Skip to main content

Advertisement

Log in

Probiotic Properties of Lactic Acid Bacteria Isolated from Water-Buffalo Mozzarella Cheese

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

This study evaluated the probiotic properties (stability at different pH values and bile salt concentration, auto-aggregation and co-aggregation, survival in the presence of antibiotics and commercial drugs, study of β-galactosidase production, evaluation of the presence of genes encoding MapA and Mub adhesion proteins and EF-Tu elongation factor, and the presence of genes encoding virulence factor) of four LAB strains (Lactobacillus casei SJRP35, Leuconostoc citreum SJRP44, Lactobacillus delbrueckii subsp. bulgaricus SJRP57 and Leuconostoc mesenteroides subsp. mesenteroides SJRP58) which produced antimicrobial substances (antimicrobial peptides). The strains survived the simulated GIT modeled in MRS broth, whole and skim milk. In addition, auto-aggregation and the cell surface hydrophobicity of all strains were high, and various degrees of co-aggregation were observed with indicator strains. All strains presented low resistance to several antibiotics and survived in the presence of commercial drugs. Only the strain SJRP44 did not produce the β-galactosidase enzyme. Moreover, the strain SJRP57 did not show the presence of any genes encoding virulence factors; however, the strain SJRP35 presented vancomycin resistance and adhesion of collagen genes, the strain SJRP44 harbored the ornithine decarboxylase gene and the strain SJRP58 generated positive results for aggregation substance and histidine decarboxylase genes. In conclusion, the strain SJRP57 was considered the best candidate as probiotic cultures for further in vivo studies and functional food products development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Todorov SD (2009) Bacteriocins from Lactobacillus plantarum: production, genetic organization and mode of action. A review. Braz J Microbiol 40:209–221

    Article  CAS  Google Scholar 

  2. Todorov SD, LeBlanc JG, Franco BDGM (2012) Evaluation of the probiotic potential and effect of encapsulation on survival for Lactobacillus plantarum ST16Pa isolated from papaya. J Microbiol Biotechnol 28:973–984

    Article  CAS  Google Scholar 

  3. FAO-WHO (2001) Food and agriculture organization of the United Nations. Word Health Organization. Report of a joint FAO-WHO expert consultation on evaluation of the health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria

  4. Sanders ME (2003) Probiotics: considerations for human health. Nutr Rev 61:91–99

    Article  Google Scholar 

  5. Hart AL, Lammers K, Brigidi P, Rizello F, Gionchetti P, Campieri M, Kamm MA, Knight SC, Stagg AJ (2004) Modulation of human dendritic cell phenotype and function by probiotic bacteria. Gut 53:1602–1609

    Article  CAS  Google Scholar 

  6. Galdeano CM, Perdigón G (2005) The probiotic bacterium Lactobacillus casei induces activation of the gut mucosal immune system through innate immunity. Clin Vaccine Immunol 13:219–222

    Article  Google Scholar 

  7. Saulnier DM, Gibson GR, Kolida S (2008) In vitro effects of selected synbiotics on the human faecal microbiota composition. FEMS Microbiol Ecol 66:516–527

    Article  CAS  Google Scholar 

  8. Vanderpool C, Yan F, Polk DB (2008) Mechanisms of probiotic action: implications for therapeutic applications in inflammatory bowel diseases. Inflamm Bowel Dis 14:1585–1596

    Article  Google Scholar 

  9. Chiang SS, Pan TM (2012) Beneficial effects of Lactobacillus paracasei subsp. paracasei NTU 101 and its fermented products. Appl Microbiol Biotechnol 93:903–916

    Article  CAS  Google Scholar 

  10. Gheytanchi E, Hesmati F, Shargh BK, Nowroozi J, Movahedzah F (2010) Study on β-galactosidase enzyme produced by isolated lactobacilli from milk and cheese. Afr J Microbiol Res 4:454–458

    CAS  Google Scholar 

  11. Cruz AG, Buriti FCA, Souza CHB, Faria JAF, Saad SMI (2009) Probiotic cheese: health benefits, technological and stability aspects. Trends Food Sci Technol 20:344–354

