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Genetics and Molecular Biology |
54-dependent PTS permease of the mannose family is responsible for sensitivity of Listeria monocytogenes to mesentericin Y105
Laboratoire de Microbiologie Fondamentale et Appliquée, CNRS ESA 6031, IBMIG, UFR Sciences, 40 avenue du Recteur Pineau, 86022 Poitiers Cedex, France1
Unité des Interactions Bactéries-Cellules, Institut Pasteur, 28 rue du Dr Roux, 75724 Paris Cedex 15, France2
Author for correspondence: Yann Héchard. Tel: +33 5 49 45 40 07. Fax: +33 5 49 45 35 03. e-mail: yann.hechard{at}univ-poitiers.fr
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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54 subunit of the RNA polymerase. This points towards expression of particular 54-dependent genes. The present study describes first, ManR, a new 54-associated activator, and second, 
, a new 54-dependent PTS permease of the mannose family, both involved in sensitivity to mesentericin Y105, since interruption of their corresponding genes led to resistance of L. monocytogenes EGDe. is likely composed of three subunits encoded by the mpt operon (mptA, mptC and mptD genes). Interruption of either the proximal (mptA) or distal (mptD) gene led to resistance, supporting results obtained in Enterococcus faecalis. Accordingly, such PTS permeases of the mannose family should be involved in sensitivity of different target strains to mesentericin Y105. In L. monocytogenes, expression of the mpt operon is shown to be controlled by 54 and ManR and to be induced by both glucose and mannose. The latter result indicates that these sugars are transported by the permease. Moreover, these sugars correlatively induce sensitivity of L. monocytogenes to mesentericin Y105, strongly favouring the primary role of . MptD, a membrane subunit of , presents an additional domain compared to most IIDMan subunits described in data banks. An in-frame deletion of this domain in mptD led to resistance of L. monocytogenes, showing its connection with sensitivity and suggesting that it could be directly involved in the recognition of the target cell by mesentericin Y105. Taken together, the results of this work demonstrate that is prominent in sensitivity to mesentericin Y105 and could be a receptor for subclass IIa bacteriocins. Keywords: bacteriocin, receptor, helicase, transport, sugar
Abbreviations: PTS; phosphotransferase system
a The European Genome Consortium is composed of Philippe Glaser, Alexandra Amend, Fernando Baquero-Mochales, Patrick Berche, Helmut Bloecker, Petra Brandt, Carmen Buchrieser, Trinad Chakraborty, Alain Charbit, Elisabeth Couvé, Antoine de Daruvar, Pierre Dehoux, Eugen Domann, Gustavo Dominguez-Bernal, Lionel Durant, Karl-Dieter Entian, Lionel Frangeul, Hafida Fsihi, Francisco Garcia del Portillo, Patricia Garrido, Werner Goebel, Nuria Gomez-Lopez, Torsten Hain, Joerg Hauf, David Jackson, Jurgen Kreft, Frank Kunst, Jorge Mata-Vicente, Eva Ng, Gabriele Nordsiek, Jose Claudio Perez-Diaz, Bettina Remmel, Matthias Rose, Christophe Rusniok, Thomas Schlueter, Jose-Antonio Vazquez-Boland, Harmut Voss, Jurgen Wehland and Pascale Cossart.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). Within the class II, constituted by non-modified peptides produced mainly by lactic acid bacteria, bacteriocins of the subclass IIa, such as mesentericin Y105 (Héchard et al., 1992 ), are of particular interest (for a review see Ennahar et al., 2000 ). They are active against the foodborne pathogen Listeria monocytogenes and share a similar primary structure, with a conserved N-terminal motif (YGNGV). Subclass IIa bacteriocins induce membrane permeabilization (Abee, 1995 ; Maftah et al., 1993 ) of sensitive strains, but their target specificity and their molecular mode of action remain elusive. Whether a receptor or a docking molecule is necessary for activity of subclass IIa bacteriocins is still debated and, to date, such molecules have not been reported. We previously hypothesized that the transcriptional factor 54 (encoded by rpoN) could direct expression of a receptor since rpoN mutants of L. monocytogenes (Robichon et al., 1997 ) and Enterococcus faecalis (Dalet et al., 2000 ) are resistant to mesentericin Y105 and related subclass IIa bacteriocins. factors are subunits of the RNA polymerase holoenzyme involved in the initial step of transcription. Among them, 54 is unique since it targets conserved -24/-12 promoter sequences and requires an activator protein for transcription initiation, referred to as 54-associated activator (Morett & Segovia, 1993 ; Shingler, 1996 ). 