Abstract
Bacteriocins produced by lactic acid bacteria (LAB) are ribosomally synthesized antimicrobial peptides, with a diverse mode of bactericidal activity. This study focused on characterization of the bactericidal activity of bacteriocin ST8SH, with special attention to control of Listeria and Enteroccus species. Lactobacillus plantarum ST8SH produces a bacteriocin of the pediocin PA-1 family (sharing 96 % similarity on genetic level) with activity against several LAB, Enterococcus spp., Klebsiella pneumoniae, Listeria spp., Streptococcus spp. and some other human and foodborne pathogens. Addition of bacteriocin ST8SH to exponential or stationary phase cultures of L. monocytogenes ScottA and E. faecalis ATCC 19433 inhibited growth for 12 h. The effects of bacteriocin ST8SH on L. monocytogenes ScottA and E. faecalis ATCC 19433 were recorded indirectly based on enzyme, protein and nucleotide material leakage. Considering the antimicrobial activity of bacteriocin ST8SH against the tested microorganisms, and the physiological characteristics of Lb. plantarum ST8SH, either the bacteriocin or the strain may be used as tools for biopreservation.
Similar content being viewed by others
References
Albano H, Todorov SD, van Reenen CA, Hogg T, Dicks LMT, Teixeira P (2007) Characterization of a bacteriocin produced by Pediococcus acidilactici isolated from “Alheira”, a fermented sausage traditionally produced in Portugal. Int J Food Microbiol 116:239–247
Atrih A, Rekhif N, Moir AJG, Lebrihi A, Lefebvre G (2001) Mode of action, purification and amino acid sequence of plantaricin C19, an anti-Listeria bacteriocin produced by Lactobacillus plantarum C19. Int J Food Microbiol 68:93–109
Bauer R, Chikindas ML, Dicks LMT (2005) Purification, partial amino acid sequence and mode of action of pediocin PD-1, a bacteriocin produced by Pediococcus damnosus NCFB 1832. Int J Food Microbiol 101:17–27
Bhunia AK, Kim WJ, Johnson MS, Ray B (1988) Purification, characterization and antimicrobial spectrum of a bacteriocin produced by Pediococcus acidilactici. J Appl Bacteriol 65:261–268
Bhunia AK, Johnson MC, Ray B, Kalchayanand N (1991) Mode of action of pediocin AcH from Pedicoccus acidilactici H on sensitive bacterial strains. J Appl Bacteriol 70:25–33
Bredholt S, Nesbakken T, Holck A (2001) Industrial application of an antilisterial strain of Lactobacillus sakei as a protective culture and its effect on the sensory acceptability of cooked, sliced, vacuum-packed meats. Int J Food Microbiol 66:191–196
Castellano P, Holzapfel WH, Vignolo G (2004) The control of Listeria innocua and Lactobacillus sakei in broth and meat slurry with the bacteriocinogenic strain Lactobacillus casei CRL705. Food Microbiol 21:291–298
Cotter PD, Hill C, Ross RP (2005) Bacteriocins: developing innate immunity for food. Nat Rev Microbiol 3:777–788
Daba H, Panadian S, Gosselin S, Simard JF, Huang R, Lacroix C (1991) Detection and activity of a bacteriocin produced by Leuconostoc mesenteroides. Appl Environ Microbiol 57:3450–3455
De Vuyst L, Vandamme EJ (1994) Bacteriocins of lactic acid bacteria, 1st edn. Blackie, London
Diep DB, Godager L, Brede D, Nes IF (1996) Data mining and characterization of a novel pediocin-like bacteriocin system from the genome of Pediococcus pentosaceus ATCC 25745. Microbiol-SGM 152:1649–1659
Favaro L, Penna ALB, Todorov SD (2015) Bacteriocinogenic LAB from cheeses—application in biopreservation? Trends Food Sci Technol 41:37–48
Felske A, Rheims H, Wokerink A, Stackebrandt E, Akkermans ADL (1997) Ribosome analysis reveals prominent activity of an uncultured member of the class Actinobacteria in grassland soils. Microbiology 143:2983–2989
Fimland G, Sletten K, Nissen-Meyer J (2002) The complete amino acid sequence of the pediocin-like antimicrobial peptide leucocin C. Biochem Biophys Res Commun 295:826–827
Fimland G, Nissen-Meyer J, Johnsen L (2005) 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 280(10):9243–9250. doi:10.1074/jbc.M412712200
