Skip to main content

Effects of pH and sugar supplements on bacteriocin-like inhibitory substance production by Pediococcus pentosaceus

Abstract

To improve bacteriocin-like inhibitory substance (BLIS) production by Pediococcus pentosaceus ATCC 43200, the influence of pH as well as the addition of sugars—either prebiotic (inulin) or not (sucrose)—on its metabolism were investigated. This strain was grown at pH 5.0 or 6.0 either in glucose-based MRS medium (control) or after addition of 0.5, 1.0 or 1.5% (w/w) sucrose and inulin (GSI-MRS) in the same percentages. In the control medium at pH 5.0, cell mass concentration after 48 h of fermentation (Xmax = 2.26 g/L), maximum specific growth rate (µmax = 0.180 h−1) and generation time (Tg = 3.84 h) were statistically coincident with those obtained in supplemented media. At pH 6.0 some variations occurred in these parameters between the control medium (Xmax = 2.68 g/L; µmax = 0.32 h−1; Tg = 2.17 h) and the above supplemented media (Xmax = 1.90, 2.52 and 1.86 g/L; µmax = 0.26, 0.33 and 0.32 h−1; Tg = 2.62, 2.06 and 2.11 h, respectively). Lactate production was remarkable at both pH values (13 and 16 g/L) and improved in all supplemented media, being 34 and 54% higher than in their respective control media, regardless of the concentration of these ingredients. Cell-free supernatant of the fermented control medium at pH 5.0 displayed an antimicrobial activity against Enterococcus 101 5.3% higher than that at pH 6.0 and even 20% higher than those of all supplemented media, regardless of the concentration of supplements. BLIS production was favored either at pH 5.0 or in the absence of any additional supplements, which were able, instead, to stimulate growth and lactate production by P. pentosaceus.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. 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):2167–2170. https://doi.org/10.1099/ijs.0.63778-0

    Article  CAS  PubMed  Google Scholar 

  2. Gibson GR, Fuller R (2000) Aspects of in vitro and in vivo research approaches directed towards identifying probiotics and prebiotics for human use. J Nutr 130(2):391S–395S

    Article  CAS  PubMed  Google Scholar 

  3. Rolfe RD (2000) The role of probiotic cultures in the control of gastrointestinal health. J Nutr 130(2):396S–402S

    Article  CAS  PubMed  Google Scholar 

  4. Cleveland J, Montiville TJ, Nes IF, Chikinda ML (2001) Bacteriocins: safe, natural antimicrobials for food preservation. Int J Microbiol 71(1):1–20

    Article  CAS  Google Scholar 

  5. Liu B, Yang M, Qi B, Chen X, Su Z, Wan Y (2010) Optimizing l-(+)-lactic acid production by thermophile Lactobacillus plantarum AS.1.3 using alternative nitrogen sources with response surface method. Biochem Eng J 59(2):212–219. https://doi.org/10.1016/j.bej.2010.08.013

    Article  CAS  Google Scholar 

  6. Behera SS, Ray RC, Zdolec N (2018) Lactobacillus plantarum with functional properties: an approach to increase safety and shelf-life of fermented foods. Biomed Res Int 2018:18. https://doi.org/10.1155/2018/9361614

    Article  CAS  Google Scholar 

  7. Axelsson L, Ahrné S, Ahrné S (2000) Lactic acid bacteria. Appl Microb Syst. Springer, Netherlands, pp 367–388

    Chapter  Google Scholar 

  8. Ray RC, Joshi VK (2014) Fermented foods: past, present and future scenario. In: Ray RC, Montet D (eds) Microorganisms and fermentation of traditional foods. CRC Press, Boca Raton, pp 1–36

    Chapter  Google Scholar 

  9. Park S, Ji Y, Park H, Lee K, Park H, RamBeck B, Shin H, Holzapfel WH (2016) Evaluation of functional properties of lactobacilli isolated from Korean white Kimchi. Food Control 69:5–12. https://doi.org/10.1016/j.foodcont.2016.04.037

    Article  CAS  Google Scholar 

  10. Leroy F, De Vuyst L (2004) Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci Technol 15(2):67–78. https://doi.org/10.1016/j.tifs.2003.09.004

    Article  CAS  Google Scholar 

  11. Simpson WJ, Taguchi H (1995) The genus Pediococcus, with notes on the genera Tetragenococcus and Aerociccis. In: Wood BJB, Holzapfel WH (eds) The genera of lactic acid bacteria. Blackie Academic and Professional, London, pp 125–172

    Chapter  Google Scholar 

  12. Costilow RN, Coughlin FM, Robach DL, Ragheb HS (1956) A study of the acid-forming bacteria from cucumber fermentations in Michigan. Food Res Int 21(1):27–33. https://doi.org/10.1111/j.1365-2621.1956.tb16888.x

