Advertisement

European Food Research and Technology

, Volume 245, Issue 3, pp 569–579 | Cite as

Differences in the occurence and efficiency of antimicrobial compounds produced by lactic acid bacteria

  • Joana Salomskiene
  • Dovile JonkuvieneEmail author
  • Irena Macioniene
  • Asta Abraitiene
  • Jurate Zeime
  • Jurate Repeckiene
  • Lina Vaiciulyte-Funk
Original paper
  • 161 Downloads

Abstract

To provide consumers with new, attractive, and healthy food products, chemical additives could be replaced by lactic acid bacteria (LAB). Twelve highly antagonistic LAB strains were screened to find the best manufacturers of antimicrobial agents and key components that ensure greater effectiveness of their antagonistic activity. The tested LAB strains appeared to produce and excrete natural antimicrobial compounds such as ethanol (0.27–0.87%), lactic (5.6–19.9 g/L), citric (0.3–3.3 g/L), benzoic (0.2–1.8 mg/L), and sorbic (0.1–1.2 mg/L) acids. The individual LAB strain showed strain-specific abilities to produce individual compounds: citric acid was observed for Streptococcus thermophilus 43, sorbic acid for Lactococcus lactis 140/2, and diacetyl for other L. lactis strains. Lactobacillus helveticus R reached the highest antimicrobial activity by the production of the largest amount of lactic acid, while L. lactis 140/2 achieved that by the complex of produced organic acids. Enterococcus faecium 41-2B was mostly effective protein producing strain (1.2 g/100 g); moreover, enterocins A and P coding genes with antimicrobial activity against Listeriamonocytogenes were found in these Enterococcus strains. Five LAB strains were characterized by containing 1–2 plasmids. The study demonstrated a delicate balance of natural antimicrobial synthesis; meanwhile, the insertion of some preservatives in the medium could not significantly decrease their antagonistic activity.

Keywords

Lactic acid bacteria Antimicrobial compounds Antilisterial activity Plasmid DNA 

Notes

Compliance with ethical standards

Conflict of interest

J. Salomskiene, D. Jonkuviene, I. Macioniene, A. Abraitiene, J. Zeime, J. Repeckiene and L. Vaiciulyte-Funk state that there are no conflicts of interest.

Compliance with ethics requirements

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and /or national research committee.

