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Probiotics and Antimicrobial Proteins

, Volume 11, Issue 1, pp 74–84 | Cite as

In Vitro Characterization of Lactic Acid Bacteria Isolated from Bovine Milk as Potential Probiotic Strains to Prevent Bovine Mastitis

  • Matías S. PellegrinoEmail author
  • Ignacio D. Frola
  • Berardo Natanael
  • Dino Gobelli
  • María E.F. Nader-Macias
  • Cristina I. Bogni
Article

Abstract

Bovine mastitis causes economic losses on dairy farms worldwide. Lactic acid bacteria (LAB) in animal health are an alternative tool to avoid antibiotic therapy on the prevention of bovine mastitis. In previous studies, 12 LAB isolated from bovine milk were selected taking into account some of the following characteristics: hydrophobicity, auto aggregative capability, inhibition of indicator pathogens, hydrogen peroxide, and capsular polysaccharide production. These LAB were considered because of their beneficial properties. In this work, we also analyzed the antimicrobial activity and the co-aggregation against mastitis causing bacteria, auto-inhibition, adhesion to bovine teat canal epithelial cells (BTCEC), and growth kinetic curves for the 12 LAB. Two of them, Lactococcus lactis subsp. lactis CRL 1655 and Lactobacillus perolens CRL 1724, were selected because they had an interesting pattern of adhesion to BTEC, the inhibition of pathogens and the co-aggregation with the 100% of the assayed pathogens. They showed a predictable difference in the PFGE genomic pattern bands. The kinetic growth of these two strains was similar between them and with the rest of the assayed LAB. The strains selected in the present study showed indispensable characteristics for their inclusion in a probiotic formulation to be used at dry-off period for the prevention of bovine mastitis.

Keywords

Lactic acid bacteria Probiotic Bovine mastitis Prevention 

Notes

Acknowledgements

These are the results obtained from the project called “Design of a probiotic product for bovine mastitis prevention” signed between Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and Universidad Nacional de Río Cuarto. M. Pellegrino and M.E.F. Nader-Macías are career investigators of the CONICET, and N. Berardo is recipient of a fellowship from CONICET.

Funding Information

This work was supported by grants of Secretaría de Ciencia y Técnica, Universidad Nacional de Río Cuarto (SECYT-UNRC) and Agencia Nacional de Promoción Científica y Tecnológica (ANPCYT- PICT 543).

Compliance with Ethical Standards

This article does not contain any studies with human or animal subjects.

