Hostname: page-component-77c89778f8-vsgnj Total loading time: 0 Render date: 2024-07-20T11:20:04.902Z Has data issue: false hasContentIssue false

Probiotic potential of Lactobacillus spp. isolated from Brazilian regional ovine cheese

Published online by Cambridge University Press:  17 January 2012

Stela Maris Meister Meira
Affiliation:
Laboratório de Bioquímica e Microbiologia Aplicada, Departamento de Ciência de Alimentos, ICTA, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves 9500, 91501-970 Porto Alegre, Brazil
Virginia Etges Helfer
Affiliation:
Laboratório de Bioquímica e Microbiologia Aplicada, Departamento de Ciência de Alimentos, ICTA, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves 9500, 91501-970 Porto Alegre, Brazil
Renata Voltolini Velho
Affiliation:
Laboratório de Bioquímica e Microbiologia Aplicada, Departamento de Ciência de Alimentos, ICTA, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves 9500, 91501-970 Porto Alegre, Brazil
Fernanda Cortez Lopes
Affiliation:
Laboratório de Bioquímica e Microbiologia Aplicada, Departamento de Ciência de Alimentos, ICTA, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves 9500, 91501-970 Porto Alegre, Brazil
Adriano Brandelli*
Affiliation:
Laboratório de Bioquímica e Microbiologia Aplicada, Departamento de Ciência de Alimentos, ICTA, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves 9500, 91501-970 Porto Alegre, Brazil
*
*For correspondence; e-mail: abrand@ufrgs.br

Abstract

Twelve Lactobacillus isolates from Brazilian starter-free ovine cheeses were evaluated for their probiotic potential. The strains were identified by 16S rDNA sequencing as Lactobacillus plantarum (7), Lb. brevis (2), Lb. casei (2) and Lb. parabuchneri (1). All strains showed variable resistance to gastric juices and relative tolerance to pancreatin and bile salts. Only five strains of Lb. plantarum could not deconjugate the sodium salt of taurodeoxycholic acid. Autoaggregation ability after 24 h was above 50% and hydrophobicity was higher than 60% for most strains. All lactobacilli could inhibit linolenic acid oxidation, except Lb. parabuchneri strain, whereas none of them could scavenge DPPH radical. β-Galactosidase activity ranged from 47·7 to 2503 Miller units. Inhibition of food pathogens Listeria monocytogenes, Staphylococcus aureus, Bacillus cereus, Escherichia coli and Salmonella typhimurium was demonstrated and the production of organic acids could be associated with this effect. The Lactobacillus strains from Brazilian regional ovine cheese showed interesting functional characteristics, mainly the strains Lb. brevis SM-B and Lb. plantarum SM-I. Both presented high acid tolerance. In addition, Lb. brevis SM-B also displayed remarkable antioxidant activity and Lb. plantarum SM-I was the highest β-galactosidase producer, exhibited high autoaggregation and hydrophobicity properties.