54-associated activators are classically composed of three distinct domains respectively involved in signal reception, transcriptional activation and DNA binding. The central domain, which directs the transcriptional activation via 54 interaction, is the most highly conserved and clearly identifies these activators. To date, neither 54-regulated operons nor activator genes have been described in L. monocytogenes and, consequently, a direct link could not be established between 54 and sensitivity of L. monocytogenes to subclass IIa bacteriocins. Recently, two bacteriocin-resistant spontaneous mutants of L. monocytogenes have been linked to phosphotransferase systems (PTSs). In the first mutant, resistant to leucocin A, a two-dimensional SDS-PAGE protein analysis revealed absence of a IIAB subunit of a PTS permease (Ramnath et al., 2000 ). In the second mutant, resistant to pediocin PA-1, a ß-glucoside PTS permease was described to be overexpressed (Gravesen et al., 2000 ). PTSs are involved in both phosphorylation and transport of sugars (Postma et al., 1993 ; Saier & Reizer, 1994 ). A phosphate moiety is transferred from phosphoenolpyruvate (PEP) to the transported sugar via the PTS proteins EI, HPr and EII. The latter is a complex permease, made of three or four subunits which can be fused: IIA and IIB are cytoplasmic subunits responsible for phosphorylation, whereas IIC is an integral membrane subunit involved in sugar transport. A IID membrane subunit, associated with IIC, is found specifically in permeases of the mannose family. Interestingly, 54 has been described to be involved in PTS expression. Finally, we recently described that interruption of genes encoding a 54-associated activator (MptR) and a 54-dependent PTS permease of the mannose family (termed ) led to resistance of E. faecalis to mesentericin Y105.
To find a link between 54 and sensitivity of L. monocytogenes to mesentericin Y105, we searched for 54-associated activators and 54-dependent genes in the L. monocytogenes EGDe genome. We found an activator and a PTS permease of the mannose family that are required for sensitivity of L. monocytogenes to mesentericin Y105.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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DNA manipulations and gene interruption.
Molecular cloning and DNA manipulations were performed as described by Sambrook et al. (1989) . Restriction and modification enzymes purchased from Life Technologies were used as recommended by the manufacturer. DNA fragments, used for gene interruption experiments, were amplified by PCR using Taq polymerase and specific primers bearing a HindIII site, as follows: manR primers, 5'-CTGCCAAGCTTGGAAGAACG-3' and 5'-CATCATCTTCCAAAGCTTGATCC-3'; mptA primers, 5'-GCTGAAGCTTTTTTGCAGTCCG-3' and 5'-GATGAGAAAGCTTCAATCAACATTGG-3'; mptD primers, 5'-CATCTCCAAAGCTTGGGGTAAC-3' and 5'-GGCGCAAGCTTGATATTTACCC-3'. A 1559 bp HindIII fragment, corresponding to the Tn917–lac/rpoN junction of pRT758 (Robichon et al., 1997 ), was used for rpoN interruption. The latter DNA fragment and the PCR products were digested with HindIII and ligated at the same site in the erythromycin-resistant pHV1248
Tn10 plasmid (Petit et al., 1990 ), giving rise to plasmids pLMK50 (‘rpoN’), pLMK51 (‘manR’), pLMK54 (‘mptA’) and pLMK55 (‘mptD’). These plasmids were used to create independent knockouts in rpoN, manR, mptA and mptD by homologous recombination with the L. monocytogenes EGDe chromosome, as previously described (Kocks et al., 1992 ). Several mutants from each transformation were analysed by Southern blotting of chromosomal DNA digested by HindIII and hybridized with probe labelled by random priming from the PCR products described above (Sambrook et al., 1989 ).
Allelic exchange of mptD.
