Piscicolin 126 is a class 2a bacteriocin produced by Carnobacterium maltaromaticum strains UAL26 and JG126. Whilst strain UAL26 shows temperature-dependent piscicolin 126 production, strain JG126 produces bacteriocin at any growth temperature. Several clones containing combinations of the ATP-binding cassette transporter (pisT) and transporter accessory (pisE) genes from JG126 and UAL26 were created and tested for bacteriocin production. Bacteriocin production at 25 °C was observed only for a clone containing both pisT and pisE from JG126 (U-TJEJ) and a clone containing pisT from UAL26 and pisE from JG126 (U-BamTUEJ). Therefore, the deletion of a single CG base pair located on pisE of UAL26 that results in a frameshift and truncation of PisE causes the temperature-dependent piscicolin 126 production. Bacteriocin production of UAL26 was induced at 25 °C by the addition of supernatant containing the autoinducer peptide (AIP); however, the antimicrobial activity was lost after two subsequent overnight cultivations due to the presumed lack of the AIP. Changes in membrane fluidity due to changes in temperature or the presence of 2-phenylethanol (PHE) affected bacteriocin production of UAL26, but not of clones U-TJEJ or U-BamTUEJ. Similarly, increased membrane fluidity due to PHE addition reduced production of sakacin A in Lactobacillus sakei Lb706 and Lactobacillus curvatus LTH 1174. The mechanism involved in the temperature-dependent piscicolin 126 production was described. Due to the conformational change in PisE at 25 °C, the transport machinery was not able to translocate AIP. To the best of our knowledge, this is the first report that links membrane fluidity with the regulation of bacteriocin production.
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Funding
This study was supported by the:
Natural Sciences and Engineering Research Council of Canada
AxelssonL.,
HolckA.(1995). The genes involved in production of and immunity to sakacin A, a bacteriocin from Lactobacillus sake Lb706. J Bacteriol 177:2125–2137[PubMed]
AxelssonL.,
KatlaT.,
BjørnslettM.,
EijsinkV. G.,
HolckA.(1998). A system for heterologous expression of bacteriocins in Lactobacillus sake. FEMS Microbiol Lett 168:137–143 [View Article][PubMed]
Biemans-OldehinkelE.,
DoevenM. K.,
PoolmanB.(2006). ABC transporter architecture and regulatory roles of accessory domains. FEBS Lett 580:1023–1035 [View Article][PubMed]
DeVuystL.,
CallewaertR.,
CrabbeK.(1996). Primary metabolite kinetics of bacteriocin biosynthesis by Lactobacillus amylovorus and evidence for stimulation of bacteriocin production under unfavourable growth conditions. Microbiology 142:817–827 [View Article]
DiepD. B.,
AxelssonL.,
GrefsliC.,
NesI. F.(2000). The synthesis of the bacteriocin sakacin A is a temperature-sensitive process regulated by a pheromone peptide through a three-component regulatory system. Microbiology 146:2155–2160[PubMed]
EijsinkV. G. H.,
BrurbergM. B.,
MiddelhovenP. H.,
NesI. F.(1996). Induction of bacteriocin production in Lactobacillus sake by a secreted peptide. J Bacteriol 178:2232–2237[PubMed]
GurskyL. J.,
MartinN. I.,
DerksenD. J.,
van BelkumM. J.,
KaurK.,
VederasJ. C.,
StilesM. E.,
McMullenL. M.(2006). Production of piscicolin 126 by Carnobacterium maltaromaticum UAL26 is controlled by temperature and induction peptide concentration. Arch Microbiol 186:317–325 [View Article][PubMed]
HühneK.,
AxelssonL.,
HolckA.,