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Bogni C, Odierno L, Raspanti C, Giraudo J, Larriestra A, Reinoso E et al (2011) War against mastitis: current concepts on controlling bovine mastitis pathogens. In: Méndez-Vilas A (ed) Science against microbial pathogens: communicating current research and technological advances. FORMATEX Research Center Inc., Spain, pp 483–494Google Scholar
  2. 2.
    Schukken H, Günthe J, Fitzpatrick J, Fontaine MC, Goetze L, Holst O et al (2011) Host-response patterns of intramammary infections in dairy cows. Vet Immunol Immunop 144(3):270–289.  https://doi.org/10.1016/j.vetimm.2011.08.022 CrossRefGoogle Scholar
  3. 3.
    De Vliegher S, Fox L, Piepers S, McDougall S, Barkema HW (2012) Invited review: mastitis in dairy heifers: nature of the disease, potential impact, prevention, and control. J Dairy Sci 95(3):1025–1040.  https://doi.org/10.3168/jds.2010-4074 CrossRefGoogle Scholar
  4. 4.
    Dieser S, Vissio C, Lasagno M, Bogni CI, Larriestra AJ, Odierno LM (2014) Prevalence of pathogens causing subclinical mastitis in Argentinean dairy herds. Pak Vet J 34:124–126Google Scholar
  5. 5.
    Petrovski K, Grinberg A, Williamson N, Abdalla ME, Lopez-Villalobos N, Parkinson TJ et al (2015) Susceptibility to antimicrobials of mastitis-causing Staphylococcus aureus, Streptococcus uberis and Str. dysgalactiae from New Zealand and the USA as assessed by the disk diffusion test. Aust Vet J 93(7):227–233.  https://doi.org/10.1111/avj.12340 CrossRefGoogle Scholar
  6. 6.
    Raspanti C, Bonetto C, Vissio C, Pellegrino MS, Reinoso EB, Dieser SA et al (2016) Prevalence and antibiotic susceptibility of coagulase-negative Staphylococcus species from bovine subclinical mastitis in dairy herds in the central region of Argentina. Rev Arg Microbiol 48(1):50–56Google Scholar
  7. 7.
    Thompson-Crispi K, Atalla H, Miglior F, Mallard B (2014) Bovine mastitis: frontiers in immunogenetics. Front Immunol 5:493CrossRefGoogle Scholar
  8. 8.
    Dua K (2001) Incidence, etiology and estimated loss due to mastitis in India—an update. Indian Dairyman 53:41–48Google Scholar
  9. 9.
    Halasa T, Nielen M, De Roos A, Van Hoorne R, De Jong G, Lam TJGM et al (2009) Production loss due to new subclinical mastitis in Dutch dairy cows estimated with a test-day model. J Dairy Sci 92(2):599–606.  https://doi.org/10.3168/jds.2008-1564 CrossRefGoogle Scholar
  10. 10.
    Vissio C, Dieser S, Agnelli H, Odierno LM, Larriestra A (2014) Accuracy of the composite somatic cell count to detect intra-mammary infection in dairy cows using latent class analysis. Prev Vet Med 113(4):547–555.  https://doi.org/10.1016/j.prevetmed.2013.11.016 CrossRefGoogle Scholar
  11. 11.
    Bradley A (2002) Bovine mastitis: an evolving disease. Vet J 164(2):116–128.  https://doi.org/10.1053/tvjl.2002.0724 CrossRefGoogle Scholar
  12. 12.
    Dufour S, Dohoo I (2012) Monitoring dry period intramammary infection incidence and elimination rates using somatic cell count measurements. J Dairy Sci 95(12):7173–7185.  https://doi.org/10.3168/jds.2012-5839 CrossRefGoogle Scholar
  13. 13.
    McDougall S, Bryan M, Tiddy R (2009) Effect of treatment with the nonsteroidal antiinflammatory meloxicam on milk production, somatic cell count, probability of re-treatment, and culling of dairy cows with mild clinical mastitis. J Dairy Sci 92(9):4421–4431.  https://doi.org/10.3168/jds.2009-2284 CrossRefGoogle Scholar
  14. 14.
    Song E, Yu M, Wang Y, Hu W, Cheng D, Swihart MT, Song Y (2015) Multi-color quantum dot-based fluorescence immunoassay array for simultaneous visual detection of multiple antibiotic residues in milk. Biosens Bioelectron 72:320–325.  https://doi.org/10.1016/j.bios.2015.05.018 CrossRefGoogle Scholar