Furtado DN, Todorov SD, Landgraf M, Destro MT, Franco BDGM (2014) Bacteriocinogenic Lactococcus lactis subsp lactis DF04Mi isolated from goat milk: characterization of the bacteriocin. Braz J Microbiol 45:1541–1550
Gonzales CF, Kunka BS (1987) Plasmid associated bacteriocin production and sucrose fermentation in Pediococcus acidilactici. Appl Environ Microbiol 53:2534–2538
Henderson JT, Chopko AL, Van Wassenaar PD (1992) Purification and primary structure of pediocin PA-1 produced by Pediococcus acidilactici PAC-10. Arch Biochem Biophys 295:5–12
Heng NCK, Wescombre PA, Burton JP, Jack RW, Tagg JR (2007) In: Riley MA, Chavan MA (eds) The diversity of bacteriocins in gram-positive bacteria bacteriocins: ecology and evolution. Springer, Berlin
Holo H, Jeknic Z, Daeschel M, Stevanovic S, Nes IF (2001) Plantaricin W from Lactobacillus plantarum belongs to a new family of two-peptide lantibiotics. Microbiology 147:643–651
Jack RW, Tagg JR, Ray B (1995) Bactericoins of gram-positive bacteria. Microbiol Rev 59:171–200
Kim WS, Hall RJ, Dunn NW (1997) The effect of nisin concentration and nutrient depletion on nisin production of Lactococcus lactis. Appl Microbiol Biotechnol 50:429–433
Knoetze H, Todorov SD, Dicks LMT (2008) A class IIa peptide from Enterococcus mundtii inhibits bacteria associated with otitis media. Int J Antimicrob Agents 31:228–234
Krier F, Revol-Junelles AM, Germain P (1998) Influence of temperature and pH on production of two bacteriocins by Leuconostoc mesenteroides subsp. mesenteroides FR52 during batch fermentation. Appl Microbiol Biotechnol 50:359–363
Kruger MF, Barbosa MDS, Miranda A, Landgraf M, Destro MT, Todorov SD, Franco BDGM (2013) Isolation of bacteriocinogenic strain of Lactococcus lactis subsp. lactis from rocket salad (Eruca sativa Mill.) and evidences of production of a variant of nisin with modification in the leader-peptide. Food Control 33:467–476
Maldonado A, Ruiz-Barba JL, Jiménez-Díaz R (2003) Purification and genetic characterization of plantaricin NC8, a novel coculture-inducible two-peptide bacteriocin from Lactobacillus plantarum NC8. Appl Environ Microbiol 69:383–389
Manca de Nadra MC, Sandino de Lamellas D, Strasser de Saad AM (1998) Pediocin N5p from Pediococcus pentosaceus, adsorption on bacterial strains. Int J Food Microbiol 39:79–85
Martinez RRC, Wachsman M, Torres NI, LeBlanc JG, Todorov SD, Franco BDGM (2013) Biochemical, antimicrobial and molecular characterization of a noncytotoxic bacteriocin produced by Lactobacillus plantarum ST71KS. Food Microbiol 34:376–381
Marugg JD, Gonzalez CF, Kunka BS, Ledeboer AM, Pucci MJ, Toonen MY, Walker SA, Zoetmudler LCM, Vandenbergh PA (1992) Cloning, expression, and nucleotide sequence of genes involved in the production of pediocin PA-1, a bacteriocin from Pediococcus acidilactici PAC1.0. Appl Environ Microbiol 58:2360–2367
Mataragas M, Drosinos EH, Metaxopoulos J (2003) Antagonistic activity of lactic acid bacteria against Listeria monocytogenes in sliced cooked cured pork shoulder stored under vacuum or modified atmosphere at 4 ± 2 °C. Food Microbiol 20:259–265
Motlagh A, Bukhtiyarova M, Ray B (1994) Complete nucleotide sequence of PSMB-74, a plasmid encoiding the production of pedicoin AcH in Pediococcus acidilactici. Lett Appl Microbiol 18:305–312
Perin LM, Nero LA (2014) Antagonistic lactic acid bacteria isolated from goat milk and identification of a novel nisin variant Lactococcus lactis. BMC Microbiol 14:36–45
Pieterse R, Todorov SD, Dicks LMT (2010) Mode of action and in vitro susceptibility of mastitis pathogens to macedocin ST91KM and preparation of a teat seal containing the bacteriocin. Braz J Microbiol 41:133–145
Powell JE, Witthuhn RC, Todorov SD, Dicks LMT (2007) Characterization of bacteriocin ST8KF produced by a kefir isolate Lactobacillus plantarum ST8KF. Int Dairy J 17:190–198
Schägger H, Van Jagow G (1987) Tricine-sodium dodecyl sulphate-polyacrylamide gel electrophoresis for the separation of protein in the range from 1 to 100 kDa. Anal Biochem 166:368–379