    Article  Google Scholar 

  12. Cruz AG, Antunes AEC, Souza ALOP, Faria JAF, Saad SMI (2009) Ice-cream as a probiotic food carrier. Food Res Int 42:1233–1239

    Article  Google Scholar 

  13. Ranadheera RDCS, Baines SK, Adams MC (2010) Importance of food in probiotic efficacy. Food Res Int 43:1–7

    Article  CAS  Google Scholar 

  14. Schillinger U, Guigas C, Holzapfel WH (2005) In vitro adherence and other properties of lactobacilli used in probiotic yoghurt-like products. Int Dairy J 15:1289–1297

    Article  CAS  Google Scholar 

  15. 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. Int J Food Microbiol 126:57–64

    Article  CAS  Google Scholar 

  16. Moraes PM, Perin LM, Todorov SD, Silva A, Franco BDGM, Nero LA (2012) Bacteriocinogenic and virulence potential of Enterococcus isolates obtained from raw milk and cheese. J Appl Microbiol 113:318–328

    Article  CAS  Google Scholar 

  17. Todorov SD, Furtado DN, Saad SMI, Tome E, Franco BDGM (2011) Potential beneficial properties of bacteriocin-producing lactic acid bacteria isolated from smoked salmon. J Appl Microbiol 110:971–986

    Article  Google Scholar 

  18. Grzéskowiak L, Collado MC, Salminen S (2012) Evaluation of aggregation abilities between commensal fish bacteria and pathogens. Aquaculture 356:412–414

    Article  Google Scholar 

  19. Schar-Zammaretti P, Ubbink J (2003) The cell wall of lactic acid bacteria: surface constituents and macromolecular conformations. Biophys J 85:4076–4409

    Article  Google Scholar 

  20. Kleerebezem M, Hols P, Bernard E, Rolain T, Zhou M, Siezen RJ, Bron PA (2010) The extracellular biology of the lactobacilli. FEMS Microbiol Rev 34:199–230

    Article  CAS  Google Scholar 

  21. Duary RK, Batish VK, Grover S (2012) Relative gene expression of bile salt hydrolase and surface proteins in two putative indigenous Lactobacillus plantarum strains under in vitro gut conditions. Mol Biol Rep 39:2541–2552

    Article  CAS  Google Scholar 

  22. Martin-Platero AM, Valdivia E, Maqueda M, Martinez-Bueno M (2009) Characterization and safety evaluation of enterococci isolated from Spanish goats’ milk cheese. Int J Food Microbiol 132:24–32

    Article  CAS  Google Scholar 

  23. De Las Rivas B, Marcobal A, Muñoz R (2005) Improved multiplex-PCR method for the simultaneous detection of food bacteria producing biogenic amines. FEMS Microbiol Lett 244:367–372

    Article  Google Scholar 

  24. Vankerckhoven V, Van Autgaerden T, Vael C, Lammens C, Chapelle S, Rossi R, Jabe D, Goossens H (2004) Development of a multiplex PCR for the detection of asa1, gelE, cylA, esp, and hyl genes in enterococci and survey for virulence determinants among European hospital isolates of Enterococcus faecium. J Clin Microbiol 42:4473–4479

    Article  CAS  Google Scholar 

  25. Russo P, Fernández de Palencia P, Romanao A, Fernández M, Lucas P, Spano G, López P (2012) Biogenic amine production by the wine Lactobacillus brevis IOEB 9809 in systems that partially mimic the gastrointestinal tract stress. BMC Microbiol 12:247–257

    Article  CAS  Google Scholar 

  26. Spano G, Russo P, Lonvaud-Funel A, Lucas P, Alexandre H, Grandvalet C, Coton E, Coton M, Barnavon L, Bach B, Rattray F, Bunte A, Magni C, Ladero V, Alvarez M, Fernández M, Lópes P, Fernández de Palencia P, Corbí A, Trip H, Lolkema J (2010) Biogenic amines in fermented foods. Eur J Clin Nutr 64:95–100