References

  1. 1.
    Yépez A, Luz C, Meca G, Vignolo G, Manes J, Aznar R (2017) Biopreservation potential of lactic acid bacteria from Andean fermented food of vegetal origin. Food Control 78:61–64CrossRefGoogle Scholar
  2. 2.
    Barnby-Smith FM (1992) Bacteriocins: applications in food preservation. Trends Food Sci Technol 3:133–137CrossRefGoogle Scholar
  3. 3.
    Varsha KK, Nampoothiri KM (2016) Appraisal of lactic acid bacteria as protective cultures. Food Control 69:61–64CrossRefGoogle Scholar
  4. 4.
    Rattanachaikunsopon P, Phumkhachorn P (2010) Lactic acid bacteria: their antimicrobial compounds and their uses in food production. Ann Biol Res 1:218–228Google Scholar
  5. 5.
    Ikeda DM, Weinert E, Chang KCS, McGinn JM, Miller SA, Keliihoomalu Ch, DuPonte MW (2013) Natural farming: lactic acid bacteria. J Sustain Agric SA 8:1–4Google Scholar
  6. 6.
    Blagojev N, Škrinjar M, Veskovic-Moračanin S, Šošo V (2012) Control of mould growth and mycotoxin production by lactic acid bacteria metabolites. Rom Biotech Lett 17:7219–7226Google Scholar
  7. 7.
    Šušković J, Kos B, Beganović J, Leboš Pavunc A, Habjanič K, Matošić S (2010) Antimicrobial activity—the most important property of probiotic and starter lactic acid bacteria. Food Technol Biotech 48:296–307Google Scholar
  8. 8.
    Ulpathakumbura CP, Ranadheera CS, Senavirathne ND, Jayawardene LPINP, Prasanna HP, Vidanarachchi JK (2016) Effect of biopreservatives on microbial, physico-chemical and sensory properties of Cheddar cheese. Food Biosci 13:21–25CrossRefGoogle Scholar
  9. 9.
    Di Gioia D, Mazzola G, Nikodinoska I, Aloisio I, Landerholc T, Rossi M, Raimondi S, Melero B, Rovira J (2016) Lactic acid bacteria as protective cultures in fermented pork meat to prevent Clostridium spp. growth. Int J Food Microbiol 235:53–59CrossRefGoogle Scholar
  10. 10.
    O’Bryan CA, Crandall PG, Ricke SC, Ndahetuye JB (2015) Lactic acid bacteria (LAB) as antimicrobials in food products: types and mechanisms of action. Handb Nat Antimicrob Food Saf Qual 6:117–136CrossRefGoogle Scholar
  11. 11.
    Magnusson J, Schnürer J (2001) Lactobacillus coryniformis subsp. coryniformis strain Si3 produces a broad-spectrum proteinaceous antifungal compound. J Appl Microbiol 67:1–5CrossRefGoogle Scholar
  12. 12.
    Niku-Paavola M-L, Laitila A, Mattila-Sandholm T, Haikara A (1999) New types of antimicrobial compounds produced by Lactobacillus plantarum. J Appl Microbiol 86:29–35CrossRefGoogle Scholar
  13. 13.
    Hawkins S (2014) Antimicrobial activity of cinnamic acid, citric acid, cinnamaldehyde, and levulinic acid against foodborne pathogens. Savannah Hawkins Senior Honors Thesis. http://trace.tennessee.edu/cgi/viewcontent.cgi?article=2750&context=utk_chanhonoproj. Accessed 26 Jan 15
  14. 14.
    Bizri J, Wahem I (2006) Citric Acid and antimicrobial affect microbiological stability and quality of tomato juice. J Food Sci 59:130–135CrossRefGoogle Scholar
  15. 15.
    Šalomskienė J, Abraitienė A, Jonkuvienė D, Mačionienė I, Repečkienė J (2015) Selection of enhanced antimicrobial activity posing lactic acid bacteria characterised by (CGT)5-PCR fingerprinting. J Food Sci Technol 52:4124–4134CrossRefGoogle Scholar
  16. 16.
    Šalomskienė J, Abraitienė A, Jonkuvienė D, Mačionienė I, Repečkienė J, Stankienė J, Vaičiulytė-Funk L (2015) Changes in antagonistic activity of lactic acid bacteria induced by their response to technological factors. J Sci Food Agric 24:289–299Google Scholar
  17. 17.
    AOAC (1990) Official method of analysis, 15th edn. Association of Official Analytical Chemists, WashingtonGoogle Scholar
  18. 18.
    Moreno M, Leisner J, Tee L, Ley C, Radu S, Rusul G, Vuyst LD (2002) Microbial analysis of Malaysian tempeh, and characterization of two bacteriocins produced by isolates of Enterococcus faecium. J Appl Microbiol 92:147–157CrossRefGoogle Scholar
  19. 19.
    O’Sullivan DJ, Klaenhammer TR (1993) Rapid Mini-Prep isolation of high-quality plasmid DNA from Lactococcus and Lactobacillus spp. Appl Environ Microbiol 59:2730–2733Google Scholar
  20. 20.
    Caplice E, Fitzgerald GF (1999) Food fermentations: role of microorganisms in food production and preservation. Int J Food Microbiol 50:131–149CrossRefGoogle Scholar
  21. 21.
    Ross RP, Morgan S, Hill C (2002) Preservation and fermentation: past, present and future. Int J Food Microbiol 79:3–16CrossRefGoogle Scholar
  22. 22.
    Janssen M, Geeraerd AH, Cappuyns A, Garcia-Gonzalez L, Schockaert G, Van Houteghem N, Vereecken KM, Debevere J, Devlieghere F, Van Impe JF (2007) Individual and combined effects of pH and lactic acid concentration on Listeria innocua inactivation: development of a predictive model and assessment of experimental variability. Appl Environ Microbiol 73:1601–1611CrossRefGoogle Scholar
  23. 23.
    Kockova M, Gerekova P, Petrulakova Z, Hybenova E, Šturdik E, Valik L (2011) Evaluation of fermentation properties of lactic acid bacteria isolated from sourdough. Acta Chim Slov 4:78–87Google Scholar
  24. 24.
    Belgacem BZ, Rehaiem A, Fajardo Bernárdez P, Manai M, Pastrana Castro L (2012) Interactive effects of pH and temperature on the bacteriocin stability by response surface analysis. Microbiology 81:195–199CrossRefGoogle Scholar
  25. 25.