Schirru S, Todorov SD, Favaro L, Mangia NP, Basaglia M, Casella S, Comunian R, Franco BDGM, Deiana P (2012) Sardinian goat’s milk as source of bacteriocinogenic potential protective cultures. Food Control 25:309–320
Stephens SK, Floriano B, Cathcart DP, Bayley SA, Witt VF, Jiménez-Díaz R, Warner PJ, Ruiz-Barba JL (1998) Molecular analysis of the locus responsible for production of plantaricin S, a two-peptide bacteriocin produced by Lactobacillus plantarum LPCO10. Appl Environ Microbiol 64:1871–1877
Todorov SD (2008) Bacteriocin production by Lactobacillus plantarum AMA-K isolated from Amasi, a Zimbabwean fermented milk product and study of adsorption of bacteriocin AMA-K to Listeria spp. Braz J Microbiol 38:178–187
Todorov SD (2009) Bacteriocins from Lactobacillus plantarum—production, genetic organization and mode of action. A review. Braz J Microbiol 40:209–221
Todorov SD, Dicks LMT (2005) Characterization of bacteriocins produced by lactic acid bacteria isolated from spoiled black olives. J Basic Microbiol 45:312–322
Todorov SD, Dicks LMT (2006) Parameters affecting the adsorption of plantaricin 423, a bacteriocin produced by Lactobacillus plantarum 423 isolated from sorghum beer. Biotechnol J 1:405–409
Todorov SD, Dicks LMT (2009) Effect of modified MRS medium on production and purification of antimicrobial peptide ST4SA produced by Enterococcus mundtii. Anaerobe 15:65–73
Todorov SD, Franco BDGM (2010) Lactobacillus plantarum: characterization of the species and application in food production. A review. Food Rev Int 26:205–229
Todorov S, Onno B, Sorokine O, Chobert JM, Ivanova I, Dousset X (1999) Detection and characterization of a novel antibacterial substance produced by Lactobacillus plantarum ST31 isolated from sourdough. Int J Food Microbiol 48:167–177
Todorov S, Gotcheva B, Dousset X, Onno B, Ivanova I (2000) Influence of growth medium on bacteriocin production in Lactobacillus plantarum ST31. J Biotechnol Biotechnol Eq 14:50–55
Todorov SD, Danova ST, Van Reenen CA, Meincken M, Dinkova G, Ivanova IV, Dicks LMT (2006) Characterization of bacteriocin HV219, produced by Lactococcus lactis subsp. lactis HV219 isolated from human vaginal secretions. J Basic Microbiol 46:226–238
Todorov SD, Wachsman M, Tomé E, Dousset X, Destro MT, Dicks LMT, Franco BDGM, Vaz-Velho M, Drider D (2010) Characterisation of an antiviral pediocin-like bacteriocin produced by Enterococcus faecium. Food Microbiol 27:869–879
Todorov SD, Kruger MF, Martinez RCR, LeBlanc JG, Franco BDGM (2012) Targeting bacteriocin genes in lactic acid bacteria—what we need to know. In: Urbano KV (ed) Advances in genetics research, vol 7. Nova, New York, pp 61–92
Van Reenen CA, Dicks LMT, Chikindas ML (1998) Isolation, purification and partial characterization of plantaricin 423, a bacteriocin produced by Lactobacillus plantarum. J Appl Microbiol 84:1131–1137
Van Reenen CA, van Zyl WH, Chikindas ML, Dicks LMT (2003) Characterization and heterologous expression of a class IIa bacteriocin, plantaricin 423, in Saccharomyces cerevisiae. Int J Food Microbiol 81:29–40
Yang R, Johnson M, Ray B (1992) Novel method to extract large amounts of bacteriocins from lactic acid bacteria. Appl Environ Microbiol 58:3355–3359
Yildrim Z, Avşar YK, Yildrim M (2002) Factors affecting the adsorption of buchnericin LB, a bacteriocin produced by Lactobacillus buchneri. Microbiol Res 157:103–107
Acknowledgments
Dr. Todorov was supported by Fundação de Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG), Belo Horizonte and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brasilia, Brazil.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Todorov, S.D., Holzapfel, W. & Nero, L.A. Characterization of a novel bacteriocin produced by Lactobacillus plantarum ST8SH and some aspects of its mode of action. Ann Microbiol 66, 949–962 (2016). https://doi.org/10.1007/s13213-015-1180-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13213-015-1180-4