Type
Research Article
Copyright
Copyright © Proprietors of Journal of Dairy Research 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Annuk, H, Shchepetova, J, Kullisaar, T, Songisepp, E, Zilmer, M & Mikelsaar, M 2003 Characterization of intestinal lactobacilli as putative probiotic candidates. Journal of Applied Microbiology 94 403412CrossRefGoogle ScholarPubMed
Begley, M, Hill, C & Gahan, CGM 2006 Bile salt hydrolase activity in probiotics. Applied and Environmental Microbiology 72 17291738CrossRefGoogle ScholarPubMed
Bizani, D & Brandelli, A 2002 Characterization of a bacteriocin produced by a newly isolated Bacillus sp. strain 8A. Journal of Applied Microbiology 93 512519CrossRefGoogle Scholar
Brand-Williams, W, Cuvelier, ME & Berset, C 1995 Use of a free radical method to evaluate antioxidant activity. LWT Food Science and Technology 28 2530CrossRefGoogle Scholar
Caldini, G, Trotta, F, Corsetti, A & Cenci, G 2008 Evidence for in vitro anti-genotoxicity of cheese non-starter lactobacilli. Antonie van Leeuwenhoek 93 5159CrossRefGoogle ScholarPubMed
Cebeci, A & Gürakan, C 2003 Properties of potential probiotic Lactobacillus plantarum strains. Food Microbiology 20 511518CrossRefGoogle Scholar
Collado, MC, Meriluoto, J & Salminen, S 2008 Adhesion and aggregation properties of probiotic and pathogen strains. European Food Research and Technology 226 10651073CrossRefGoogle Scholar
Corcoran, BM, Stanton, C, Fitzgerald, GF & Ross, RP 2005 Survival of probiotic lactobacilli in acidic environments is enhanced in the presence of metabolizable sugars. Applied and Environmental Microbiology 71 30603067CrossRefGoogle ScholarPubMed
Corsetti, A, Caldini, G, Mastrangelo, M, Trotta, F, Valmorri, S & Cenci, G 2008 Raw milk traditional Italian ewe cheeses as a source of Lactobacillus casei strains with acid-bile resistance and antigenotoxic properties. International Journal of Food Microbiology 125 330335CrossRefGoogle ScholarPubMed
Coton, M, Berthier, F & Coton, E 2008 Rapid identification of the three major species of dairy obligate heterofermenters Lactobacillus brevis, Lactobacillus fermentum and Lactobacillus parabuchneri by species-specific duplex PCR. FEMS Microbiology Letters 284 150157CrossRefGoogle ScholarPubMed
De Vuyst, L & Leroy, F 2007 Bacteriocins from lactic acid bacteria: production, purification, and food applications. Journal of Molecular Microbiology and Biotechnology 13 194199Google ScholarPubMed
FAO/WHO 2002 Guidelines for the evaluation of probiotics in food. London, Ontario: Food and Agriculture Organization of the United Nations and World Health Organization Working Group Report, 111Google Scholar
Granato, D, Branco, GF, Nazzaro, F, Cruz, AG & Faria, JAF 2010 Functional foods and nondairy probiotic food development: Trends, concepts, and products. Comprehensive Review of Food Science and Food Safety 9 292302CrossRefGoogle ScholarPubMed
Guglielmotti, DM, Marcó, MB, Golowczyc, M, Reinheimer, JA & Quiberoni, LQ 2007 Probiotic potential of Lactobacillus delbrueckii strains and their phage resistant mutants. International Dairy Journal 17 916925CrossRefGoogle Scholar
Guo, Z, Wang, J, Yan, L, Chen, W & Liu, X 2009 In vitro comparison of probiotic properties of Lactobacillus casei Zhang, a potential new probiotic, with selected probiotic strains. LWT Food Science and Technology 42 16401646CrossRefGoogle Scholar
Holzapfel, WH, Geisen, R & Schillinger, U 1995 Ecological preservation of foods with reference to protective cultures, bacteriocins and food-grade enzymes. International Journal of Food Microbiology 24 343362CrossRefGoogle Scholar
Huang, Y & Adams, MC 2004 In vitro assessment of the upper gastrointestinal tolerance of potential probiotic dairy propionibacteria. International Journal of Food Microbiology 91 253260CrossRefGoogle ScholarPubMed
Ibrahim, SA & O'Sullivan, DJ 2000 Use of chemical mutagenesis for the isolation of food grade β-galactosidase overproducing mutants of bifidobacteria, lactobacilli and Streptococcus thermophilus. Journal of Dairy Science 83 923930CrossRefGoogle ScholarPubMed
Jacobsen, C, Rosenfeldt, N, Hayford, A, Møller, P, Michaelsen, K, Pærregaard, A, Sandström, B & Tvede, M 1999 Screening of probiotic activities of forty seven strains of Lactobacillus spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans. Applied and Environmental Microbiology 65 49494956CrossRefGoogle ScholarPubMed
Kullisaar, T, Zilmer, M, Mikelsaar, M, Vihalemm, T, Annuk, H, Kairane, C & Kilk, A 2002 Two antioxidative lactobacilli strains as promising probiotics. International Journal of Food Microbiology 72 215224CrossRefGoogle ScholarPubMed
Lin, M & Chang, F 2000 Antioxidative effect of intestinal bacteria Bifidobacterium longum ATCC 15708 and Lactobacillus acidophilus ATCC 4356. Digestive Disease Science 45 16171622CrossRefGoogle ScholarPubMed
Lisboa, MP, Bonatto, D, Bizani, D, Henriques, JAP & Brandelli, A 2006 Characterization of a bacteriocin-like substance produced by Bacillus amyloliquefaciens isolated from the Brazilian Atlantic forest. International Microbiology 9 111118Google ScholarPubMed
Majhenic, AC, Lorberg, PM & Rogelj, I 2007 Characterisation of the Lactobacillus community in traditional Karst ewe's cheese. International Journal of Dairy Technology 60 182190CrossRefGoogle Scholar
Maragkoudakis, PA, Zoumpopoulou, G, Miaris, C, Kalantzopoulos, G, Pot, B & Tsakalidou, E 2006 Probiotic potential of Lactobacillus strains isolated from dairy products. International Dairy Journal 16 189199CrossRefGoogle Scholar
