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Characterization of putative class II bacteriocins identified from a non-bacteriocin-producing strain Lactobacillus casei ATCC 334

  • Applied genetics and molecular biotechnology
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Abstract

Several putative class II bacteriocin-like genes were identified in Lactobacillus casei ATCC 334, all of which might encode peptides with a double-glycine leader. Six peptides encoded by these genes were heterologously expressed in Escherichia coli and then partially purified in order to test their bacteriocin activity. The results revealed that the mature LSEI_2163 peptide was a class IId bacteriocin that exhibited antimicrobial activity against some lactobacilli and several Listeria species. Similarly, mature LSEI_2386 was a putative pheromone peptide that also had significant bacteriocin activity against several Listeria species. The activities of both peptides tolerated 121°C for 30 min but not treatment with proteinase K or trypsin. The two Cys residues located at positions 4 and 24 in the mature LSEI_2163 peptide were shown by mass spectrometry to form a disulfide bridge, which was required for optimal antibacterial activity. However, replacement of one or both Cys with Ser would cause significant reduction of the antibacterial activity, the reduction being greater when only one of the Cys residues (C4S) was replaced than when both (C4S/C24S) were replaced.

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References

  • Anderssen EL, Diep DB, Nes IF, Eijsink VG, Nissen-Meyer J (1998) Antagonistic activity of Lactobacillus plantarum C11: two new two-peptide bacteriocins, plantaricins EF and JK, and the induction factor plantaricin A. Appl Environ Microbiol 64:2269–2272

    CAS  Google Scholar 

  • Boman HG (2003) Antibacterial peptides: basic facts and emerging concepts. J Intern Med 254:197–215

    Article  CAS  Google Scholar 

  • Brurberg MB, Nes IF, Eijsink VG (1997) Pheromone-induced production of antimicrobial peptides in Lactobacillus. Mol Microbiol 26:347–360

    Article  CAS  Google Scholar 

  • Cleveland J, Montville TJ, Nes IF, Chikindas ML (2001) Bacteriocins: safe, natural antimicrobials for food preservation. Int J Food Microbiol 71:1–20

    Article  CAS  Google Scholar 

  • Cotter PD, Hill C, Ross RP (2005) Bacteriocins: developing innate immunity for food. Nat Rev Microbiol 3:777–788

    Article  CAS  Google Scholar 

  • Diep DB, Havarstein LS, Nes IF (1996) Characterization of the locus responsible for the bacteriocin production in Lactobacillus plantarum C11. J Bacteriol 178:4472–4483

    CAS  Google Scholar 

  • Diep DB, Godager L, Brede D, Nes IF (2006) Data mining and characterization of a novel pediocin-like bacteriocin system from the genome of Pediococcus pentosaceus ATCC 25745. Microbiology 152:1649–1659

    Article  CAS  Google Scholar 

  • Fimland G, Eijsink VG, Nissen-Meyer J (2002) Mutational analysis of the role of tryptophan residues in an antimicrobial peptide. Biochemistry 41:9508–9515

    Article  CAS  Google Scholar 

  • Franz CM, van Belkum MJ, Holzapfel WH, Abriouel H, Galvez A (2007) Diversity of enterococcal bacteriocins and their grouping in a new classification scheme. FEMS Microbiol Rev 31:293–310

    Article  CAS  Google Scholar 

  • Garneau S, Martin NI, Vederas JC (2002) Two-peptide bacteriocins produced by lactic acid bacteria. Biochimie 84:577–592

    Article  CAS  Google Scholar 

  • Hauge HH, Mantzilas D, Moll GN, Konings WN, Driessen AJ, Eijsink VG, Nissen-Meyer J (1998) Plantaricin A is an amphiphilic alpha-helical bacteriocin-like pheromone which exerts antimicrobial and pheromone activities through different mechanisms. Biochemistry 37:16026–16032

    Article  CAS  Google Scholar 

  • Havarstein LS, Diep DB, Nes IF (1995) A family of bacteriocin ABC transporters carry out proteolytic processing of their substrates concomitant with export. Mol Microbiol 16:229–240

    Article  CAS  Google Scholar 

  • Holo H, Nilssen O, Nes IF (1991) Lactococcin A, a new bacteriocin from Lactococcus lactis subsp. cremoris: isolation and characterization of the protein and its gene. J Bacteriol 173:3879–3887

    CAS  Google Scholar 

  • Huhne K, Axelsson L, Holck A, Krockel L (1996) Analysis of the sakacin P gene cluster from Lactobacillus sake Lb674 and its expression in sakacin-negative Lb. sake strains. Microbiology (Reading, England) 142:1437–1448

    Article  Google Scholar 

  • Kalmokoff ML, Banerjee SK, Cyr T, Hefford MA, Gleeson T (2001) Identification of a new plasmid-encoded sec-dependent bacteriocin produced by Listeria innocua 743. Appl Environ Microbiol 67:4041–4047