  15. 15.
    Wang D, Wang Z, Yan Z, Wu J, Ali T, Li J, Lv Y, Han B (2015) Bovine mastitis Staphylococcus aureus: antibiotic susceptibility profile, resistance genes and molecular typing of methicillin-resistant and methicillin-sensitive strains in China. Infect Genet Evol 31:9–16.  https://doi.org/10.1016/j.meegid.2014.12.039 CrossRefGoogle Scholar
  16. 16.
    FAO, WHO (2015) Guidelines for the evaluation of probiotics in food. Food and Agriculture Organization of the United Nations and World Health Organization Working Group, GenevaGoogle Scholar
  17. 17.
    Nader-Macías MEF, Bogni C, Sesma F, Espeche MC, Pellegrino M, Saavedra L et al (2011) Alternative approaches for the prevention of bovine mastitis. In: Bitterlich A, Fisch S (eds) Probiotics, bioactive compounds and vaccines: bioactives compounds. Nova Science Publishers Inc., New York, pp 1–34Google Scholar
  18. 18.
    Walsh M, Gardiner G, Hart O, Lawlor PG, Daly M, Lynch B et al (2008) Predominance of a bacteriocin-producing Lactobacillus salivarius component of a five-strain probiotic in the porcine ileum and effects on host immune phenotype. FEMS Microbiol Ecol 64(2):317–327.  https://doi.org/10.1111/j.1574-6941.2008.00454.x CrossRefGoogle Scholar
  19. 19.
    Ryan M, Flynn J, Hill C, Ross RP, Meaney WJ (1999a) The natural food grade inhibitor lacticin 3147 can prevent mastitis in non-lactating dairy cows. J. Dairy Sci 82(12):2625–2631.  https://doi.org/10.3168/jds.S0022-0302(99)75519-0 CrossRefGoogle Scholar
  20. 20.
    Twomey D, Wheelock A, Flynn J, Meaney WJ, Hill C, Ross R (2000) Protection against Staphylococcus aureus mastitis in dairy cows using a bismuth-based teat seal containing the bacteriocin, lacticin 3147. J Dairy Sci 83(9):1981–1988.  https://doi.org/10.3168/jds.S0022-0302(00)75075-2 CrossRefGoogle Scholar
  21. 21.
    Crispie F, Alonso-Gómez M, O’Loughlin C, Klostermann K, Flynn J, Arkins S et al (2008) Intramammary infusion of a live culture for treatment of bovine mastitis: effect of live lactococci on the mammary immune response. J Dairy Res 75(3):374–384.  https://doi.org/10.1017/S0022029908003385 CrossRefGoogle Scholar
  22. 22.
    Klostermann K, Crispie F, Flynn J, Ross RP, Hill C, Meaney W (2008) Intramammary infusion of a live culture of Lactococcus lactis for treatment of bovine mastitis: comparison with antibiotic treatment in field trials. J Dairy Res 75(3):365–373.  https://doi.org/10.1017/S0022029908003373 CrossRefGoogle Scholar
  23. 23.
    Bouchard D, Seridan B, Saraoui T, Rault L, Germon P, Gonzalez-Moreno C et al (2015) Lactic acid bacteria isolated from bovine mammary microbiota: potential allies against bovine mastitis. PLoS One 10(12):e0144831.  https://doi.org/10.1371/journal.pone.0144831 CrossRefGoogle Scholar
  24. 24.
    Giannino M, Aliprandi M, Feligini M, Vanoni L, Brasca M, Fracchetti F (2009) A DNA array based assay for the characterization of microbial community in raw milk. J Microbiol meth 78(2):181–188.  https://doi.org/10.1016/j.mimet.2009.05.015 CrossRefGoogle Scholar
  25. 25.
    Espeche M, Otero M, Sesma F, Nader-Macias MEF (2009) Screening of surface properties and antagonistic substances production by lactic acid bacteria isolated from the mammary gland of healthy and mastitic cows. Vet Microbiol 135(3):346–357.  https://doi.org/10.1016/j.vetmic.2008.09.078 CrossRefGoogle Scholar
  26. 26.
    Espeche MC, Pellegrino M, Frola I, Larriestra A, Bogni C, Nader-Macías MEF (2012) Lactic acid bacteria from raw milk as potentially beneficial strains to prevent bovine mastitis. Anaerobe 18(1):103–109.  https://doi.org/10.1016/j.anaerobe.2012.01.002 CrossRefGoogle Scholar
  27. 27.