Martins, FS, Silva, AA, Vieira, AT, Barbosa, FHF, Arantes, RME, Teixeira, MM & Nicoli, JR 2009 Comparative study of Bifidobacterium animalis, Escherichia coli, Lactobacillus casei and Saccharomyces boulardii probiotic properties. Archives of Microbiology 191 623630CrossRefGoogle ScholarPubMed
Mathara, JM, Schillinger, U, Guigas, C, Franz, C, Kutima, PM, Mbugua, SK, Shin, HK & Holzapfel, WH 2008 Functional characteristics of Lactobacillus spp. from traditional Maasai fermented milk products in Kenya. International Journal of Food Microbiology 126 5764CrossRefGoogle ScholarPubMed
Moser, SA & Savage, DC 2001 Bile salt hydrolase activity and resistance to toxicity of conjugated bile salts are unrelated properties in lactobacilli. Applied and Environmental Microbiology 67 34763480CrossRefGoogle ScholarPubMed
Navidghasemizad, S, Hesari, J, Saris, P & Nahaei, MR 2009 Isolation of lactic acid bacteria from Lighvan cheese, a semihard cheese made from raw sheep milk in Iran. International Journal of Dairy Technology 62 260264CrossRefGoogle Scholar
Nespolo, CR & Brandelli, A 2010 Production of bacteriocin-like substances by lactic acid bacteria isolated from regional ovine cheese. Brazilian Journal of Microbiology 41 10091018CrossRefGoogle ScholarPubMed
Nespolo, CR, Correa, APF, Ritter, AC & Brandelli, A 2010 Comparison of Fascal cheese produced with natural, commercial or autochthonous cultures. International Journal of Dairy Technology 63 387395CrossRefGoogle Scholar
Ortu, S, Felis, GE, Marzotto, M, Deriu, A, Molicotti, P, Sechi, LA, Dellaglio, F & Zanetti, S 2007 Identification and functional characterization of Lactobacillus strains isolated from milk and Gioddu, a traditional Sardinian fermented milk. International Dairy Journal 17 13121320CrossRefGoogle Scholar
Pan, X, Chen, F, Wua, T, Tang, H & Zhao, Z 2009 The acid, bile tolerance and antimicrobial property of Lactobacillus acidophilus NIT. Food Control 20 598602CrossRefGoogle Scholar
Parvez, S, Malik, KA, Kang, SA & Kim, HY 2006 Probiotics and their fermented food products are beneficial for health. Journal of Applied Microbiology 100 11711185CrossRefGoogle ScholarPubMed
Pinto, MGV, Franz, CMAP, Schillinger, U & Holzapfel, WH 2006 Lactobacillus spp. with in vitro probiotic properties from human faeces and traditional fermented products. International Journal of Food Microbiology 109 205214CrossRefGoogle Scholar
Pisano, MB, Fadda, ME, Deplano, M, Corda, A, Casula, M & Cosentino, S 2007 Characterizarion of Fiore Sardo cheese manufactured with the addition of autochthonous cultures. Journal of Dairy Research 74 255261CrossRefGoogle Scholar
Sánchez, I, Seseña, S, Poveda, JM, Cabezas, L & Palop, L 2006 Genetic diversity, dynamics, and activity of Lactobacillus community involved in traditional processing of artisanal Manchego cheese. International Journal of Food Microbiology 107 265273CrossRefGoogle ScholarPubMed
Sengül, M 2006 Microbiological characterization of Civil cheese, a traditional Turkish cheese: microbiological quality, isolation and identification of its indigenous lactobacilli. World Journal of Microbiology and Biotechnology 22 613618CrossRefGoogle Scholar
Sengül, M & Cakmakci, S 2003 Characterization of natural isolates of lactic acid bacteria from Erzincan (Savak) Tulum cheese. Milchwissenschaft 58 510513Google Scholar
Servin, AL 2004 Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiology Reviews 28 405440CrossRefGoogle ScholarPubMed
Thompson, JD, Higgins, DG & Gibson, TJ 1994 CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22 46734680CrossRefGoogle Scholar
Ustok, FI, Tari, C & Harsa, S 2010 Biochemical and thermal properties of β-galactosidase enzymes produced by artisanal yoghurt cultures. Food Chemistry 119 11141120CrossRefGoogle Scholar
Valerio, F, Bellis, PD, Lonigro, SL, Morelli, L, Visconti, A & Lavermicocca, P 2006 In vitro and in vivo survival and transit tolerance of potentially probiotic strains carried by artichokes in the gastrointestinal tract. Applied and Environmental Microbiology 72 30423045CrossRefGoogle ScholarPubMed
Vasiljevic, T & Shah, NP 2008 Probiotics – From Metchnikoff to bioactives. International Dairy Journal 18 714728CrossRefGoogle Scholar
Vinderola, CG & Reinheimer, JA 2003 Lactic acid starter and probiotic bacteria: a comparative “in vitro” study of probiotic characteristics and biological barrier resistance. Food Research International 36 895904CrossRefGoogle Scholar
Vinderola, G, Capellini, B, Villarreal, F, Suárez, V, Quiberoni, A & Reinheimer, JA 2008 Usefulness of a set of simple in vitro tests for the screening and identification of probiotic candidate strains for dairy use. LWT Food Science and Technology 41 16781688CrossRefGoogle Scholar
Wang, AN, Yi, XW, Yu, HF, Dong, B & Qiao, SY 2009 Free radical scavenging activity of Lactobacillus fermentum in vitro and its antioxidative effect on growing-finishing pigs. Journal of Applied Microbiology 107 11401148CrossRefGoogle ScholarPubMed
Xu, H, Jeong, HS, Lee, HY & Ahn, J 2009 Assessment of cell surface properties and adhesion potential of selected probiotic strains. Letters in Applied Microbiology 49 434442CrossRefGoogle ScholarPubMed
Zanoni, S, Pompei, A, Cordisco, L, Amaretti, A, Rossi, M & Matteuzzi, D 2008 Growth kinetics on oligo- and polysaccharides and promising features of three antioxidative potential probiotic strains. Journal of Applied Microbiology 105 12661276CrossRefGoogle ScholarPubMed