Skip to main content
SpringerLink
Log in

A novel enterocin T1 with anti-Pseudomonas activity produced by Enterococcus faecium T1 from Chinese Tibet cheese

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

An enterocin-producing Enterococcus faecium T1 was isolated from Chinese Tibet cheese. The enterocin was purified by SP-Sepharose and reversed phase HPLC. It was identified as unique from other reported bacteriocins based on molecular weight (4629 Da) and amino acid compositions; therefore it was subsequently named enterocin T1. Enterocin T1 was stable at 80–100 °C and over a wide pH range, pH 3.0–10.0. Protease sensitivity was observed to trypsin, pepsin, papain, proteinase K, and pronase E. Importantly, enterocin T1 was observed to inhibit the growth of numerous Gram-negative and Gram-positive bacteria including Pseudomonas putida, Pseudomonas aeruginosa, Pseudomonas fluorescens, Escherichia coli, Salmonella typhimurium, Shigella flexneri, Shigella sonnei, Staphylococcus aureus, Listeria monocytogenes. Take together, these results suggest that enterocin T1 is a novel bacteriocin with the potential to be used as a bio-preservative to control Pseudomonas spp. in food.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Achemchem F, Martínez-Bueno M, Abrini J, Valdivia E, Maqueda M (2005) Enterococcus faecium F58, a bacteriocinogenic strain naturally occurring in Jben, a soft, farmhouse goat’s cheese made in Morocco. J Appl Microbiol 99:141–150

    Article  CAS  Google Scholar 

  • Alvarado C, Garcia-Almendarez B, Martin S, Regalado C (2005) Anti-Listeria monocytogenes bacteriocin-like inhibitory substances from Enterococcus faecium UQ31 isolated from artisan Mexican-style cheese. Curr Microbiol 51:110–115

    Article  CAS  Google Scholar 

  • Aymerich T, Holo H, Håvarstein LS, Hugas M, Garriga M, Nes IF (1996) Biochemical and genetic characterization of enterocin A from Enterococcus faecium, a new antilisterial bacteriocin in the pediocin family of bacteriocins. Appl Environ Microbiol 62:1676–1682

    CAS  Google Scholar 

  • Batdorj B et al (2006) Purification and characterization of two bacteriocins produced by lactic acid bacteria isolated from Mongolian airag. J Appl Microbiol 101:837–848

    Article  CAS  Google Scholar 

  • Chatterjee C, Paul M, Xie LL, van der Donk WA (2005) Biosynthesis and mode of action of lantibiotics. Chem Rev 105:633–683

    Article  CAS  Google Scholar 

  • Cintas LM, Casaus P, Håvarstein LS, Hernandez PE, Nes IF (1997) Biochemical and genetic characterization of enterocin P, a novel sec-dependent bacteriocin from Enterococcus faecium P13 with a broad antimicrobial spectrum. Appl Environ Microbiol 63:4321–4330

    CAS  Google Scholar 

  • Cintas LM, Casaus P, Herranz C, Håvarstein LS, Holo H, Hernández PE, Nes IF (2000) Biochemical and genetic evidence that Enterococcus faecium L50 produces enterocins L50A and L50B, thesec-dependent enterocin P, and a novel bacteriocin secreted without an N-terminal extension termed enterocin Q. J Bacteriol 182:6806–6814

    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 

  • Craven H, Macauley B (1992) Microorganisms in pasteurised milk after refrigerated storage. 1. Identification of types. Aust J Dairy Technol 47:38–45

    Google Scholar 

  • Drider D, Rebuffat S (2011) Prokaryotic antimicrobial peptides: from genes to applications. Springer Science & Business Media, Berlin

    Book  Google Scholar 

  • Drider D, Fimland G, Héchard Y, McMullen LM, Prévost H (2006) The continuing story of class IIa bacteriocins. Microbiol Mol Biol Rev 70:564–582

    Article  CAS  Google Scholar 

  • Eneroth Å, Ahrné S, Molin G (2000) Contamination of milk with Gram-negative spoilage bacteria during filling of retail containers. Int J Food Microbiol 57:99–106

    Article  Google Scholar 

  • Ennahar S, Deschamps N (2000) Anti-Listeria effect of enterocin A, produced by cheese-isolated Enterococcus faecium EFM01, relative to other bacteriocins from lactic acid bacteria. J Appl Microbiol 88:449–457

    Article  CAS  Google Scholar 

  • Farias ME, De Ruiz H, Aida A, Sesma F (1994) Bacteriocin production by lactic acid bacteria isolated from regional cheeses: inhibition of foodborne pathogens. J Food Prot® 57:1013–1015

    CAS  Google Scholar 

  • Foulquié Moreno M, Sarantinopoulos P, Tsakalidou E, De Vuyst L (2006) The role and application of enterococci in food and health. Int J Food Microbiol 106:1–24