    Frola I, Pellegrino M, Espeche MC, Giraudo JA, Nader-Macias MEF, Bogni C (2011) Effects of intramammary inoculation of lactobacillus perolens CRL 1724 in lactating cows udders. J Dairy Res 79(1):84–92.  https://doi.org/10.1017/S0022029911000835 CrossRefGoogle Scholar
  28. 28.
    Frola I, Pellegrino M, Espeche M, Giraudo JA, Nader-Macias MEF, Bogni CI (2012) Effects of intramammary inoculation of Lactobacillus perolens CRL 1724 in lactating cows’ udders. J Dairy Res 79(01):84–92.  https://doi.org/10.1017/S0022029911000835 CrossRefGoogle Scholar
  29. 29.
    Hütt P, Shchepetova J, Lõivukene K, Kullisaar T, Mikelsaar M (2006) Antagonistic activity of probiotic lactobacilli and bifidobacteria against entero- and uropathogens. J Appl Microb 100(6):1324–1332.  https://doi.org/10.1111/j.1365-2672.2006.02857.x CrossRefGoogle Scholar
  30. 30.
    Reid G, Mac Groarty J, Chow A, Chow AW, Bruce AW, Eisen A et al (1990) Coaggregation of urogenital bacteria in vitro and in vivo. Curr Microbiol 20(1):47–52.  https://doi.org/10.1007/BF02094024 CrossRefGoogle Scholar
  31. 31.
    Otero M, Nader-Macías MEF (2007) Lactobacillus adhesion to epithelial cells from bovine vagina. In: Méndez-Vilas A (ed) Communicating current research and educational topics and trends in applied microbiology, FORMATEX Research Center Inc., Spain, pp 749–757Google Scholar
  32. 32.
    Malthus TR (1826) An essay on the principle of population. 6th. John Murray, LondonGoogle Scholar
  33. 33.
    Tanskanen E, Tulloch D, Hillier A, Davidson B (1990) Pulsed-field gel electrophoresis of SmaI digests of lactococcal genomic DNA, a novel method of strain identification. Appl Environ Microb 56(10):3105–3111Google Scholar
  34. 34.
    Pellegrino M, Rodriguez N, Vivas A, Giraudo J, Bogni C (2016) Staphylococcus aureus avirulent mutant vaccine induces humoral and cellular immune responses on pregnant heifers. Vaccine 34(29):3356–3362.  https://doi.org/10.1016/j.vaccine.2016.05.014 CrossRefGoogle Scholar
  35. 35.
    Perea-Vélez M, Hermans K, Verhoeven T, Lebeer SE, Vanderleyden J, De Keersmaecker SCJ (2007) Identification and characterization of starter lactic acid bacteria and probiotics from Columbian dairy products. J appl microb 103(3):666–674.  https://doi.org/10.1111/j.1365-2672.2007.03294.x CrossRefGoogle Scholar
  36. 36.
    Juárez Tomás M, Ocaña V, Wies B, Nader-Macías MEF (2003) Growth and lactic production by vaginal Lactobacillus acidophilus CRL 1259, and inhibition of uropathogenic Escherichia coli. J Med Microbiol 52(12):1117–1124.  https://doi.org/10.1099/jmm.0.05155-0 CrossRefGoogle Scholar
  37. 37.
    Maršálková S, Cizek M, Vasil M, Bomba A, Nad P, Datelinka I et al (2003) Testing two Lactobacillus plantarum and Lactobacillus acidophilus strains for their suitability as a lipoid probiotic. Berl Munch Tierarztl 117(3–4):145–147Google Scholar
  38. 38.
    Çon A, Gökalp H (2000) Production of bacteriocin-like metabolites by lactic acid cultures isolated from sucuk samples. Meat Sci 55(1):89–96.  https://doi.org/10.1016/S0309-1740(99)00129-1 CrossRefGoogle Scholar
  39. 39.
    Saarela M, Mogensen G, Fondén R, Mättö J, Mattila-Sandholm T (2000) Probiotic bacteria: safety, functional and technological properties. J Biotechnol 84(3):197–215.  https://doi.org/10.1016/S0168-1656(00)00375-8 CrossRefGoogle Scholar
  40. 40.
    Ouwehand A, Salminen S, Isolauri E (2002) Probiotics: an overview of beneficial effects. A Van Leeuw J Microb 82(1/4):279–289.  https://doi.org/10.1023/A:1020620607611 CrossRefGoogle Scholar
  41. 41.
    Gueimonde M, Salminen S (2006) New methods for selecting and evaluating probiotics. Dig Liver Dis 38:S242–S247.  https://doi.org/10.1016/S1590-8658(07)60003-6 CrossRefGoogle Scholar