    Article  Google Scholar 

  13. Etchells JL, Costilow RN, Anderson TE, Bell TA (1964) Pure culture fermentation of brined cucumbers. Appl Environ Microbiol 12(6):523–535

    CAS  Google Scholar 

  14. Piva A, Headon DR (1994) Pediocin A, a bacteriocin produced by Pediococcus pentosaceus FBB61. Microbiol 140(4):697–702. https://doi.org/10.1099/00221287-140-4-697

    Article  CAS  Google Scholar 

  15. Rueckert PW (1979) Studies on a bacteriocin-like activity produced by Pediococcus pentosaceus effective against Gram-positive organisms. MS thesis, Michigan State University East Lansing

  16. Leite JA, Tulini FL, Reis-Teixeira FB, Rabinovitch L, Chaves JQ, Rosa NG (2016) Bacteriocin-like inhibitory substances (BLIS) produced by Bacillus cereus: preliminary characterization and application of partially purified extract containing BLIS for inhibiting Listeria monocytogenes in pineapple pulp. LWT Food Sci Technol 72:261–266. https://doi.org/10.1016/j.lwt.2016.04.058

    Article  CAS  Google Scholar 

  17. Heng NCK, Wescombe PA, Burton JP, Jack RW, Tagg JR (2007) The diversity of bacteriocins in Gram-positive bacteria. In: Riley MA, Chavan MA (eds) Bacteriocins: ecology and evolution 45-92. Springer, New York, pp 45–92

    Chapter  Google Scholar 

  18. De Vuyst L, Vandamme EJ (1994) Lactic acid bacteria and bacteriocins: Their practical importance. In: De Vuyst L, Vandamme EJ (eds) Bacteriocins of Lactic Acid Bacteria. Microbiology Genetics and Applications. Blackie Academic and Professional, Glasgow, pp 1–11

    Chapter  Google Scholar 

  19. Settanni L, Corsetti A (2008) Application of bacteriocins in vegetable food biopreservation. Int J Food Microbiol 121:123–138. https://doi.org/10.1016/j.ijfoodmicro.2007.09.001

    Article  CAS  PubMed  Google Scholar 

  20. Allison GE, Klaenhammer TR (1998) Phage resistance mechanism in lactic acid bacteria. Int Dairy J 8:207–226

    Article  Google Scholar 

  21. Oscáriz JC, Lasa I, Pisabarro AG (1999) Detection and characterization of cerein 7, a new bacteriocin produced by Bacillus cereus with broad spectrum of activity. FEMS Microbiol Lett 178:337–341. https://doi.org/10.1111/j.1574-6968.1999.tb08696.x

    Article  PubMed  Google Scholar 

  22. Todorov SD, Dicks LMT (2004) Effect of medium components on bacteriocin production by Lactobacillus pentosus ST151BR, a strain isolated from beer produced by the fermentation of maize, barley and soy flour. World J Microbiol Biotechnol 20(6):643–650. https://doi.org/10.1023/B:WIBI.0000043196.09610.de

    Article  CAS  Google Scholar 

  23. Soro-Yao AA, Schumann P, Thonart P, Djè KM, Pukall R (2014) The use of MALDI-TOF Mass Spectrometry, ribotyping and phenotypic tests to identify lactic acid bacteria from fermented cereal foods in Abidjan (Côte d’Ivoire). Microbiol J 18(8):78–86. https://doi.org/10.2174/1874285801408010078

    Article  Google Scholar 

  24. Shukla R, Goyal A (2014) Probiotic potential of Pediococcus pentosaceus CRAG3: a new isolate from fermented cucumber. Probiotics Antimicrob Proteins 6(1):11–21. https://doi.org/10.1007/s12602-013-9149-8

    Article  CAS  PubMed  Google Scholar 

  25. Sabo SS, Converti A, Todorov SD, Domínguez JM, Oliveira RPS (2015) Effect of inulin on growth and bacteriocin production by Lactobacillus plantarum in stationary and shaken cultures. Int J Food Sci Technol 50(4):864–870. https://doi.org/10.1111/ijfs.12711

    Article  CAS  Google Scholar 

  26. Wagner EM, Jen KLC, Artiss JD, Remaley AT (2008) Dietary alpha-cyclodextrin lowers LDL-C and alters plasma fatty acid profile in LDLr-KO mice on a high-fat diet. Metabolism 57(8):1046–1051. https://doi.org/10.1016/j.metabol.2008.02.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Holub I, Gostner A, Theis S, Nosek L, Kudlich T, Melcher R, Scheppach W (2010) Novel findings of the metabolic effects of the low glycemic carbohydrate isomaltose (Palatinose™). Br J Nutr 103(12):1730–1737. https://doi.org/10.1017/S0007114509993874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Roberfroid M (2007) Prebiotics: the concept revisited. J Nutr 137(3):830S–837S

