Skip to main content
Log in

Safety and biotechnological properties of Enterococcus faecalis and Enterococcus faecium isolates from Meju

  • Article
  • Published:
Journal of the Korean Society for Applied Biological Chemistry Submit manuscript

Abstract

We assessed the safety and biotechnological properties of 17 Enterococcus faecalis and 18 Enterococcus faecium strains isolated from Meju to select starter candidates for quality Meju production. Minimum inhibitory concentration assays showed that all strains were susceptible to ampicillin, chloramphenicol, ciprofloxacin, erythromycin, gentamicin, penicillin G, and tetracycline, as judged by the breakpoint values defined at the species level by the European Committee on Antimicrobial Susceptibility Testing, whereas two E. faecalis strains were resistant to vancomycin, which could be ascribed to acquired resistance. None of the strains exhibited α- or β-hemolytic activities or biofilm formation. Both species showed similar levels of biogenic amine production, and noticeable amounts of tyramine (3397.4 ± 172.4 ppm) were produced by all strains in the presence of precursors (histidine, lysine, ornithine, and tyrosine). All strains exhibited protease, lipase, and acid production, with decreased activity observed with increasing NaCl concentrations. This study confirmed the necessity of antibiotic resistance screening of Enterococcus species for food production, with the identification of vancomycin-resistant strains from Meju.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Adams MR (1999) Safety of industrial lactic acid bacteria. J Biotechnol 68:171–178

    Article  CAS  Google Scholar 

  • Aguirre M, Collins MD (1993) Lactic acid bacteria and human clinical infection. J Appl Bacteriol 75:95–107

    Article  CAS  Google Scholar 

  • Bhardwaj A, Malik RK, Chauhan P (2008) Functional and safety aspects of enterococci in dairy foods. Indian J Microbiol 48:317–325

    Article  Google Scholar 

  • Bover-Cid S, Holzapfel WH (1999) Improved screening procedure for biogenic amine production by lactic acid bacteria. Int J Food Microbiol 53:33–41

    Article  CAS  Google Scholar 

  • Carelli D, Centonze D, Palermo C, Quinto M, Rotunno T (2007) An interference free amperometric biosensor for the detection of biogenic amines in food products. Biosens Bioelectron 23:640–647

    Article  CAS  Google Scholar 

  • Cho TY, Han G-H, Bahn KN, Son Y-W, Jang M-R, Lee C-H, Kim S-H, Kim D-B, Kim S-B (2006) Evaluation of biogenic amines in Korean commercial fermented foods. Korean J Food Sci Biotechnol 38:730–737

    Google Scholar 

  • CLSI (2007) Performance standards for antimicrobial susceptibility testing; seventeenth informational supplement. CLSI document M100-S17. Clinical and Laboratory Standards Institute, Wayne

    Google Scholar 

  • de Las Rivas B, Marcobal A, Munoz R (2005) Improved multiplex-PCR method for the simultaneous detection of food bacteria producing biogenic amines. FEMS Microbiol Lett 244:367–372

    Article  Google Scholar 

  • Domann E, Hain T, Ghai R, Billion A, Kuenne C, Zimmermann K, Chakraborty T (2007) Comparative genomic analysis for the presence of potential enterococcal virulence factors in the probiotic Enterococcus faecalis strain Symbioflor 1. Int J Med Microbiol 297:533–539

    Article  CAS  Google Scholar 

  • Endtz HP, van den Braak N, Verbrugh HA, van Belkum A (1999) Vancomycin resistance: status quo and quo vadis. Eur J Clin Microbiol Infect Dis 18:683–690

    Article  CAS  Google Scholar 

  • Fifadara N, Radu S, Hassan Z, Beuchat LR, Rusul G (2003) Hemolytic and nonhemolytic vancomycin-resistant Enterococcus faecalis isolated from beef imported to Malaysia. J Food Prot 66:1845–1850