    Joshi V, Sharma S, Ran SN (2006) Production, purification, stability and efficacy of bacteriocin from isolates of natural lactic acid fermentation of vegetables. Food Technol Biotechnol 44:435–439Google Scholar
  26. 26.
    Aslam M, Shahid M, Rehman FU, Naveed NH, Batool A, Sharif S, Asia A (2011) Purification and characterization of bacteriocin isolated from Streptococcus thermophilus. Afr J Microbiol Res 5:2642–2648CrossRefGoogle Scholar
  27. 27.
    Poeta P, Costa D, Rojo-Bezares B, Zarazaga M, Klibi N, Rodrigues J, Torres C (2007) Detection of antimicrobial animals. Microbiol Res 162:257–263CrossRefGoogle Scholar
  28. 28.
    Moraes PM, Perin LM, Ortolani MB, Yamazi AK, Viçosa GN, Nero LA (2010) Protocols for the isolation and detection of lactic acid bacteria with bacteriocinogenic potential. LWT-Food Sci Technol 43:1320–1324CrossRefGoogle Scholar
  29. 29.
    Escamilla-Martínez EE, Cisneros YM, Fernández FJ, Quirasco-Baruch M, Ponce-Alquicira E (2017) Identification of structural and immunity genes of a lass IIb bacteriocin encoded in the enterocin A operon of Enterococcus faecium strain MXVK29. J Food Prot 80:1851–1856CrossRefGoogle Scholar
  30. 30.
    Smetankova J, Hladikova Z, Valach F, Zimanova M, Kohajdova Z, Greif G, Greifova M (2012) Influence of aerobic and anaerobic conditions on the growth and metabolism of selected strains of Lactobacillus plantarum. Acta Chim Slov 5:204–210CrossRefGoogle Scholar
  31. 31.
    Jonkuvienė D, Vaičiulytė-Funk L, Šalomskienė J, Alenčikienė G, Mieželienė A (2016) Potential of Lactobacillus reuteri from spontaneous sourdough as a starter additive for improving quality parameters of bread. Food Technol Biotechnol 54:342–350Google Scholar
  32. 32.
    Dalié DKD, Deschamps AM, Richard-Forget F (2010) Lactic acid bacteria—potential for control of mould growth and mycotoxins: a review. Food Control 21:370–380CrossRefGoogle Scholar
  33. 33.
    Mobolaji OA, Wuraola FO (2011) Assessment of the antimicrobial activity of lactic acid bacteria isolated from two fermented maize products—ogi and kunnu-zaki. Malays J Microbiol 7:124–128Google Scholar
  34. 34.
    Castellano P, Ibarreche MP, Massani MB, Fontana C, Vignolo GM (2017) Strategies for pathogen biocontrol using lactic acid bacteria and their metabolites: a focus on meat ecosystems and industrial environments. Microorganisms 5:1–25CrossRefGoogle Scholar
  35. 35.
    Gálvez A, Abriouel H, López RL, Omar BN (2007) Bacteriocin-based strategies for food biopreservation. Int J Food Microbiol 120:51–70CrossRefGoogle Scholar
  36. 36.
    Kluge H, Broz J, Eder K (2006) Effect of benzoic acid on growth performance, nutrient digestibility, nitrogen balance, gastrointestinal microflora and parameters of microbial metabolism in piglets. J Anim Physiol Anim Nutr 90:316–324CrossRefGoogle Scholar
  37. 37.
    Liewen MB, Marth EH (1985) Growth and inhibition of microorganisms in the presence of sorbic acid: a review. J Food Prot 48:364–375CrossRefGoogle Scholar
  38. 38.
    Mills S, McAuliffe OE, Coffey A, Fitzgerald GF, Ross RP (2006) Plasmids of lactococci genetic accessories or genetic necessities. FEMS Microbiol Lett 30:243–273CrossRefGoogle Scholar
  39. 39.
    Lönner C, Preve-Åkesson K, Ahrné S (1990) Plasmid contents of lactic acid bacteria isolated from different types of sour dough. Curr Microbiol 20:201–207CrossRefGoogle Scholar
  40. 40.
    Rosvoll TC, Pedersen T, Sletvold H, Johnsen PJ, Sollid JE, Simonsen GS, Jensen LB, Nielsen KM, Sundsfjord A (2010) PCR-based plasmid typing in Enterococcus faecium strains reveals widely distributed pRE25-, pRUM-, pIP501- and pHTbeta-related replicons associated with glycopeptide resistance and stabilizing toxin-antitoxin systems. FEMS. Immunol Med Microbiol 58:254–268CrossRefGoogle Scholar
  41. 41.
    Toğay SO, Keskin AC, Açik L, Temiz A (2010) Virulence genes, antibiotic resistance and plasmid profiles of Enterococcus faecalis and Enterococcus faecium from naturally fermented Turkish foods. J Appl Microbiol 109:1084–1092CrossRefGoogle Scholar
  42. 42.
    Pouwels PH, Leer RJ (1993) Genetics of lactobacilli: plasmids and gene expression. Antonie Van Leeuwenhoek 64:85–107CrossRefGoogle Scholar
  43. 43.
    Samaržija D, Antunac N, Havranek JL (2001) Taxonomy, physiology and growth of Lactococcus lactis: a review. Mljekarstvo 51:35–48Google Scholar
  44. 44.
    Zhang WY, Zhang HP (2014) Genomics of lactic acid bacteria. In: Zhang HP, Cai YM (eds) Lactic acid bacteria-fundamentals and practice, 1st edn. Springer Publishing Inc., New YorkCrossRefGoogle Scholar
  45. 45.
    Shareck J, Choi Y, Lee B, Miguez CB (2004) Cloning vectors based on cryptic plasmids isolated from lactic acid bacteria: their characteristics and potential applications in biotechnology. Crit Rev Biotechnol 24:155–208CrossRefGoogle Scholar
  46. 46.
    Schroeter J, Klaenhammer T (2009) Genomics of lactic acid bacteria. FEMS Immunol Med Microbiol 292:1–6CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Joana Salomskiene
    • 1
  • Dovile Jonkuviene
    • 1
    Email author
  • Irena Macioniene
    • 1
  • Asta Abraitiene
    • 2
  • Jurate Zeime
    • 1
  • Jurate Repeckiene
    • 3
  • Lina Vaiciulyte-Funk
    • 1
  1. 1.Food InstituteKaunas University of TechnologyKaunasLithuania
  2. 2.Institute of BiotechnologyVilnius UniversityVilniusLithuania
  3. 3.Nature Research Center, Institute of BotanyVilniusLithuania

Personalised recommendations