    Article  Google Scholar 

  27. Turchi B, Mancini S, Frantini F, Pedonese F, Nuvoloni R, Bertelloni F, Ebani VV, Cerri D (2013) Preliminary evaluation of probiotic potential of Lactobacillus plantarum strains isolated from Italian food products. World J Microbiol Biotechnol 29:1913–1922

    Article  Google Scholar 

  28. Silva LF (2010). Identificação e Caracterização da microbiota lática isolada de queijo mussarela de búfala [Identification and characterization of lactic acid bacteria isolated from water buffalo Mozzarella cheese]. Dissertation, São Paulo State University

  29. Jeronymo-Ceneviva (2013). Avaliação do potencial probiótico de bactérias acidoláticas produtoras de substância antimicrobiana isoladas de mussarela de búfala. [Evaluation of probiotic potential of bacteriocin producer lactic acid bacteria isolated from water buffalo mozzarella cheese]. Dissertation, São Paulo State University

  30. Buriti FCA, Castro IA, Saad SMI (2010) Viability of Lactobacillus acidophilus in synbiotic guava mousses and its survival under in vitro simulated gastrointestinal conditions. Int J Food Microbiol 137:121–129

    Article  CAS  Google Scholar 

  31. Todorov SD, Botes M, Guigas C, Schillinger U, Wiid I, Wachsman MB, Holzapfel WH, Dicks LM (2008) Boza, a natural source of probiotic lactic acid bacteria. J Appl Microbiol 104:465–477

    CAS  Google Scholar 

  32. Carvalho KG, Kruger MF, Furtado DN, Todorov SD, Franco BDGM (2009) Evaluation of the role of environmental factors in the human gastrointestinal tract on the behaviour of probiotic cultures Lactobacillus casei Shirota and Lactobacillus casei LC01 by the use of semi-dynamic in vitro model. Annals Microbiol 59:439–445

    Article  Google Scholar 

  33. Vinderola CG, Reinheimer JA (2003) Lactic acid starter and probiotic bacteria: a comparative ‘‘in vitro’’ study of probiotic characteristics and biological barrier resistance. Food Res Int 36:895–904

    Article  CAS  Google Scholar 

  34. Ji Y, Kima H, Park H, Lee J, Lee H, Shin H, Kim B, Franz CMAP, Holzapfel WH (2013) Functionality and safety of lactic bacterial strains from Korean kimchi. Food Control 31:467–473

    Article  CAS  Google Scholar 

  35. Bedani R, Rossi E, Saad S (2013) Impact of inulin and okara on Lactobacillus acidophilus La-5 and Bifidobacterium animalis Bb-12 viability in a fermented soy product and probiotic survival under in vitro simulated gastrointestinal conditions. Food Microbiol 34:382–389

    Article  CAS  Google Scholar 

  36. Senaka Ranadheera S, Evans CA, Adams MC, Baines SK (2012) Probiotic viability and physico-chemical and sensory properties of plain and stirred fruit yogurts made from goat’s milk. Food Chem 135:1411–1418

    Article  CAS  Google Scholar 

  37. Ross S, Jonsson H (2002) A high-molecular mass cell-surface protein from Lactobacillus reuteri 1063 adheres to mucus components. Microbiology 148:433–442

    Google Scholar 

  38. Taheri HR, Moravej H, Tabndeh F, Zaghari M, Schivazad M (2009) Screening of lactic acid bacteria toward their selection as a source of chicken probiotic. Poult Sci 88:1586–1593

    Article  CAS  Google Scholar 

  39. Todorov SD, Prévost H, Lebois M, Dousset X, LeBlanc JG, Franco BDGM (2011) Bacteriocinogenic Lactobacillus plantarum ST16 Pa isolated from papaya (Carica papaya)—From isolation to application: Characterization of a bacteriocin. Food Res Int 44:1351–1363

    Article  CAS  Google Scholar 

  40. Dhanani AS, Gaudana SB, Bagchi T (2011) The ability of Lactobacillus adhesin EF-Tu to interfere with pathogen adhesion. Eur Food Res Technol 232:777–785