    CAS  Google Scholar 

  • Franz CM, Holzapfel WH, Stiles ME (1999) Enterococci at the crossroads of food safety? Int J Food Microbiol 47:1–24

    Article  CAS  Google Scholar 

  • Franz CM, Huch M, Abriouel H, Holzapfel W, Galvez A (2011) Enterococci as probiotics and their implications in food safety. Int J Food Microbiol 151:125–140

    Article  CAS  Google Scholar 

  • Gardiner GE, Ross RP, Wallace JM, Scanlan FP, Jagers PP, Fitzgerald GF, Collins JK, Stanton C (1999) Influence of a probiotic adjunct culture of Enterococcus faecium on the quality of cheddar cheese. J Agric Food Chem 47:4907–4916

    Article  CAS  Google Scholar 

  • Halasz A, Barath A, Sarkadi LS, Holzapfel W (1994) Biogenic amines and their production by microorganisms in food. Trends Food Sci Tech 5:42–49

    Article  CAS  Google Scholar 

  • Heilmann C, Schweitzer O, Gerke C, Vanittanakom N, Mack D, Gotz F (1996) Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol 20:1083–1091

    Article  CAS  Google Scholar 

  • Hidron AI, Edwards JR, Patel J, Horan TC, Sievert DM, Pollock DA, Fridkin SK, National Healthcare Safety Network T, Participating National Healthcare Safety Network F (2008) NHSN annual update: antimicrobial-resistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006–2007. Infect Control Hosp Epidemiol 29:996–1011

    Article  Google Scholar 

  • Hwang DF, Chang SH, Shiua CY, Chai T (1997) High-performance liquid chromatographic determination of biogenic amines in fish implicated in food poisoning. J Chromatogr B Biomed Sci Appl 693:23–29

    Article  CAS  Google Scholar 

  • Jeong DW, Cho H, Lee H, Li C, Garza J, Fried M, Bae T (2011) Identification of the P3 promoter and distinct roles of the two promoters of the SaeRS two-component system in Staphylococcus aureus. J Bacteriol 193:4672–4684

    Article  CAS  Google Scholar 

  • Jeong DW, Kim HR, Han S, Jeong CO, Lee JH (2013) A proposal to unify two subspecies of Staphylococcus equorum: Staphylococcus equorum subsp. equorum and Staphylococcus equorum subsp. linens. Antonie van Leeuwenhoek 104:1049–1062

    Article  CAS  Google Scholar 

  • Jeong DW, Han S, Lee JH (2014a) Safety and technological characterization of Staphylococcus equorum isolates from jeotgal, a Korean high-salt-fermented seafood, for starter development. Int J Food Microbiol 188:108–115

    Article  CAS  Google Scholar 

  • Jeong DW, Kim HR, Jung G, Han S, Kim CT, Lee JH (2014b) Bacterial community migration in the ripening of doenjang, a traditional Korean fermented soybean food. J Microbiol Biotechnol 24:648–660

    Article  CAS  Google Scholar 

  • Jung JY, Lee SH, Jeon CO (2014) Microbial community dynamics during fermentation of doenjang-meju, traditional Korean fermented soybean. Int J Food Microbiol 185:112–120

    Article  CAS  Google Scholar 

  • Kim D-Y, Kwon D-J (2014) Quality characteristics of Doenjang manufactured with soybean Koji. Korean J Food Preserv 21:434–441

    Article  Google Scholar 

  • Kim J-H, Ahn H-J, Yook H-S, Park HJ, Byun M-W (2001) Biogenic amines contents in commercial Korean traditional fremented soybean paste. Korean J Food Sci Biotechnol 33:682–685

    Google Scholar 

  • Kim JH, Yoo JS, Lee CH, Kim SY, Lee SK (2006) Quality properties of soybean pastes made from meju with mold producing protease isolated from traditional meju. J Korean Soc Appl Biol Chem 49:7–14