    Article  Google Scholar 

  • Franz C, Schillinger U, Holzapfel W (1996) Production and characterization of enterocin 900, a bacteriocin produced by Enterococcus faecium BFE 900 from black olives. Int J Food Microbiol 29:255–270

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gálvez A, Abriouel H, López RL, Omar NB (2007) Bacteriocin-based strategies for food biopreservation. Int J Food Microbiol 120:51–70

    Article  Google Scholar 

  • Garcia M, Sanz B, Garcia-Collia P, Ordonez J (1989) Activity and thermostability of the extracellular lipases and proteinases from pseudomonads isolated from raw milk. Milchwissenschaft 44:547–550

    CAS  Google Scholar 

  • Ghrairi T, Frere J, Berjeaud J, Manai M (2008) Purification and characterisation of bacteriocins produced by Enterococcus faecium from Tunisian rigouta cheese. Food Control 19:162–169

    Article  CAS  Google Scholar 

  • Heng NC, Tagg JR (2006) What’s in a name?. Class distinction for bacteriocins, Nat Rev Microbiol 4

    Google Scholar 

  • Herranz C et al (1999) Biochemical and genetic evidence of enterocin P production by two Enterococcus faecium-like strains isolated from fermented sausages. Curr Microbiol 39:282–290

    Article  CAS  Google Scholar 

  • Hickey RM, Twomey DP, Ross RP, Hill C (2003) Production of enterolysin A by a raw milk enterococcal isolate exhibiting multiple virulence factors. Microbiol 149:655–664

    Article  CAS  Google Scholar 

  • Jang S, Lee J, Jung U, Choi HS, Suh HJ (2014) Identification of an anti-listerial domain from Pediococcus pentosaceus T1 derived from Kimchi, a traditional fermented vegetable. Food Control 43:42–48

    Article  CAS  Google Scholar 

  • Kang J, Lee M (2005) Characterization of a bacteriocin produced by Enterococcus faecium GM-1 isolated from an infant. J Appl Microbiol 98:1169–1176

    Article  CAS  Google Scholar 

  • Kaur G et al (2011) Nisin and class IIa bacteriocin resistance among Listeria and other foodborne pathogens and spoilage bacteria. Microb Drug Resist 17:197–205

    Article  Google Scholar 

  • Khalil R, Elbahloul Y, Djadouni F, Omar S (2009) Isolation and partial characterization of a bacteriocin produced by a newly isolated Bacillus megaterium 19 strain. Pak J Nutr 8:242–250

    Article  CAS  Google Scholar 

  • Khay EO, Idaomar M, Castro L, Bernárdez P, Senhaji N, Abrini J (2013) Antimicrobial activities of the bacteriocin-like substances produced by lactic acid bacteria isolated from Moroccan dromedary milk. Afr J Biotechnol 10:10447–10455

    Google Scholar 

  • Klaenhammer TR (1993) Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol Rev 12:39–85

    Article  CAS  Google Scholar 

  • Klein G, Rüben C, Upmann M (2013) Antimicrobial activity of essential oil components against potential food spoilage microorganisms. Curr Microbiol 67:200–208

    Article  CAS  Google Scholar 

  • Liu X et al (2011) Identification of an N-terminal formylated, two-peptide bacteriocin from Enterococcus faecalis 710C. J Agric Food Chem 59:5602–5608

    Article  CAS  Google Scholar 

  • Losteinkit C, Uchiyama K, Ochi S, Takaoka T, Nagahisa K, Shioya S (2001) Characterization of bacteriocin N15 produced by Enterococcus faecium N15 and cloning of the related genes. J Biosci Bioeng 91:390–395

    Article  CAS  Google Scholar 

  • Lü X, Yi L, Dang J, Dang Y, Liu B (2014) Purification of novel bacteriocin produced by Lactobacillus coryniformis MXJ 32 for inhibiting bacterial foodborne pathogens including antibiotic-resistant microorganisms. Food Control 46:264–271

    Article  Google Scholar 

  • Maqueda M, Sánchez-Hidalgo M, Fernández M, Montalbán-López M, Valdivia E, Martínez-Bueno M (2008) Genetic features of circular bacteriocins produced by Gram-positive bacteria. FEMS Microbiol Rev 32:2–22

    Article  CAS  Google Scholar 

  • Messaoudi S et al (2012) Purification and characterization of a new bacteriocin active against Campylobacter produced by Lactobacillus salivarius SMXD51. Food Microbiol 32:129–134

    Article  CAS  Google Scholar 

  • Moreno M et al (2002) Microbial analysis of Malaysian tempeh, and characterization of two bacteriocins produced by isolates of Enterococcus faecium. J Appl Microbiol 92:147–157

    Article  CAS  Google Scholar 

  • Nes IF, Diep DB, Håvarstein LS, Brurberg MB, Eijsink V, Holo H (1996) Biosynthesis of bacteriocins in lactic acid bacteria. Antonie Van Leeuwenhoek 70:113–128

