Advertisement

Molecular Biology Reports

, Volume 46, Issue 1, pp 461–469 | Cite as

Antimicrobial activity of bacteriocin-like inhibitory substance produced by Pediococcus pentosaceus: from shake flasks to bioreactor

  • Pamela Oliveira de Souza de Azevedo
  • Attilio Converti
  • Martin Gierus
  • Ricardo Pinheiro de Souza OliveiraEmail author
Original Article

Abstract

Bacteriocins are peptides produced by various species of bacteria, especially lactic acid bacteria (LAB), which have a large spectrum of action against spoilage bacteria and foodborne pathogens. However, when not entirely characterized, they are alternatively called bacteriocin-like inhibitory substances (BLIS). Pediococcus pentosaceus ATCC 43200 grew and produced BLIS optimally when cultivated anaerobically in bioreactor for 24 h at 30 °C and 200 rpm in De Man, Rogosa and Sharp (MRS) medium supplemented with 1.5% peptone. Under such optimal conditions, the cell mass concentration (3.41 g/L) was 66% higher, the generation time (1.28 h) 38% shorter and the BLIS activity against different indicator strains significantly higher than in MRS medium without any supplement taken as a control, and the exponential phase started 4 h before. The agar diffusion method showed BLIS inhibition halos against LAB strains with diameter in the range 11.0–19.5 mm and specific areas between 377.1 and 2654.6 mm2/mL, while BLIS activity against Listeria strains was better quantified by the liquid medium assay that showed, for the fermented broth without any dilution, 100 and 50% inhibition of Listeria innocua and Listeria seeligeri growth, respectively. These results highlight the potential of P. pentosaceus BLIS as a natural antimicrobial for application in the food industry.

Keywords

Probiotic bacteria Lactic acid bacteria Fermentation process Bacteriocin-like inhibitory substance Natural antimicrobial 

Notes

Acknowledgements

This work was supported by the São Paulo Research Foundation (FAPESP) under Grant 2016/06284-9, by the National Council for Scientific and Technological Development - CNPq and by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Human and animal participants