    Article  CAS  Google Scholar 

  41. Granato D, Bergonzelli GE, Pridmore RD, Marvin L, Rouvet M, Corthesy-Theulaz IE (2004) Cell surface-associated elongation factor Tu mediates the attachment of Lactobacillus johnsonii NCC533 (La1) to human intestinal cells and mucins. Infect Immun 72:2160–2169

    Article  CAS  Google Scholar 

  42. Todorov SD, Dicks LMT (2008) Evaluation of lactic acid bacteria from kefir, molasses and olive brine as possible probiotics based on physiological properties. Ann Microbiol 58:661–670

    Article  Google Scholar 

  43. Juers DH, Matthews BW, Huber R (2012) LacZ b-galactosidase: Structure and function of an enzyme of historical and molecular biological importance. Protein Sci 21:1792–1807

    Article  CAS  Google Scholar 

  44. Almeida CC, Lorena SL, Pavan CR, Akasaka HM, Mesquita MA (2012) Beneficial effects of long-term consumption of a probiotic combination of Lactobacillus casei Shirota and Bifidobacterium breve Yakult may persist after suspension of therapy in lactose-intolerant patients. Nutr Clin Pract 27:247–251

    Article  Google Scholar 

  45. Labayen I, Forga L, Gonzalez A, Lenoir-Wijnkoop I, Martínez JA (2001) Relationship between lactose digestion, gastrointestinal transit time and symptoms in lactose malabsorbers after dairy consumption. Aliment Pharmacol Ther 15:543–549

    Article  CAS  Google Scholar 

  46. Todorov SD, Furtado DN, Saad SMI, Franco BDGM (2011) Bacteriocin production and resistance to drugs are advantageous features for Lactobacillus acidophilus La-14, a potencial probiotic strain. New Microbiol 34:357–370

    CAS  Google Scholar 

  47. Botes M, Loos B, Van Reenen CA, Dicks LMT (2008) Adhesion of the probiotic strains Enterococcus mundtii ST4SA and Lactobacillus platarum 423 to Caco-2 cells under conditions simulating the intestinal tract, and in the presence of antibiotics and anti-inflammatory medicaments. Arch Microbiol 190:573–584

    Article  CAS  Google Scholar 

  48. Todorov SD, Botes M, Danova ST, Dicks LMT (2007) Probiotic properties of Lactococcus lactis ssp. lactis HV219, isolated from human vaginal secretions. J Appl Microbiol 103:629–639

    Article  CAS  Google Scholar 

  49. Kastner S, Perreten V, Bleuler H, Hungenschmidt G, Lacroix C, Meile L (2006) Antibiotic susceptibility patterns and resistance genes of starter cultures and probiotic bacteria used in food. Syst Appl Microbiol 29:145–155

    Article  CAS  Google Scholar 

  50. Hummel A, Holzapfel WH, Franz CMAP (2007) Characterization and transfer of antibiotic resistance genes from enterococci isolated from food. Syst Appl Microbiol 30:1–7

    Article  CAS  Google Scholar 

  51. Hemme D, Foucaud-Scheunemann C (2004) Leuconostoc, characteristics, use in dairy technology and prospects in functional foods. Int Dairy J 14:467–494

    Article  Google Scholar 

  52. Rosenblatt-Farrell N (2009) The landscape of antibiotic resistance. Environ Health Perspect 117:245–250

    Article  Google Scholar 

  53. Dicks LM, Fraser T, Doeschate K, Van Reenen CA (2009) Lactic acid bacteria population in children diagnosed with human immunodeficiency virus. J Paediatr Child Health 45:567–572

    Article  Google Scholar 

  54. Capita R, Alonso-Calleja C (2013) Antibiotic-resistant bacteria: a challenge for the food industry. Crit Rev Food Sci Nut 53:11–48

    Article  CAS  Google Scholar 

  55. Salyers AA, Gupta A, Wang Y (2004) Human intestinal bacteria as reservoirs for antibiotic resistance genes. Trends Microbiol 12:412–416

    Article  CAS  Google Scholar 

  56. Gevers D, Huys G, Swings J (2003) In vitro conjugal transfer of tetracycline resistance from Lactobacillus isolates to other Gram-positive bacteria. FEMS Microbiol Lett 225:125–130

