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Production of bacteriocin-like inhibitory substance by Bifidobacterium lactis in skim milk supplemented with additives

Published online by Cambridge University Press:  08 April 2015

Fabio Andres Castillo Martinez
Affiliation:
Department of Biochemical and Pharmaceutical Technology, Faculty of Pharmaceutical Sciences, University of São Paulo, São Paulo, Brazil
José Manuel Domínguez
Affiliation:
Chemical Engineering Department, Faculty of Sciences, University of Vigo (Campus Ourense), As Lagoas s/n, 32004 Ourense, Spain
Attilio Converti
Affiliation:
Departament of Civil, Chemical and Environmental Engineering, Pole of Chemical Engineering, Genoa University, Genoa, Italy
Ricardo Pinheiro de Souza Oliveira*
Affiliation:
Department of Biochemical and Pharmaceutical Technology, Faculty of Pharmaceutical Sciences, University of São Paulo, São Paulo, Brazil
*
*For correspondence; e-mail: rpsolive@usp.br

Abstract

Bacteriocins are natural compounds used as food biopreservatives instead of chemical preservatives. Bifidobacterium animalis subsp. lactis (Bifid. lactis) was shown to produce a bacteriocin-like inhibitory substance (BLIS) able to inhibit the growth of Listeria monocytogenes selected as an indicator microorganism. To enhance this production by the strain Bifid. lactis BL 04, skim milk (SM) was used as a fermentation medium either in the presence or in the absence of yeast extract, Tween 80 or inulin as stimulating additives, and the results in terms of bacterial growth and BLIS production were compared with those obtained in a traditional high cost complex medium such as Man, Rogosa and Sharpe (MRS). To this purpose, all the cultivations were carried out in flasks at 200 rpm under anaerobic conditions ensured by a nitrogen flowrate of 1·0 L/min for 48 h, and BLIS production was quantified by means of a modified agar diffusion assay at low values of both temperature and concentration of List. monocytogenes. Although all these ingredients were shown to exert positive influence on BLIS production in both media, yeast extract and SM were by far the best ingredient and the best medium, respectively, allowing for a BLIS production at the late exponential phase of 2000 AU/ml.

Type
Research Article
Copyright
Copyright © Proprietors of Journal of Dairy Research 2015 