KröckelL.(1996). Analysis of the sakacin P gene cluster from Lactobacillus sake Lb674 and its expression in sakacin-negative Lb. sake strains. Microbiology 142:1437–1448 [View Article][PubMed]
JackR. W.,
WanJ.,
GordonJ.,
HarmarkK.,
DavidsonB. E.,
HillierA. J.,
WettenhallR. E. H.,
HickeyM. W.,
CoventryM. J.(1996). Characterization of the chemical and antimicrobial properties of piscicolin 126, a bacteriocin produced by Carnobacterium piscicola JG126. Appl Environ Microbiol 62:2897–2903[PubMed]
KhouitiZ.,
SimonJ. P.(2004). Carnocin KZ213 produced by Carnobacterium piscicola 213 is adsorbed onto cells during growth. Its biosynthesis is regulated by temperature, pH and medium composition. J Ind Microbiol Biotechnol 31:5–10 [View Article][PubMed]
KillianJ. A.,
FabrieC. H.,
BaartW.,
MoreinS.,
de KruijffB.(1992). Effects of temperature variation and phenethyl alcohol addition on acyl chain order and lipid organization in Escherichia coli derived membrane systems. A 2H- and 31P-NMR study. Biochim Biophys Acta 1105:253–262 [View Article][PubMed]
KroghA.,
LarssonB.,
von HeijneG.,
SonnhammerE. L.(2001). Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580 [View Article][PubMed]
KuipersO. P.,
BeerthuyzenM. M.,
de RuyterP. G.,
LuesinkE. J.,
de VosW. M.(1995). Autoregulation of nisin biosynthesis in Lactococcus lactis by signal transduction. J Biol Chem 270:27299–27304 [View Article][PubMed]
MessensW.,
VerluytenJ.,
LeroyF.,
De VuystL.(2003). Modelling growth and bacteriocin production by Lactobacillus curvatus LTH 1174 in response to temperature and pH values used for European sausage fermentation processes. Int J Food Microbiol 81:41–52 [View Article][PubMed]
Molina-HöppnerA.,
DosterW.,
VogelR. F.,
GänzleM. G.(2004). Protective effect of sucrose and sodium chloride for Lactococcus lactis during sublethal and lethal high-pressure treatments. Appl Environ Microbiol 70:2013–2020 [View Article][PubMed]
NedwellD. B.(1999). Effect of low temperature on microbial growth: lowered affinity for substrates limits growth at low temperature. FEMS Microbiol Ecol 30:101–111 [View Article][PubMed]
QuadriL. E. N.(2002). Regulation of antimicrobial peptide production by autoinducer-mediated quorum sensing in lactic acid bacteria. Antonie van Leeuwenhoek 82:133–145 [View Article][PubMed]
SchwabC.,
GänzleM. G.(2006). Effect of membrane lateral pressure on the expression of fructosyltransferases in Lactobacillus reuteri. Syst Appl Microbiol 29:89–99 [View Article][PubMed]
SkaugenM.,
CintasL. M.,
NesI. F.(2003). Genetics of bacteriocin production in lactic acid bacteria. Genetics of Lactic Acid Bacteria225–260WoodB. J. B.,
WarnerP. J.
New York: Kluwer; [View Article]
van BelkumM. J.,
StilesM. E.(1995). Molecular characterization of genes involved in the production of the bacteriocin leucocin A from Leuconostoc gelidum. Appl Environ Microbiol 61:3573–3579[PubMed]
van BelkumM. J.,
StilesM. E.(2006). Characterization of the theta-type plasmid pCD3.4 from Carnobacterium divergens, and modulation of its host range by RepA mutation. Microbiology 152:171–178 [View Article][PubMed]
VaughanA.,
EijsinkV. G.,
Van SinderenD.(2003). Functional characterization of a composite bacteriocin locus from malt isolate Lactobacillus sakei 5. Appl Environ Microbiol 69:7194–7203 [View Article][PubMed]
VogelR. F.,
PohleB. S.,
TichaczekP. S.,
HammesW. P.(1993). The competitive advantage of Lactobacillus curvatus LTH 1174 in sausage fermentations is caused by formation of curvacin A. Syst Appl Microbiol 16:457–462 [View Article]