Allelic exchange of mptD was achieved by integration-excision of a plasmid bearing a deleted fragment of mptD. This fragment was obtained by PCR as follows. One gene fragment from each side of the additional domain we wanted to delete was amplified with the following primers: Del1 (5'-ATGAAGCTTTTCAAGGGGTTAAAGT TGG-3') and Del2 (5'-GCAAGGTTGTTACTTTAATTTCCGCACCTTCATCAAGTTTAACTTTCG-3') together and Del3 (5'-CGAAAGTTAAACTTGATGAAGGTGCGGAAATTAAAGTAACAACCTTGC-3') and Del4 (5'-ACGTAAGCTTTAAGTCCAGTATACGC-3') together. The resulting PCR products, overlapping by 25 bp, were then used in a PCR reaction, leading to a 84 bp deleted fragment of mptD (655–738mptD). This fragment was first cloned in pGEM-T (Promega), confirmed by sequencing and then subcloned as a HindIII fragment in pHV1248Tn10. The resulting plasmid, pLMY2, was used to achieve integration in mptD by homologous recombination. Excision events were then screened by their erythromycin sensitivity. Finally, erythromycin-sensitive clones were tested for the presence of the required deletion by PCR with primers Del1 and Del4 and sequencing. This gave rise to the strain EGY2 (EGDe-655–738mptD).
Bacteriocin purification and assays.
Mesentericin Y105 was purified as reported (Guyonnet et al., 2000 ). Nisin, a class I bacteriocin, was purchased from Sigma. L. monocytogenes sensitivity was assayed by spot-on-lawn or microtitre plate tests. The former was achieved by overlaying a BHI agar (1·5%) plate with a BHI agar lawn (0·7%) previously inoculated with 1% L. monocytogenes. Purified bacteriocin was then spotted on the lawn, the plate was incubated overnight at 37 °C and zones of inhibition were recorded. The microtitre plate tests were conducted as follows. Bacteria were grown overnight in LB medium and inoculated in 1 ml fresh LB medium to a final OD620 between 0·01 and 0·03. The culture was supplemented or not with either fructose, glucose, mannose or cellobiose at 2 g l-1. Four aliquots of 200 µl from each sample were then distributed in a microtitre plate. Plates were incubated at 37 °C with agitation at 120 r.p.m. and bacterial growth was monitored by measurement of the OD620. Purified mesentericin Y105 (100 ng) was added after 2 h, when the culture had reached an OD620 between 0·05 and 0·1.
Transcription analysis.
L. monocytogenes EGDe and its derivatives were grown in 3 ml LB medium supplemented or not with glucose, mannose, fructose or cellobiose (2 g l-1) to an OD600 of 0·6. The bacterial pellets collected by centrifugation were resuspended in 100 µl lysis buffer (10 mg lysozyme ml-1, 10 mM Tris, 1 mM EDTA, pH 7·5) and incubated for 1 h at 37 °C. Total RNA was then extracted with the RNAwiz reagent (Ambion) and treated as recommended. The RNA pellets were finally resuspended in 50 µl diethylpyrocarbonate-treated water containing 20 U RNase-free DNase I. Slot-blot hybridization was performed as described by Sambrook et al. (1989) . A 32P-labelled mptD probe was prepared by random priming from the PCR product obtained with the mptD primers described above. Radioactivity was measured with an Instant Imager apparatus (Packard).
DNA sequencing.