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References

Aasen, IM, Møretrø, T, Katla, T, Axelsson, L & Storrø, I 2000 Influence of complex nutrients, temperature and pH on bacteriocin production by Lactobacillus sakei CCUG 42687. Applied Microbiology and Biotechnology 53 159166CrossRefGoogle ScholarPubMed
Abd, ES, Saleh, MH, Kholi, FA, El-Sayed, AM, Abdou, SM & El- Shibiny, S 2004 Isolation and characterization of bacteriocins produced by Bifidobacterium lactis BB-12 and Bifidobacterium longum BB-46. 9th Egyptian Conference for Dairy Science and Technology. Cairo, EgyptGoogle Scholar
Anand, SK, Srinivasan, RA & Rao, LK 1984 Antimicrobial activity associated with Bifidobacterium bifidum-I. Cultured Dairy Products Journal 2 67Google Scholar
Anand, SK, Srinivasan, RA, Rao, LK 1985 Antibacterial activity associated with Bifidobacterium bifidum-II. Cultured Dairy Products Journal 2 2123Google Scholar
Avonts, L, Uytven, EV, De Vuyst, L 2004 Cell growth and bacteriocin production of probiotic Lactobacillus strains in different media. International Dairy Journal 14 947955CrossRefGoogle Scholar
Ballongue, J 2004 Bifidobacteria and probiotic action. In Lactic Acid Bacteria: Microbiological and Functional Aspects, 3rd edition. New York: Marcel Dekker, pp. 67124Google Scholar
Cabo, ML, Murado, MA, Gonzalez, MP, Vazquez, JA, Pastoriza, L 2001 An empirical model for describing the effects of nitrogen sources on nisin production. Letters in Applied Microbiology 33 425429CrossRefGoogle ScholarPubMed
Cheikhyoussef, A, Cheikhyoussef, 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 746753CrossRefGoogle Scholar
Cheikhyoussef, A, Pogori, N, Chen, H, Tian, F, Chen, W, Tang, J & Zhang, H 2009a Antimicrobial activity and partial characterization of bacteriocin-like inhibitory substances (BLIS) produced by Bifidobacterium infantis BCRC 14602. Food Control 20 553559CrossRefGoogle Scholar
Cheikhyoussef, A, Pogori, N, Chen, H, Zhao, J, Tang, J, Chen, W & Zhang, H 2009b Comparison of three different methods for the isolation of bacteriocin-like inhibitory substances from Bifidobacterium infantis BCRC 14602. Journal of Rapid Methods and Automation in Microbiology 17 182194CrossRefGoogle Scholar
Cheikhyoussef, A, Pogori, N, Chen, W & Zhang, H 2008 Antimicrobial proteinaceous compounds obtained from bifidobacteria: from production to their application. International Journal of Food Microbiology 125 215222CrossRefGoogle ScholarPubMed
Collado, M, Hernández, M & Sanz, Y 2005 Production of bacteriocin-like inhibitory compounds by human fecal Bifidobacterium strains. Journal of Food Protection 68 10341340CrossRefGoogle ScholarPubMed
Deegan, LH, Cotter, PD, Hill, C & Ross, P 2006 Bacteriocins: biological tools for bio-preservation and shelf-life extension. International Dairy Journal 16 10581071CrossRefGoogle Scholar
Eijsink, VGH, Axelsson, L, Diep, DB, Håvarstein, LS, Holo, H & Nes, IF 2002 Production of class II bacteriocins by lactic acid bacteria; an example of biological warfare and communication. Antonie van Leeuwenhoek 81 639654CrossRefGoogle ScholarPubMed
Gomes, AMP & Malcata, FX 1999 Bifidobacterium spp. and Lactobacillus acidophilus: biological, biochemical, technological and therapeutical properties relevant for use as probiotics. Trends in Food Science and Technology 10 139157CrossRefGoogle Scholar
Jalili, H, Razavi, H & Safari, M 2010 Effect of whey permeate and yeast extract on metabolic activity of Bifidobacterium animalis subsp. lactis Bb 12 cultivated in skim milk based media. Iranian Journal of Biotechnology 1 3845Google Scholar
Janer, C, Pel, C & Requena, T 2004 Caseinomacropeptide and whey protein concentrate enhance Bifidobacterium lactis growth in milk. Food Chemistry 86 263267CrossRefGoogle Scholar
Kang, KH, Shin, HJ, Park, YH & Lee, TS 1989 Studies on the antibacterial substances produced by lactic acid bacteria: purification and some properties of antibacterial substance “Bifilong” produced by B. longum. Korean Dairy Science 1 204216Google Scholar
Keren, T, Yarmus, M, Halevy, G & Shapira, R 2004 Immunodetection of the bacteriocin lactacin RM: analysis of the influence of temperature and tween 80 on its expression and activity. Applied and Environmental Microbiology 70 20982104CrossRefGoogle Scholar
Lee, JH, Li, X & O'Sullivan, DJ 2011 Transcription analysis of a lantibiotic gene cluster from Bifidobacterium longum DJO10A. Applied and Environmental Microbiology 77 58795887CrossRefGoogle ScholarPubMed
Leroy, F & De Vuyst, L 2001 Growth of the bacteriocin-producing Lactobacillus sakei strain CTC 494 in MRS broth is strongly reduced due to nutrient exhaustion: a nutrient depletion model for the growth of lactic acid bacteria. Applied and Environmental Microbiology 67 44074413CrossRefGoogle ScholarPubMed
Leroy, F, Vankrunkelsven, S, De Greef, J & De Vuyst, L 2003 The stimulating effect of a harsh environment on the bacteriocin activity by Enterococcus faecium RZS C5 and dependency on the environmental stress factor used. International Journal of Food Microbiology 83 2738CrossRefGoogle ScholarPubMed
Martinez, FAC, Balciunas, EM, Converti, A, Cotter, PD & Oliveira, RPS 2013 Bacteriocin production by Bifidobacterium spp. A review. Biotechnology Advances 31 482488CrossRefGoogle ScholarPubMed
Mendonça, TT, Gomez, JGC, Buffoni, E, Sánchez Rodriguez, RJ, Schripsema, J, Lopes, MSG & Silva, LF 2013 Exploring the potential of Burkholderia sacchari to produce polyhydroxyalkanoates. Journal of Applied Microbiology 116 815829CrossRefGoogle ScholarPubMed
Oliveira, RPS, Perego, P, Oliveira, MN & Converti, A 2012 Growth, organic acids profile and sugar metabolism of Bifidobacterium lactis in co-culture with Streptococcus thermophilus: the inulin effect. Food Research International 48 2127CrossRefGoogle Scholar
Picard, C, Fioramonti, J, Francois, A, Robinson, T, Neant, F & Matuchansky, C 2005 Review article: bifidobacteria as probiotic agents - physiological effects and clinical benefits. Alimentary Pharmacology and Therapeutics 22 495512CrossRefGoogle ScholarPubMed
Pongtharangkul, T & Demirci, A 2004 Evaluation of agar diffusion bioassay for nisin quantification. Applied and Microbial Biotechnology 65 268272CrossRefGoogle ScholarPubMed
Ramirez-Farias, C, Slezak, K, Fuller, Z, Duncan, A, Holtrop, G & Louis, P 2009 Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii. British Journal of Nutrition 101 541550CrossRefGoogle ScholarPubMed
Tomás, MSJ, Bru, E, Nader-Macías, MEF 2010 Estimation of combined effects of carbon and nitrogen sources on the growth and bacteriocin production of Lactobacillus salivarius from human source. Journal of Basic Microbiology 50 190199CrossRefGoogle ScholarPubMed
Van der Meulen, R, Adriany, T, Verbrugghe, K & De Vuyst, L 2006 Kinetic analysis of bifidobacterial metabolism reveals a minor role for succinic acid in the regeneration of NAD+ through its growth-associated production. Applied and Environmental Microbiology 72 52045210CrossRefGoogle ScholarPubMed
Von Ah, U 2006 Identification of Bifidobacterium thermophilum RBL67 isolated from baby faeces and partial purification of its bacteriocin. PhD Thesis, Swiss Federal Institute of Technology Zurich, SwitzerlandGoogle Scholar
Yildirim, Z & Johnson, M 1998 Characterization and antimicrobial spectrum of bifidocin B, a bacteriocin produced by Bifidobacterium bifidum NCFB 1454. Journal of Food Protection 61 4751CrossRefGoogle Scholar
Yildirim, Z, Winters, D & Johnson, M 1999 Purification, amino acid sequence and mode of action of bifidocin B produced by Bifidobacterium bifidum NCFB 1454. Journal of Applied Microbiology 86 4554CrossRefGoogle ScholarPubMed