    Article  CAS  PubMed  Google Scholar 

  29. Oliveira RPS, Torres BR, Perego P, Oliveira MN, Converti A (2012) Co-metabolic models of Streptococcus thermophilus in co-culture with Lactobacillus bulgaricus or Lactobacillus acidophilus. Biochem Eng J 62:62–69. https://doi.org/10.1016/j.bej.2012.01.004

    Article  CAS  Google Scholar 

  30. Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125(6):1401–1412

    Article  CAS  PubMed  Google Scholar 

  31. Van Tyne D, Gilmore MS (2014) Friend turned foe: evolution of enterococcal virulence and antibiotic resistance. Annu Rev Microbiol 68:337–356. https://doi.org/10.1146/annurev-micro-091213-113003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Anderson CA, Jonas D, Huber I, Karygianni L, Wölber J, Hellwig E, Arweiler N, Vach K, Wittmer A, Al-Ahmad A (2016) Enterococcus faecalis from food, clinical specimens and oral sites: prevalence of virulence factors in association with biofilm formation. Front Microbiol 6:1534. https://doi.org/10.3389/fmicb.2015.01534

    Article  PubMed  PubMed Central  Google Scholar 

  33. Franz CM, Huch M, Abriouel H, Holzapfel W, Galvez A (2011) Enterococci as probiotic and their implications in food safety. Int J Food Microbiol 151:125–140. https://doi.org/10.1016/j.ijfoodmicro.2011.08.014

    Article  CAS  PubMed  Google Scholar 

  34. Hammerum AM (2012) Enterococci of animal origin and their significance for public health. Clin Microb Infect 18:619–625. https://doi.org/10.1111/j.1469-0691.2012.03829.x

    Article  CAS  Google Scholar 

  35. CDC (2010) Preliminary FoodNet data on the incidence of infection with pathogens transmitted commonly through food – 10 states. Morb Mortal Wkly Rep 59:418–422

    Google Scholar 

  36. Katouli M (2010) Population structure of gut Escherichia coli and its role in development of extra-intestinal infections. Iran J Microb 2:59–72

    Google Scholar 

  37. Greig JD, Ravel A (2009) Analysis of foodborne outbreak data reported internationally for source attribution. Int J Food Microbiol 130(2):77–87. https://doi.org/10.1016/j.ijfoodmicro.2008.12.031

    Article  CAS  PubMed  Google Scholar 

  38. Sofy AR, El-Monem A, Sharaf MA, Al Karim AG, Hmed AA, Moharam KM (2017) Prevalence of the harmful gram-negative bacteria in ready-to-eat-foods in Egypt. Food Public Health 7(3):59–68. https://doi.org/10.5923/j.fph.20170703.02

    Article  Google Scholar 

  39. Sidek NLM, Tan JS, Abbasiliasi S, Wonga FWF, Mustafa S, Ariff AB (2016) Aqueous two-phase flotation for primary recovery of bacteriocin-like inhibitory substance (BLIS) from Pediococcus acidilactici Kp10. J Chromatogr B 1027:81–87. https://doi.org/10.1016/j.jchromb.2016.05.024

    Article  CAS  Google Scholar 

  40. Blickstad E, Molin G (1981) Growth and lactic acid production of Pediococcus pentosaceus at different gas environments, temperatures, pH values and nitrite concentrations. Eur J Appl Microbiol Biotechnol 13(3):170–174. https://doi.org/10.1007/BF00703048

    Article  CAS  Google Scholar 

  41. Abbasiliasi S, Tan JS, Ibrahim TAT, Ramanan RN, Vakhshiteh F, Mustafa S, Ling TC, Rahim RA, Ariff AB (2012) Isolation of Pediococcus acidilactici Kp10 with ability to secrete bacteriocin-like inhibitory substance from milk products for application in food industry. BMC Microbiol 12:260. https://doi.org/10.1186/1471-2180-12-260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Perez RH, Perez MTM, Elegado FB (2015) Bacteriocins from lactic acid bacteria: a review of biosynthesis, mode of action, fermentative production, uses, and prospects. Int J Phil Sci Technol 8(2):61–67

    Article  Google Scholar 

  43. Azevedo POS, Converti A, Domínguez JM, de Souza Oliveira RP (2017) Stimulating effects of sucrose and inulin on growth, lactate and bacteriocin productions by Pediococcus pentosaceus. Probiotics Antimicrob Proteins 9(4):466–472. https://doi.org/10.1007/s12602-017-9292-8