Cycle sequencing was achieved with the ABI Prism BigDye terminator cycle sequencing ready reaction kit (Perkin-Elmer) and analysed with the ABI Prism 310 genetic analyser.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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54-associated activators and 54-dependent genes in the EGDe genome54-associated activators to screen the L. monocytogenes EGDe genome. Three ORFs, encoding putative 54-associated activators, were found in BLAST searches. One ORF has similarity (35% identity) with activators of the NifA/NtrC family whereas the two others display similarity (31 and 38% identity) with activators of the LevR family. Inactivation of each activator gene was performed; only one, named manR, was further studied since, in contrast to the others (data not shown), its inactivation led to resistance of L. monocytogenes EGDe to mesentericin Y105 (see below). The manR gene encodes a putative 938 aa protein (GenBank accession number AF397144), which displays highest similarity with LevR of Bacillus subtilis (38% identity) (Débarbouillé et al., 1991 ) and MptR of E. faecalis (40% identity) (Héchard et al., 2001 ). According to Prosite, ManR has classical motifs found in other 54-associated activators: an ATP/GTP-binding site motif A (position 144–151) and a 54-interaction domain (position 209–224). Interestingly, ManR also bears a 10 aa sequence (position 217–226, see Fig. 1) integrally matching the classical DEAH motif, usually found in helicases (Luking et al., 1998 ). Because helicase activity could explain the energy coupling of DNA unwinding in 54-dependent transcription, such similarities between 54-associated activators and helicases were searched for but not yet found (Buck et al., 2000 ). In addition, we found a DEAH motif, differing in only one or two positions (see Fig. 1) in other 54-associated activators. These observations suggest that ManR and other 54-associated activators could harbour both an ATPase and a helicase activity, allowing initiation of transcription. Finally, ManR has two PTS regulation domains (PRD-I and PRD-II in positions 501–566 and 863–929, respectively), described in LevR of B. subtilis to be involved in regulation of its activity by PTS components.
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). They putatively encode the proteins MptA (321 aa), MptC (268 aa) and MptD (303 aa), which share high similarities with subunits of PTS permeases of the mannose family (i.e. IIABMan, IICMan, IIDMan, respectively). MptA, MptC and MptD thus compose a putative PTS permease, named .
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are involved in sensitivity to mesentericin Y10554, ManR and are involved in sensitivity of L. monocytogenes EGDe to mesentericin Y105, as previously shown for 54 of L. monocytogenes L028 (Robichon et al., 1997 ).
MptD plays a particular role in sensitivity
The distal gene of the mpt operon, mptD, seems to play a particular role in sensitivity since its interruption led to resistance. Interestingly, MptD bears an additional domain compared to three other IIDMan subunits found in the L. monocytogenes EGDe genome and to most of IIDMan subunits described in the literature except E. faecalis (Héchard et al., 2001 ) and Streptococcus salivarius (Lortie et al., 2000 ) or found in GenBank (Fig. 3). Among 22 bacterial sequenced genomes (finished or unfinished) found to possess at least one orthologue of IIDMan, only several Gram-positive bacteria (i.e. E. faecalis, Streptococcus spp. (5 examples), Lactococcus lactis and Clostridium acetobutylicum) have a IIDMan with an additional domain. Interestingly, these Gram-positive bacteria have sometimes been described to be sensitive to subclass IIa bacteriocins. The mutant strain EGY2 has an 84 bp in-frame deletion of mptD (655–738mptD), created by allelic exchange (see Methods). It likely encodes the 219–246MptD protein with a 28 aa deletion in the additional domain (bold characters in Fig. 3). Strain EGY2 was tested for sensitivity to mesentericin Y105, as described above. It was fully resistant, indicating that the presence of the additional domain is of primary importance for sensitivity.
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shows that expression of the mpt operon is highly induced in the presence of glucose or mannose. This indicates that the permease, putatively encoded by the mpt operon, is responsible for glucose and mannose transport.
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54 and ManR are responsible for its expression.
Mannose and glucose influence sensitivity of L. monocytogenes to mesentericin Y105
L. monocytogenes EGDe was grown in LB medium supplemented with glucose, mannose, fructose or cellobiose at 2 g l-1. Fig. 5(a) shows that, in the absence of mesentericin Y105, no significant difference in L. monocytogenes EGDe growth curves could be observed, whereas the presence of mesentericin Y105 affected L. monocytogenes growth in a medium supplemented with mannose or glucose but not with cellobiose or fructose. These results show that glucose and mannose specifically induce sensitivity of L. monocytogenes to mesentericin Y105.
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shows that, in the absence of mesentericin Y105, growth of L. monocytogenes increases along with mannose concentration whereas, in the presence of mesentericin Y105, growth inhibition increases along with mannose concentration. These results show that mannose (and glucose, data not shown) has a dose-dependent effect on L. monocytogenes sensitivity to mesentericin Y105. It underlines that the level of sensitivity is tightly linked to sugar availability, suggesting that mannose or glucose directly causes expression of a molecule responsible for sensitivity to mesentericin Y105. |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). Since 54 has been described to direct sensitivity of L. monocytogenes and E. faecalis to subclass IIa bacteriocins, we thus hypothesized that it could be responsible for the expression of such a receptor.