    CAS  Google Scholar 

  • Kim D-Y, Park G-Y, Jang S-W, Hong S-C, Kown D-J (2013) Establishment of optimal soybean Koji manufacturing conditions. Korean J Food Preserv 20:379–385

    Article  Google Scholar 

  • Lina G, Quaglia A, Reverdy ME, Leclercq R, Vandenesch F, Etienne J (1999) Distribution of genes encoding resistance to macrolides, lincosamides, and streptogramins among staphylococci. Antimicrob Agents Chemother 43:1062–1066

    CAS  Google Scholar 

  • Martin B, Garriga M, Hugas M, Aymerich T (2005) Genetic diversity and safety aspects of enterococci from slightly fermented sausages. J Appl Microbiol 98:1177–1190

    Article  CAS  Google Scholar 

  • Nam YD, Lee SY, Lim SI (2012) Microbial community analysis of Korean soybean pastes by next-generation sequencing. Int J Food Microbiol 155:36–42

    Article  Google Scholar 

  • Patel G, Snydman DR, AST Infectious Diseases Community of Practice (2013) Vancomycin-resistant Enterococcus infections in solid organ transplantation. Am J Transpl 4:59–67

    Article  Google Scholar 

  • Perez-Pulido R, Abriouel H, Ben Omar N, Lucas R, Martinez-Canamero M, Galvez A (2006) Safety and potential risks of enterococci isolated from traditional fermented capers. Food Chem Toxicol 44:2070–2077

    Article  CAS  Google Scholar 

  • Perin LM, Miranda RO, Todorov SD, de Melo Franco BDG, Nero LA (2014) Virulence, antibiotic resistance and biogenic amines of bacteriocinogenic lactococci and enterococci isolated from goat milk. Int J Food Microbiol 185:121–126

    Article  CAS  Google Scholar 

  • Pinheiro ET, Gomes BPFA, Drucker DB, Zaia AA, Ferraz CCR, Souza-Filho FJ (2004) Antimicrobial susceptibility of Enterococcus faecalis isolated from canals of root filled teeth with periapical lesions. Int Endod J 37:756–763

    Article  CAS  Google Scholar 

  • Santos MM, Piccirillo C, Castro PM, Kalogerakis N, Pintado ME (2012) Bioconversion of oleuropein to hydroxytyrosol by lactic acid bacteria. World J Microbiol Biotechnol 28:2435–2440

    Article  CAS  Google Scholar 

  • Shalaby AR (1996) Significance of biogenic amines to food safety and human health. Food Res Int 29:675–690

    Article  CAS  Google Scholar 

  • Shukla S, Park HK, Kim JK, Kim M (2010) Determination of biogenic amines in Korean traditional fermented soybean paste (Doenjang). Food Chem Toxicol 48:1191–1195

    Article  CAS  Google Scholar 

  • Sila Santos MH (1996) Biogenic amines: their importance in foods. Int J Food Microbiol 29:213–231

    Article  Google Scholar 

  • Zheng B, Tomita H, Inoue T, Ike Y (2009) Isolation of VanB-type Enterococcus faecalis strains from nosocomial infections: first report of the isolation and identification of the pheromone-responsive plasmids pMG2200, Encoding VanB-type vancomycin resistance and a Bac41-type bacteriocin, and pMG2201, encoding erythromycin resistance and cytolysin (Hly/Bac). Antimicrob Agents Chemother 53:735–747

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2014R1A1A2057003).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jong-Hoon Lee.

Additional information

Miran Jeong and Do-Won Jeong have contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jeong, M., Jeong, DW. & Lee, JH. Safety and biotechnological properties of Enterococcus faecalis and Enterococcus faecium isolates from Meju . J Korean Soc Appl Biol Chem 58, 813–820 (2015). https://doi.org/10.1007/s13765-015-0110-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13765-015-0110-2

Keywords

Navigation