    Article  CAS  Google Scholar 

  44. Adams M, Hall C (1988) Growth inhibition of food-borne pathogens by lactic and acetic acids and their mixtures. Int J Food Sci Technol 23(3):287–292. https://doi.org/10.1111/j.1365-2621.1988.tb00581.x

    Article  CAS  Google Scholar 

  45. Holyoak CD, Stratdford M, McMullin Z, Cole MB, Crimmins K, Brown AJ, Coote PJ (1996) Activity of the membrane H1-ATPase and optimal glycolytic flux required for rapid adaptation and growth in the presence of weak acid preservative sorbic acid. Appl Environ Microbiol 62(9):3158–3164

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Dunkley KD, Callaway TR, Chalova VI, McReynolds JL, Hume ME, Dunkley CS, Kubena LF, Nisbet DJ, Ricke SC (2009) Foodborne Salmonella ecology in the avian gastrointestinal tract. Anaerobe 15(1–2):26–35. https://doi.org/10.1016/j.anaerobe.2008.05.007

    Article  CAS  PubMed  Google Scholar 

  47. Rehman H, Vahjen W, Kohl-Parisini A, Ijaz A, Zentek J (2009) Influence of fermentable carbohydrates on the intestinal bacteria and enteropathogens in broilers. Worlds Poult Sci J 65(1):75–90. https://doi.org/10.1017/S0043933909000063

    Article  Google Scholar 

  48. Rémésy C, Levrat MA, Gamet L, Demigné C (1993) Cecal fermentations in rats fed oligosaccharides (inulin) are modulated by dietary calcium level. Am J Physiol 264(5 Pt 1):G855–G862. https://doi.org/10.1152/ajpgi.1993.264.5.G855

    Article  PubMed  Google Scholar 

  49. Azevedo POS, Converti A, Gierus M, Oliveira RPS (2018) Antimicrobial activity of bacteriocin-like inhibitory substance produced by Pediococcus pentosaceus: from shake flasks to bioreactor. Mol Biol Rep 46(1):461–469. https://doi.org/10.1007/s11033-018-4495-y

    Article  CAS  PubMed  Google Scholar 

  50. Singh PK, Sharma S, Kumari Am Korpole S (2014) A non-pediocin low molecular weight antimicrobial peptide produced by Pediococcus pentosaceus strain IE-3 shows increased activity under reducing environment. BMC Microbiol 14:226. https://doi.org/10.1186/s12866-014-0226-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Mathys S, von Ah Ueli, Lacroix C, Staub E, Mini R, Cereghetti T, Meile L (2007) Detection of the pediocin gene pedA in strains from human faeces by real-time PCR and characterization of Pediococcus acidilactici UVAI. BMC Biotechnol 7:55. https://doi.org/10.1186/1472-6750-7-55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Mortvedt-Abildgaard CI, Nissen-Meyer J, Jelle B, Grenov B, Skaugen M, Nes IF (1995) Production and pH-dependent bactericidal activity of Lactocin S, a lantibiotic from Lactobacillus sake L45. Appl Environ Microbiol 61:175–179

    CAS  Google Scholar 

  53. Conventry MJ, Gordon JB, Wilcock A, Harmark K, Davidson BE, Hickey MW, Hillier AJ, Wan J (1997) Detection of bacteriocins of lactic acid bacteria isolated from foods and comparison with pediocin and nisin. J Appl Microbiol 83(2):248–258

    Article  Google Scholar 

  54. Ramírez LAG, Otálvaro EVA (2008) Determinación del potencial bactericida In vitro de un aislado nativo de Lactobacillus casei frente E. coli. Rev Lasallista Invest 5(2):68–73

    Google Scholar 

  55. Pranckuté R, Kaunietis A, Kuisiené N, Citavicius D (2014) Development of synbiotics with inulin, palatinose, α-cyclodextrin and probiotic bacteria. Pol J Microbiol 63(1):33–41

    PubMed  Google Scholar 

Download references

Funding

This study was funded by São Paulo Research Foundation (FAPESP) under Grants [2018/04385-8 and 2018/04563-3] and by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001 and the National Council for Scientific and Technological Development (CNPq). Collaboration of the Promotion of Scientific and Technological Development of CONICYT, FONDECYT / POSTDOCTORAL (N° 3180765) Chile.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ricardo Pinheiro de Souza Oliveira.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

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

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Souza de Azevedo, P.O., de Azevedo, H.F., Figueroa, E. et al. Effects of pH and sugar supplements on bacteriocin-like inhibitory substance production by Pediococcus pentosaceus. Mol Biol Rep 46, 4883–4891 (2019). https://doi.org/10.1007/s11033-019-04938-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-019-04938-w

Keywords