    Article  CAS  Google Scholar 

  • Nes IF, Diep DB, Holo H (2007) Bacteriocin diversity in Streptococcus and Enterococcus. J Bacteriol 189:1189–1198

    Article  CAS  Google Scholar 

  • Nes IF, Diep DB, Ike Y (2014) Enterococcal bacteriocins and antimicrobial proteins that contribute to niche control. In: Gilmore MS, Clewell DB, Ike Y, Shankar N (eds) Enterococci: from commensals to leading causes of drug resistant infection. Massachusetts Eye and Ear Infirmary, Boston

  • Nissen-Meyer J, Oppegård C, Rogne P, Haugen HS, Kristiansen PE (2010) Structure and mode-of-action of the two-peptide (Class-IIb) bacteriocins. Probiot Antimicrob Proteins 2:52–60

    Article  CAS  Google Scholar 

  • Pringsulaka O, Thongngam N, Suwannasai N, Atthakor W, Pothivejkul K, Rangsiruji A (2012) Partial characterisation of bacteriocins produced by lactic acid bacteria isolated from Thai fermented meat and fish products. Food Control 23:547–551

    Article  CAS  Google Scholar 

  • Saavedra L, Sesma F (2011) Purification techniques of bacteriocins from lactic acid bacteria and other Gram-positive bacteria. In: Prokaryotic antimicrobial peptides. Springer, Berlin, pp 99–113

  • Samelis J, Roller S, Metaxopoulos J (1994) Sakacin B, a bacteriocin produced by Lactobacillus sake isolated from Greek dry fermented sausages. J Appl Bacteriol 76:475–486

    Article  CAS  Google Scholar 

  • Snyder AB, Worobo RW (2014) Chemical and genetic characterization of bacteriocins: antimicrobial peptides for food safety. J Sci Food Agric 94:28–44

    Article  CAS  Google Scholar 

  • Sperber WH, Doyle MP (2009) Compendium of the microbiological spoilage of food and beverages. Springer, Berlin

    Book  Google Scholar 

  • Svetoch EA et al (2008) Diverse antimicrobial killing by Enterococcus faecium E 50–52 bacteriocin. J Agric Food Chem 56:1942–1948

    Article  CAS  Google Scholar 

  • Svetoch EA, Eruslanov BV, Perelygin VV, Levchuk VP, Seal BS, Stern NJ (2010) Inducer bacteria, unique signal peptides, and low-nutrient media stimulate in vitro bacteriocin production by Lactobacillus spp. and Enterococcus spp. strains. J Agric Food Chem 58:6033–6038

    Article  CAS  Google Scholar 

  • Tiwari BK, Valdramidis VP, O’Donnell CP, Muthukumarappan K, Bourke P, Cullen P (2009) Application of natural antimicrobials for food preservation. J Agric Food Chem 57:5987–6000

    Article  CAS  Google Scholar 

  • Todokoro D, Tomita H, Inoue T, Ike Y (2006) Genetic analysis of bacteriocin 43 of vancomycin-resistant Enterococcus faecium. Appl Environ Microbiol 72:6955–6964

    Article  CAS  Google Scholar 

  • Todorov SD et al (2010) Characterisation of an antiviral pediocin-like bacteriocin produced by Enterococcus faecium. Food Microbiol 27:869–879

    Article  CAS  Google Scholar 

  • Vithanage NR, Yeager TR, Jadhav SR, Palombo EA, Datta N (2014) Comparison of identification systems for psychrotrophic bacteria isolated from raw bovine milk. Int J Food Microbiol 189:26–38

    Article  CAS  Google Scholar 

  • Yang R, Johnson MC, Ray B (1992) Novel method to extract large amounts of bacteriocins from lactic acid bacteria. Appl Environ Microbiol 58:3355–3359

    CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the Research Fund for the Doctoral Program of Higher Education of China (No. 20112302110051), National Science Foundation, China (Nos. 31271906/C2002204, 31571850/C200502).

Author information

Authors and Affiliations

  1. School of Chemical Engineering and Technology, Harbin Institute of Technology, Harbin, 150090, Heilongjiang, China

    Hui Liu, Lanwei Zhang, Huaxi Yi, Xue Han, Wei Gao, Chunliang Chi & Wei Song

  2. College of Life Sciences, Heilongjiang University, Harbin, 150070, Heilongjiang, China

    Haiying Li & Chunguang Liu

Authors
  1. Hui Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lanwei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Huaxi Yi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xue Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wei Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chunliang Chi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Wei Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Haiying Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Chunguang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Lanwei Zhang or Huaxi Yi.

Ethics declarations

Conflict of interest

No conflict of interest is declared.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, H., Zhang, L., Yi, H. et al. A novel enterocin T1 with anti-Pseudomonas activity produced by Enterococcus faecium T1 from Chinese Tibet cheese. World J Microbiol Biotechnol 32, 21 (2016). https://doi.org/10.1007/s11274-015-1973-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-015-1973-4

Keywords

Search

Navigation