  42. 42.
    Soleimani N, Kermanshahi R, Yakhchali B, Sattari T (2010) Antagonistic activity of probiotic lactobacilli against Staphylococcus aureus isolated from bovine mastitis. Afric J Microbiol Res 4(20):2169–2173Google Scholar
  43. 43.
    Reid G, McGroarty J, Angotti R, Cook RL (1988) Lactobacillus inhibitor production against Escherichia coli and co-aggregation ability with uropathogens. Can J Microbol 34(3):344–351.  https://doi.org/10.1139/m88-063 CrossRefGoogle Scholar
  44. 44.
    Boris S, Suarez J, Velazquez F, Barbés C (1998) Adherence of human lactobacilli to vaginal epithelial cells and interaction with uropathogens. Infect Immun 66(5):1985–1989Google Scholar
  45. 45.
    Havenaar R, Brink BT, Huis In’t Veld J (1992) Selection of strains for probiotics use. In: Fuller R (ed) Probiotics. The scientific basis. Chapman and Hall Inc., London, pp 209–223Google Scholar
  46. 46.
    Reid G, Jass J, Sebulsky M, McCormick J (2003) Potential use of probiotics in clinical practice. Clin Microbial Rev 16:652–658CrossRefGoogle Scholar
  47. 47.
    Ocaña V, Nader-Macías MEF (2001) Adhesión of Lactobacillus vaginal strains with probiotic properties to vaginal epithelial cells. Biocell 25(3):265–273Google Scholar
  48. 48.
    Diepers A, Krömker V, Zinke C, Wente N, Pan L, Paulsen K et al (2017) In vitro ability of lactic acid bacteria to inhibit mastitis-causing pathogens. Sust Chem Pharm 5:84–92Google Scholar
  49. 49.
    Wadstroum T, Andersson K, Sydow M, Axelsson L, Lindgren S, Gullmar B (1987) Surface properties of lactobacilli isolated from the small intestine of pigs. J Appl Bacteriol 62(6):513–520.  https://doi.org/10.1111/j.1365-2672.1987.tb02683.x CrossRefGoogle Scholar
  50. 50.
    Henriksson A, Szewzyk R, Conway P (1991) Characteristics of the adhesive determinants of Lactobacillus fermentum 104. Appl Environ Microb 57(2):499–502Google Scholar
  51. 51.
    Frece J, Kos B, Svetec I, Zgaga Z, Mrša V, Šušković J (2005) Importance of S-layer proteins in probiotic activity of Lactobacillus acidophilus M92. J Appl Microb 98(2):285–292.  https://doi.org/10.1111/j.1365-2672.2004.02473.x CrossRefGoogle Scholar
  52. 52.
    Fuller R (1975) Nature of the determinant responsible for the adhesion of lactobacilli to chicken crop epithelial cells. Microbiology 87(2):245–250Google Scholar
  53. 53.
    Siezen R, Bayjanov J, Felis G, van der Sijde M, Starrenburg M, Molenaar D et al (2011) Genome-scale diversity and niche adaptation analysis of Lactococcus lactis by comparative genome hybridization using multi-strain arrays. Microb Biotechnol 4(3):383–402.  https://doi.org/10.1111/j.1751-7915.2011.00247.x CrossRefGoogle Scholar
  54. 54.
    Sun Z, Harris H, McCann A, Guo C, Argimo’n S, Zhang W et al (2015) Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera. Nat Commun 6:8322.  https://doi.org/10.1038/ncomms9322 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Matías S. Pellegrino
    • 1
    • 2
    Email author
  • Ignacio D. Frola
    • 1
  • Berardo Natanael
    • 1
    • 2
  • Dino Gobelli
    • 1
  • María E.F. Nader-Macias
    • 2
    • 3
  • Cristina I. Bogni
    • 1
  1. 1.Departamento de Microbiología e Inmunología, Facultad de Ciencias Exactas, Físico-Químicas y NaturalesUniversidad Nacional de Río CuartoCordobaArgentina
  2. 2.Member of Consejo Nacional de Investigaciones Científicas y Tecnológicas (CIC-CONICET)Buenos AiresArgentina
  3. 3.Departamento de Microbiología PreventivaCERELA-CONICET (Centro de Referencia para Lactobacilos-Consejo Nacional de Investigaciones Científicas y Técnicas de Argentina)San Miguel de TucumanArgentina

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