    Article  CAS  Google Scholar 

  57. Jacobsen L, Wilcks A, Hammer K, Huys G, Gevers D, Andersen SR (2007) Horizontal transfer of tet(M) and erm(B) resistance plasmids from food strains of Lactobacillus plantarum to Enterococcus faecalis JH2-2 in the gastrointestinal tract of gnotobiotic rats. FEMS Microbiol Ecol 59:158–166

    Article  CAS  Google Scholar 

  58. Hwanhlem N, Biscola V, El-Ghaish S, Jaffrès E, Dousset X, Haertlé T, Kittikun AH, Chobert JC (2013) Bacteriocin-producing lactic acid bacteria isolated from mangrove forests in Southern Thailand as potential bio-control agents: Purification and characterization of bacteriocin produced by Lactococcus lactis subsp. lactis KT2W2L. Probiotics Antimicrob Proteins 5(4):264–278

    Article  CAS  Google Scholar 

  59. Ahmadova A, Todorov SD, Hadji-Sfaxi I, Choiset Y, Rabesona H, Messaoudi S, Kuliyev A, Franco BD, Chobert JM, Haertlé T (2013) Antimicrobial and antifungal activities of Lactobacillus curvatus strain isolated from homemade Azerbaijani cheese. Anaerobe 20:42–49

    Article  CAS  Google Scholar 

  60. Ribeiro SC, Coelho MC, Todorov SD, Franco BDGM, Dapkevicius MLE, Silva CCG (2014) Technological properties of bacteriocin-producing lactic acid bactéria isolated from Pico cheese an artisanal cow´s milk cheese. J Appl Microbiol 116:573–585

    Article  CAS  Google Scholar 

  61. D’Aimmo MR, Modesto M, Biavati B (2007) Antibiotic resistance of lactic acid bacteria and Bifidobacterium spp. isolated from dairy and pharmaceutical products. Int J Food Microbiol 115:35–42

    Article  Google Scholar 

  62. Klein G (2011) Antibiotic resistance and molecular characterization of probiotic and clinical Lactobacillus strains in relation to safety aspects of probiotics. Foodborne Pathog Dis 8:267–281

    Article  CAS  Google Scholar 

  63. Mathur S, Singh R (2005) Antibiotic resistance in food lactic acid bacteria—a review. Int J Food Microbiol 105:281–295

    Article  CAS  Google Scholar 

  64. Cañas PMI, Alonso SG, Pérez PR, Prieto SS, Romero EG, Herreros MLLP (2009) Biogenic amine production by Oenococcus oeni isolates from malolactic fermentation of Tempranillo wine. J Food Protect 72:907–910

    Google Scholar 

  65. Romano A, Trip H, Lolkema JS, Lucas PMA (2013) Three-component lysine/ornithine decarboxylation system in Lactobacillus saerimneri 30a. J Bacteriol 195:1249–1254

    Article  CAS  Google Scholar 

  66. Cotton M, Romano A, Spano G, Ziegler K, Vetrana C, Desmarais C, Lonvaud-Funes A, Lucas P, Cotto E (2010) Occurrence of biogenic amine-forming lactic acid bacteria in wine and cider. Food Microbiol 27:1078–1085

    Article  Google Scholar 

Download references

Acknowledgments

The authors are grateful to the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Brazil, Projects No. 2010/09302-1 and 2011/11922-0), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil) for the financial support, and to Dr. Elisabetta Tome from Universidad Central de Venezuela, Caracas, Venezuela, for providing Leuc. mesenteroides subsp. mesenteroides UCV10CET strain (CDCH Project No PG-03.7371.2008).

Conflict of interest

The authors declare that there is no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ana Lúcia B. Penna.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jeronymo-Ceneviva, A.B., de Paula, A.T., Silva, L.F. et al. Probiotic Properties of Lactic Acid Bacteria Isolated from Water-Buffalo Mozzarella Cheese. Probiotics & Antimicro. Prot. 6, 141–156 (2014). https://doi.org/10.1007/s12602-014-9166-2

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-014-9166-2

Keywords

Navigation