We demonstrate here that the 54 regulon of L. monocytogenes is clearly involved in sensitivity to mesentericin Y105, bringing experimental support to assessments arising from our earlier work on E. faecalis (Héchard et al., 2001 ). Interruption of either rpoN, manR, mptA or mptD (encoding, respectively, 54, a 54-associated activator and two subunits of the permease) led to resistance of L. monocytogenes EGDe. , a PTS permease of the mannose family, is encoded by the mpt operon. This operon, which bears a -24/-12 promoter, was not expressed in the rpoN and manR mutants, showing that its expression is positively controlled by 54 and ManR. In E. faecalis, the mpt operon also bears a putative -24/-12 promoter although it was not experimentally demonstrated to be regulated by MptR or 54 (Héchard et al., 2001 ). The localization of the mpo operon immediately downstream from manR suggests that it could also be controlled by ManR and preliminary results indicate a possible cross-regulation between the mpo and mpt operons. Accordingly, ManR likely controls these two operons whereas MptR of E. faecalis presumably controls expression of mpt only. Relationships between these operons would not be surprising according to the known regulation of carbohydrate metabolism.
The presence of glucose or mannose induced sensitivity of L. monocytogenes and E. faecalis to mesentericin Y105. These sugars also induced expression of the mpt operon of L. monocytogenes (not shown in E. faecalis), indicating that transports glucose and mannose in accordance with previous observations showing a specific inducible effect of the transported sugar on PTS permease expression (Postma et al., 1993 ). These correlated results suggest that the level of expression is directly linked to sensitivity of L. monocytogenes to mesentericin Y105.
Since mesentericin Y105 and related subclass IIa bacteriocins have a narrow spectrum of inhibition, we are wondering about the specificity of the target strains. The IIDMan membrane subunit of , MptD, contains an additional domain compared to most other IIDMan proteins. The mutant EGY2, which putatively encodes a truncated MptD protein, i.e. lacking 28 aa in this additional domain, became resistant to mesentericin Y105. Assuming that the truncated MptD protein is expressed and remains functional, it strongly suggests a primary role of this domain in the sensitivity of L. monocytogenes. The introduction of point mutations in the additional domain constitutes the next step of our work to confirm the role of this domain and to identify the implicated amino acids as well as their possible interaction.
The involvement of in sensitivity to subclass IIa bacteriocins is emphasized by the report of a spontaneous mutant resistant to leucocin A, a subclass IIa bacteriocin (Ramnath et al., 2000 ). The authors clearly showed the absence of expression of a IIABMan PTS component in this mutant. Moreover, the N-terminal sequence of the protein shares high identity (17 of 20 residues) with the MptA protein described here. In addition, Gravesen et al. (2000) recently reported the overexpression of a ß-glucoside PTS in a spontaneous L. monocytogenes mutant resistant to pediocin PA-1, another subclass IIa bacteriocin. This pediocin PA-1 resistant mutant was then shown to be defective in expression (Y. Héchard, unpublished results) and the ß-glucoside PTS was shown to be overexpressed in our L. monocytogenes LUT758 mutant lacking 54 (A. L. Gravesen, personal communication). In S. salivarius, mutants that lack the synthesis of IIABLMan (similar to MptA) are derepressed for several genes, such as the ß-galactosidase gene (Gauthier et al., 1990 ). We thus speculate that overexpression of the ß-glucoside PTS is a consequence of the lack of expression. Taken together, these results are evidence that is a key component for sensitivity of L. monocytogenes to different subclass IIa bacteriocins.