    Article  CAS  Google Scholar 

  • Kjos M, Snipen L, Salehian Z, Nes IF, Diep DB (2010) The abi proteins and their involvement in bacteriocin self-immunity. J Bacteriol 192:2068–2076

    Article  CAS  Google Scholar 

  • Klaenhammer TR (1988) Bacteriocins of lactic acid bacteria. Biochimie 70:337–349

    Article  CAS  Google Scholar 

  • Maqueda M, Galvez A, Bueno MM, Sanchez-Barrena MJ, Gonzalez C, Albert A, Rico M, Valdivia E (2004) Peptide AS-48: prototype of a new class of cyclic bacteriocins. Curr Protein Pept Sci 5:399–416

    Article  CAS  Google Scholar 

  • Moretro T, Naterstad K, Wang E, Aasen IM, Chaillou S, Zagorec M, Axelsson L (2005) Sakacin P non-producing Lactobacillus sakei strains contain homologues of the sakacin P gene cluster. Res Microbiol 156:949–960

    Article  CAS  Google Scholar 

  • Nikolskaya AN, Galperin MY (2002) A novel type of conserved DNA-binding domain in the transcriptional regulators of the AlgR/AgrA/LytR family. Nucleic Acids Res 30:2453–2459

    Article  CAS  Google Scholar 

  • Nissen-Meyer J, Nes IF (1997) Ribosomally synthesized antimicrobial peptides: their function, structure, biogenesis, and mechanism of action. Arch Microbiol 167:67–77

    Article  CAS  Google Scholar 

  • Nissen-Meyer J, Rogne P, Oppegard C, Haugen HS, Kristiansen PE (2009) Structure-function relationships of the non-lanthionine-containing peptide (class II) bacteriocins produced by gram-positive bacteria. Curr Pharm Biotechnol 10:19–37

    Article  CAS  Google Scholar 

  • Oppegard C, Rogne P, Emanuelsen L, Kristiansen PE, Fimland G, Nissen-Meyer J (2007) The two-peptide class II bacteriocins: structure, production, and mode of action. J Mol Microbiol Biotechnol 13:210–219

    Article  CAS  Google Scholar 

  • Richard C, Drider D, Elmorjani K, Marion D, Prevost H (2004) Heterologous expression and purification of active divercin V41, a class IIa bacteriocin encoded by a synthetic gene in Escherichia coli. J Bacteriol 186:4276–4284

    Article  CAS  Google Scholar 

  • Saenz Y, Rojo-Bezares B, Navarro L, Diez L, Somalo S, Zarazaga M, Ruiz-Larrea F, Torres C (2009) Genetic diversity of the pln locus among oenological Lactobacillus plantarum strains. Int J Food Microbiol 134:176–183

    Article  CAS  Google Scholar 

  • Tichaczek PS, Vogel RF, Hammes WP (1994) Cloning and sequencing of sakP encoding sakacin P, the bacteriocin produced by Lactobacillus sake LTH 673. Microbiology 140:361–367

    Article  CAS  Google Scholar 

  • Venema K, Abee T, Haandrikman AJ, Leenhouts KJ, Kok J, Konings WN, Venema G (1993) Mode of action of lactococcin B, a thiol-activated bacteriocin from Lactococcus lactis. Appl Environ Microbiol 59:1041–1048

    CAS  Google Scholar 

  • Venema K, Dost MH, Venema G, Kok J (1996) Mutational analysis and chemical modification of Cys24 of lactococcin B, a bacteriocin produced by Lactococcus lactis. Microbiology 142:2825–2830

    Article  CAS  Google Scholar 

  • Wang G, Li X, Wang Z (2009) APD2: the updated antimicrobial peptide database and its application in peptide design. Nucleic Acids Res 37:D933–D937

    Article  CAS  Google Scholar 

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Acknowledgments

This work is supported in part by a grant (NSC99-2628-B007-001-MY3) from the National Science Council of Taiwan, R.O.C.

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Authors and Affiliations

  1. Institute of Molecular Medicine and Department of Life Science, National Tsing Hua University, Hsinchu, Taiwan, Republic of China

    Yang-Cheng Kuo, Cheng-Feng Liu, Jhao-Fen Lin, An-Chieh Li, Ta-Chun Lo & Thy-Hou Lin

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  1. Yang-Cheng Kuo
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  2. Cheng-Feng Liu
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  3. Jhao-Fen Lin
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  4. An-Chieh Li
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Correspondence to Thy-Hou Lin.

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Kuo, YC., Liu, CF., Lin, JF. et al. Characterization of putative class II bacteriocins identified from a non-bacteriocin-producing strain Lactobacillus casei ATCC 334. Appl Microbiol Biotechnol 97, 237–246 (2013). https://doi.org/10.1007/s00253-012-4149-2

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