic peptides, proAdams 1992). Little, however, is known about the ecology of duced by lactic acid bacteria (Klaenhammer 1993). Class IIa resistance to bacteriocins and other antimicrobial peptides bacteriocins, such as the leucocins produced by members of (Frank 1994 ; Dykes 1995). With an increased interest in the the genus Leuconostoc, exhibit inhibitory activity against the commercial application of bacteriocins as biopreservatives (de important foodborne pathogen Listeria monocytogenes Vuyst and Vandamme 1994), investigations into the ecology (Hastings et al. 1991 ;Klaenhammer 1993 ; Felix et al. 1994).of resistance to these compounds is important to assess the The development of spontaneous L. monocytogenes mutants, potential for spread of resistance in natural populations. In resistant to class IIa bacteriocins such as mesenterocin 52 and this study the fitness costs associated with class IIa bacteriocin pediocin AcH, have been reported (Larsen and No Ârrung resistance in L. monocytogenes was investigated, along with 1993 ; Noerlis and Ray 1994 ;Rekhif et al. 1994). The mechimplications this has for the spread of resistance in popuanism of resistance to bacteriocins such as nisin, which lations of this pathogen. belongs to the class I bacteriocins or lantibiotics, have been investigated widely and...

Frequency of Bacteriocin Resistance Development and Associated Fitness Costs in Listeria monocytogenes

“…A fitness cost as described above would be expected to influence the stability of a bacteriocin-resistant culture, since a bacteriocin-sensitive revertant with a higher growth rate would invade the resistant culture, as described previously (10). It is therefore surprising that bacteriocin resistance in most cases was very stable and that the pediocin-resistant mutants, in spite of having more pronounced fitness costs, were more stable than their nisin-resistant counterparts.…”

“…In one report, however, sequential exposure to nisin was required to attain stable resistance to the bacteriocin in L. monocytogenes (27). Resistance to class IIa and other bacteriocins occurred at frequencies of 10 Ϫ6 to 10 Ϫ3 in L. monocytogenes (10,33,41), and the developed resistance was stable in some mutants (9,33) but unstable in others (10). Pediocin resistance has been reported to develop at very high levels (see, for example, reference 9), ostensibly by an on-off type mechanism, but nisin resistance occurs by small and gradual increases in MIC (15).…”

“…In concordance with this, bacteriocin resistance development has in most, but not all, mutants been associated with fitness costs. Nisin or class IIa bacteriocin resistance conferred various degrees of growth inhibition in some spontaneous mutants of Listeria and other organisms (9,10,14,21,26,27), while others had growth characteristics similar to those of the wild-type strain (3,39).…”

Physiological implications of class IIa bacteriocin resistance in Listeria monocytogenes strains

“…The decreased growth rate in 412P, and in other class IIa bacteriocin-resistant B73 strains (Dykes & Hastings, 1998), has been interpreted as a fitness cost associated with class IIa bacteriocin resistance. This fitness cost was thought to be due to energyexpensive metabolic pathways in resistant strains (Dykes & Hastings, 1998). By taking a closer look at the physiology of these resistant strains, we can suggest a more straightforward explanation for the reduction in specific growth rate, namely the reduced consumption rate of glucose.…”

Antibacterial efficacy of nisin, pediocin 34 and enterocin FH99 against L. monocytogenes, E. faecium and E. faecalis and bacteriocin cross resistance and antibiotic susceptibility of their bacteriocin resistant variants

“…This could be related to the fitness cost commonly associated to the development of the nisin resistant phenotype i.e. the changes conferring bacteriocin resistance could possibly reduce the growth potential of the cells or render them more sensitive to preservation parameters such as salt, low pH, or low temperature (Dykes and Hastings 1998). Only cross-resistance to the membrane disturbing polymixin B was depicted by the three resistant variants of E. faecium (VRE).…”