In conclusion, we propose that could either influence the expression of an unknown molecule involved in sensitivity or, via its IICMan–IIDMan membrane complex, be a docking molecule or a receptor for mesentericin Y105 and other subclass IIa bacteriocins. Since deletion of the additional domain of MptD led to resistance, we propose that this domain could directly interact with bacteriocins or that its deletion could change the structure of the permease, leading to a lower affinity for the bacteriocins. Finally, a IICMan–IIDMan complex has already been described to facilitate penetration of phage lambda DNA across the inner membrane of Escherichia coli (Esquinas-Rychen & Erni, 2001 ). It would be interesting to see whether both phage and bacteriocin could interact with cells via a similar mechanism.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Received 23 April 2001;
revised 3 August 2001;
accepted 23 August 2001.
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S. Calvez, A. Rince, Y. Auffray, H. Prevost, and D. Drider Identification of new genes associated with intermediate resistance of Enterococcus faecalis to divercin V41, a pediocin-like bacteriocin Microbiology, May 1, 2007; 153(5): 1609 - 1618. [Abstract] [Full Text] [PDF]
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 J. Deutscher, C. Francke, and P. W. Postma How Phosphotransferase System-Related Protein Phosphorylation Regulates Carbohydrate Metabolism in Bacteria Microbiol. Mol. Biol. Rev., December 1, 2006; 70(4): 939 - 1031. [Abstract] [Full Text] [PDF]
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S. Bieler, F. Silva, C. Soto, and D. Belin Bactericidal Activity of both Secreted and Nonsecreted Microcin E492 Requires the Mannose Permease. J. Bacteriol., October 1, 2006; 188(20): 7049 - 7061. [Abstract] [Full Text] [PDF]
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D. Drider, G. Fimland, Y. Hechard, L. M. McMullen, and H. Prevost The Continuing Story of Class IIa Bacteriocins Microbiol. Mol. Biol. Rev., June 1, 2006; 70(2): 564 - 582. [Abstract] [Full Text] [PDF]
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M. Begley, C. Hill, and R. P. Ross Tolerance of Listeria monocytogenes to Cell Envelope-Acting Antimicrobial Agents Is Dependent on SigB. Appl. Envir. Microbiol., March 1, 2006; 72(3): 2231 - 2234. [Abstract] [Full Text] [PDF]
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T. Tominaga and Y. Hatakeyama Determination of Essential and Variable Residues in Pediocin PA-1 by NNK Scanning Appl. Envir. Microbiol., February 1, 2006; 72(2): 1141 - 1147. [Abstract] [Full Text] [PDF]
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A. Oust, T. Moretro, K. Naterstad, G. D. Sockalingum, I. Adt, M. Manfait, and A. Kohler Fourier Transform Infrared and Raman Spectroscopy for Characterization of Listeria monocytogenes Strains Appl. Envir. Microbiol., January 1, 2006; 72(1): 228 - 232. [Abstract] [Full Text] [PDF]
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M. J. Yebra, V. Monedero, M. Zuniga, J. Deutscher, and G. Perez-Martinez Molecular analysis of the glucose-specific phosphoenolpyruvate : sugar phosphotransferase system from Lactobacillus casei and its links with the control of sugar metabolism Microbiology, January 1, 2006; 152(1): 95 - 104. [Abstract] [Full Text] [PDF]
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P. Tsang, J. Merritt, T. Nguyen, W. Shi, and F. Qi Identification of genes associated with mutacin I production in Streptococcus mutans using random insertional mutagenesis Microbiology, December 1, 2005; 151(12): 3947 - 3955. [Abstract] [Full Text] [PDF]
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 L. Johnsen, G. Fimland, and J. Nissen-Meyer The C-terminal Domain of Pediocin-like Antimicrobial Peptides (Class IIa Bacteriocins) Is Involved in Specific Recognition of the C-terminal Part of Cognate Immunity Proteins and in Determining the Antimicrobial Spectrum J. Biol. Chem., March 11, 2005; 280(10): 9243 - 9250. [Abstract] [Full Text] [PDF]