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. 1.
    Cortés-Zavaleta O, López-Malo A, Hernández-Mendonza A, García HS (2014) Antifungal activity of Lactobacilli and its relationship with 3-phenyllactic acid production. Int J Food Microbiol 173(3):30–35Google Scholar
  2. 2.
    Porto MCW, Kuniyoshi TM, Azevedo POS, Vitolo M, Oliveira RPS (2017) Pediococcus spp.: an important genus of lactic acid bacteria and pediocin producers. Biotechnol Adv 35(3):361–374Google Scholar
  3. 3.
    Altuntaş EG, Ayhan K, Peker S, Ayhan B, Demiralp D (2014) Purification and mass spectrometry based characterization of a pediocin produced by Pediococcus acidilactici. Mol Biol Rep 41:6879–6885Google Scholar
  4. 4.
    Kothari D, Tyagi A, Patel S, Goyal A (2011) Dextransucrase from the mutant of Pediococcus pentosaceus (PPm) is more stable than the wild type. Biotechnology 1(4):199–205Google Scholar
  5. 5.
    Ly MH Covarrubias-Cervantes M, Dury-Brun C, Bordet S, Voilley A, Le TM, Belin JM, Waché Y (2008) Interactions between bacterial surfaces milk proteins, impact on food emulsions stability. Food Hydrocoll 22(5):742–751Google Scholar
  6. 6.
    Cheikhyoussef A, Cheikhyossef N, Chen H, Zhao J, Tang J, Zhang H, Chen W (2010) Bifidin I-A new bacteriocin produced by Bifidobacterium infantis BCRC 14602: purification and partial amino acid sequence. Food Control 21(5):746–753Google Scholar
  7. 7.
    Saad N, Delattre C, Urdaci M, Schmitter JM, Bressollier P (2013) An overview of the last advances in probiotic and prebiotic field. LWT Food Sci Technol 50(1):1–16Google Scholar
  8. 8.
    Zhang B, Tong H, Dong X (2005) Pediococcus cellicola sp. nov., a novel lactic acid coccus isolated from a distilled-spirit-fermenting cellar. Int J Syst Evol Microbiol 55(5):2167–2170Google Scholar
  9. 9.
    Hough JS, Briggs DE, Stevens R, Young TW (1982) Malting and Brewing. Science, 2nd edn. Chapman & Hall, New YorkGoogle Scholar
  10. 10.
    Priest FG (2006) Microbiology and microbial control in the Brewery. In: Priest FG, Stewart GH (eds) Handbook of brewing, 2nd edn. Tylor and Francis, Boca Roca, pp 607–628Google Scholar
  11. 11.
    Reddy KVR, Yedery RD, Gupta SM (2004) Antimicrobial peptides: premises and promises. Int J Antimicrob Agents 24(6):536–547Google Scholar
  12. 12.
    Galvez A, Lopez RL, Abriouel H, Valdivia E, Omar NB (2008) Application of bacteriocins in the control of food borne pathogenic and spoilage bacteria. Crit Rev Biotechnol 28(2):125–152Google Scholar
  13. 13.
    Collins B, Cotter PD, Hill C, Ross RP (2010) Applications of lactic acid bacteria-produced bacteriocins. In: Mozzi F, Raya RR, Vignolo GM (eds), Novel applications. Wiley-Blackwell, Iowa, pp 89–109Google Scholar
  14. 14.
    Perin LM, Moraes PM, Viçosa GN, Júnior AS, Nero LA (2012) Identification of bacteriocinogenic Lactococcus isolates from raw milk and cheese capable of producing nisin A and nisin Z. Int Dairy J 25(1):46–51Google Scholar
  15. 15.
    Jack RW, Tagg JR, Ray B (1995) Bacteriocins of Gram-positive bacteria. Microbiol Mol Biol Rev 59(2):171–200Google Scholar
  16. 16.
    Tagg JR, Dajani AS, Wannamaker LW (1976) Bacteriocin of Gram-positive bacteria. Bacteriol Rev 40(3):722–756Google Scholar
  17. 17.
    Saad SMI (2006) Probiotics and prebiotics: the state of the art. Braz J Pharm Sci 42(1):1–16Google Scholar
  18. 18.
    Anastasiadou S, Papagianni M, Filiousis G, Ambrosiadis I, Koidis P (2008) Growth and metabolism of a meat isolated strain of Pediococcus pentosaceus in submerged fermentation. Purification, characterization and properties of the produced pediocin SM-1. Enzyme Microb Technol 43(6):448–454Google Scholar
  19. 19.
    Drider D, Fimland G, Héchard Y, McMullen LM, Prévost H (2006) The continuing story of class IIa bacteriocins. Microbiol Mol Biol Rev 70(2):564–582Google Scholar
  20. 20.
    Díez L, Bojo-Bezares B, Zarazaga M, Rodríguez JM, Torres C, Ruiz-Larrea F (2012) Antimicrobial activity of pediocin PA-1 against Oenococcus oeni and other wine bacteria. Food Microbiol 31(2):167–172Google Scholar
  21. 21.
    Chen Y, Kirk N, Piper PW (1993) Effects of medium composition on MFα1 promoter-directed secretion of a small protease inhibitor in Saccharomyces cerevisiae batch fermentation. Biotechnol Lett 15(3):223–228Google Scholar
  22. 22.
    Lilly MD (1976) Production of intracellular microbial enzymes. In: Wingard Junior LB, Katchalski-Katzir E, Goldstein L (eds) Applied biochemistry and bioengineering, 2nd edn. Academic Press, New York, pp. 306Google Scholar
  23. 23.
    Sidek NLM, Tan JS, Abbasiliasi S, Wonga FWF, Mustafa S, Ariff AB (2017) Aqueous two-phase flotation for primary recovery of bacteriocin-like inhibitory substance (BLIS) from Pediococcus acidilactici Kp10. J Chromatogr B 1027:81–87Google Scholar
  24. 24.
    Merril CR, Goldman D, Sedman SA, Ebert MH (1981) Ultrasensitive strain for proteins in polyacrylamide gels shows regional variation in cerebrospinal fluid proteins. Science 211(4489):1437–1438Google Scholar
  25. 25.
    Callewaert R, De Vuyst L (2000) Bacteriocin production with Lactobacillus amylovorus DCE 471 is improved and stabilized by Fed-Batch fermentation. Appl Environ Microbiol 66(2):606–613Google Scholar
  26. 26.
    De Vuyst L, Vandamme EJ (1992) Influence of the carbon source on nisin production in Lactococcus lactis subsp. lactis batch fermentations. J Gen Microbiol 138(3):571–578Google Scholar
  27. 27.
    De Vuyst L, Callewaert R, Crabbé K (1996) Primary metabolic kinetics of bacteriocin biosynthesis by Lactobacillus amylovorus and evidence for stimulation of bacteriocin production under unfavorable growth conditions. Microbiol 142(4):817–827Google Scholar
  28. 28.
    Moortvedt-Abildgaard CIJ, Nissen-Meyer B, Jelle B, Grenov B, Skaugen M, Nes IF (1995) Production and pH-dependent bactericidal activity of lactocin S, a lantibiotic from Lactobacillus sakei L45. Appl Environ Microbiol 61(1):175–179Google Scholar
  29. 29.
    Piva A, Headon DR (1994) Pediocin A, a bacteriocin produced by Pediococcus pentosaceus FBB61. Microbiol 140(4):697–702Google Scholar
  30. 30.
    Azevedo POS, Molinari F, Oliveira RPS (2018) Importance of the agar-media in the evaluation of bacteriocin activity against the same test microorganisms. Braz J Pharm Sci 54(1):1–6Google Scholar
  31. 31.
    Cabo ML, Murado MA, González MP, Pastoriza L (1999) A method for bacteriocin quantification. J Appl Microbiol 87(6):907–914Google Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of Biochemical and Pharmaceutical TechnologyUniversity of São PauloSão PauloBrazil
  2. 2.Department of Civil, Chemical and Environmental EngineeringPole of Chemical EngineeringGenoaItaly
  3. 3.Department of Agrobiotechnology, Institute of Animal Nutrition, Livestock Products, and Nutrition Physiology (TTE), IFA-TullnUniversity of Natural Resources and Life Sciences (BOKU)ViennaAustria

Personalised recommendations