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J. Xue, I. Hunter, T. Steinmetz, A. Peters, B. Ray, and K. W. Miller Novel Activator of Mannose-Specific Phosphotransferase System Permease Expression in Listeria innocua, Identified by Screening for Pediocin AcH Resistance Appl. Envir. Microbiol., March 1, 2005; 71(3): 1283 - 1290. [Abstract] [Full Text] [PDF]
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V. Vadyvaloo, S. Arous, A. Gravesen, Y. Hechard, R. Chauhan-Haubrock, J. W. Hastings, and M. Rautenbach Cell-surface alterations in class IIa bacteriocin-resistant Listeria monocytogenes strains Microbiology, September 1, 2004; 150(9): 3025 - 3033. [Abstract] [Full Text] [PDF]
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M. Ramnath, S. Arous, A. Gravesen, J. W. Hastings, and Y. Hechard Expression of mptC of Listeria monocytogenes induces sensitivity to class IIa bacteriocins in Lactococcus lactis Microbiology, August 1, 2004; 150(8): 2663 - 2668. [Abstract] [Full Text] [PDF]
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G. M. Gibbs, B. E. Davidson, and A. J. Hillier Novel Expression System for Large-Scale Production and Purification of Recombinant Class IIa Bacteriocins and Its Application to Piscicolin 126 Appl. Envir. Microbiol., June 1, 2004; 70(6): 3292 - 3297. [Abstract] [Full Text] [PDF]
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S. Arous, C. Buchrieser, P. Folio, P. Glaser, A. Namane, M. Hebraud, and Y. Hechard Global analysis of gene expression in an rpoN mutant of Listeria monocytogenes Microbiology, May 1, 2004; 150(5): 1581 - 1590. [Abstract] [Full Text] [PDF]
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A. Gravesen, B. Kallipolitis, K. Holmstrom, P. E. Hoiby, M. Ramnath, and S. Knochel pbp2229-Mediated Nisin Resistance Mechanism in Listeria monocytogenes Confers Cross-Protection to Class IIa Bacteriocins and Affects Virulence Gene Expression Appl. Envir. Microbiol., March 1, 2004; 70(3): 1669 - 1679. [Abstract] [Full Text] [PDF]
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V. Vadyvaloo, J. L. Snoep, J. W. Hastings, and M. Rautenbach Physiological implications of class IIa bacteriocin resistance in Listeria monocytogenes strains Microbiology, February 1, 2004; 150(2): 335 - 340. [Abstract] [Full Text] [PDF]
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T. Katla, K. Naterstad, M. Vancanneyt, J. Swings, and L. Axelsson Differences in Susceptibility of Listeria monocytogenes Strains to Sakacin P, Sakacin A, Pediocin PA-1, and Nisin Appl. Envir. Microbiol., August 1, 2003; 69(8): 4431 - 4437. [Abstract] [Full Text] [PDF]
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D. J. Studholme and R. Dixon Domain Architectures of {sigma}54-Dependent Transcriptional Activators J. Bacteriol., March 15, 2003; 185(6): 1757 - 1767. [Full Text] [PDF]
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V. Vadyvaloo, J. W. Hastings, M. J. van der Merwe, and M. Rautenbach Membranes of Class IIa Bacteriocin-Resistant Listeria monocytogenes Cells Contain Increased Levels of Desaturated and Short-Acyl-Chain Phosphatidylglycerols Appl. Envir. Microbiol., November 1, 2002; 68(11): 5223 - 5230. [Abstract] [Full Text] [PDF]
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D. J. A. Netz, M. d. C. d. F. Bastos, and H.-G. Sahl Mode of Action of the Antimicrobial Peptide Aureocin A53 from Staphylococcus aureus Appl. Envir. Microbiol., November 1, 2002; 68(11): 5274 - 5280. [Abstract] [Full Text] [PDF]
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G. Fimland, V. G. H. Eijsink, and J. Nissen-Meyer Comparative studies of immunity proteins of pediocin-like bacteriocins Microbiology, November 1, 2002; 148(11): 3661 - 3670. [Abstract] [Full Text] [PDF]
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A. Gravesen, M. Ramnath, K. B. Rechinger, N. Andersen, L. Jansch, Y. Hechard, J. W. Hastings, and S. Knochel High-level resistance to class IIa bacteriocins is associated with one general mechanism in Listeria monocytogenes Microbiology, August 1, 2002; 148(8): 2361 - 2369. [Abstract] [Full Text] [PDF]
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), fructose (
), glucose (
) or mannose (
) at 2 g l-1; (b) mannose 0·125 g l-1 (