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Efficacy of a Ruminal Bacteriocin Against Pure and Mixed Cultures of Bovine Mastitis Pathogens

  • Fernanda Godoy-Santos
  • Marcelo S. Pinto
  • Ana A. T. Barbosa
  • Maria A. V. P. Brito
  • Hilário C. MantovaniEmail author
Original research article
  • 26 Downloads

Abstract

Bacteriocins have been suggested as an alternative to conventional antibiotics for the prevention and treatment of mastitis infections. Predominant bacteria associated with bovine mastitis (n = 276 isolates) were evaluated for their susceptibility to bovicin HC5, a ruminal bacteriocin produced by Streptococcus equinus HC5. Bovicin HC5 inhibited most (> 80%) of the streptococcal and staphylococcal strains tested, but showed no effect against Escherichia coli strains. Susceptibility and resistance testing indicated that approximately 95% of the S. aureus strains were inhibited by concentrations of bovicin HC5 varying from 40 to 2560 AU ml−1. Bovicin HC5 (62.50 AU ml−1) also inhibited the growth of aerobic and anaerobic mixed cultures of S. aureus and S. agalactiae, but the combination with 0.25 mmol l−1 of EDTA showed even greater bactericidal activity. These results demonstrate that bovicin HC5 is effective against the most prevalent pathogens found in contagious udder infections and could complement the use antibiotics in mastitis prophylaxis and therapy.

Keywords

Bacteriocins Bovicin HC5 Mastitis Staphylococcus Streptococcus 

Notes

Acknowledgements

This research has been supported by the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG, Belo Horizonte, Brazil), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES; Brasília, Brazil) and Instituto Nacional de Ciência e Tecnologia de Ciência Animal (INCT -CA, Viçosa, Brazil). F.G.S. and A.A.T.B. were supported by a fellowship from the Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq, Brasília, Brazil.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Jamali H, Barkema HW, Jacques M, Lavallee-Bourget EM, Malouin F, Saini V, Stryhn H, Dufour S (2018) Invited review: incidence, risk factors, and effects of clinical mastitis recurrence in dairy cows. J Dairy Sci 101:4729–4746.  https://doi.org/10.3168/jds.2017-13730 CrossRefGoogle Scholar
  2. 2.
    Klaas IC, Zadoks RN (2018) An update on environmental mastitis: challenging perceptions. Transbound Emerg Dis 65:166–185.  https://doi.org/10.1111/tbed.12704 CrossRefGoogle Scholar
  3. 3.
    Murphy SC, Martin NH, Barbano DM, Wiedmann M (2016) Influence of raw milk quality on processed dairy products: how do raw milk quality test results relate to product quality and yield? J Dairy Sci 99:10128–10149.  https://doi.org/10.3168/jds.2016-11172 CrossRefGoogle Scholar
  4. 4.
    Taponen S, Liski E, Heikkilä AM, Pyörälä S (2017) Factors associated with intramammary infection in dairy cows caused by coagulase-negative staphylococci, Staphylococcus aureus, Streptococcus uberis, Streptococcus dysgalactiae, Corynebacterium bovis, or Escherichia coli. J Dairy Sci 100:493–503.  https://doi.org/10.3168/jds.2016-11465 CrossRefGoogle Scholar
  5. 5.
    Barlow J (2011) Mastitis therapy and antimicrobial susceptibility: a multispecies review with a focus on antibiotic treatment of mastitis in dairy cattle. J Mammary Gland Biol Neoplasia 16:383–407.  https://doi.org/10.1007/s10911-011-9235-z CrossRefGoogle Scholar
  6. 6.
    Oniciuc E-A, Nicolau AI, Hernández M, Rodríguez-Lázaro D (2017) Presence of methicillin-resistant Staphylococcus aureus in the food chain. Trends Food Sci Technol 61:49–59.  https://doi.org/10.1016/j.tifs.2016.12.002 CrossRefGoogle Scholar
  7. 7.
    Ahmad V, Khan MS, Jamal QMS, Alzohairy MA, Al Karaawi MA, Siddiqui MU (2017) Antimicrobial potential of bacteriocins: in therapy, agriculture and food preservation. Int J Antimicrob Agents 49:1–11.  https://doi.org/10.1016/j.ijantimicag.2016.08.016 CrossRefGoogle Scholar
  8. 8.
    Francoz D, Wellemans V, Dupré JP, Karreman HJ, Roy JP, Labelle F, Lacasse P, Dufour S (2017) A systematic review and qualitative analysis of treatments other than conventional antimicrobials for clinical mastitis in dairy cows. J Dairy Sci 100:7751–7770.  https://doi.org/10.3168/jds.2016-12512 CrossRefGoogle Scholar
  9. 9.
    Rea MC, Ross RP, Cotter PD, Hill C (2011) Classification of bacteriocins from Gram-positive bacteria. In: Drider D, Rebuffat S (eds) Prokaryotic antimicrobial peptides. Springer, New York, pp 29–53.  https://doi.org/10.1007/978-1-4419-7692-5_3 CrossRefGoogle Scholar
  10. 10.
    Taylor J, Hirsch A, Mattick ATR (1949) The treatment of bovine streptococcal and staphylococcal mastitis with nisin. Vet Rec 61:197–198.  https://doi.org/10.3168/jds.2007-0153 Google Scholar
  11. 11.
    Ryan MP, Flynn J, Hill C, Ross RP, Meaney WJ (1999) The natural food grade inhibitor, lacticin 3147, reduced the incidence of mastitis after experimental challenge with Streptococcus dysgalactiae in nonlactating dairy cows. J Dairy Sci 82:2625–2631.  https://doi.org/10.3168/jds.S0022-0302(99)75519-0 CrossRefGoogle Scholar
  12. 12.
    Guan R, Wu J-Q, Xu W, Su X-Y, Hu S-H (2017) Efficacy of vaccination and nisin Z treatments to eliminate intramammary Staphylococcus aureus infection in lactating cows. J Zhejiang Univ Sci B 18:360–364.  https://doi.org/10.1631/jzus.B1500222 CrossRefGoogle Scholar
  13. 13.
    Wu J, Hu S, Cao L (2007) Therapeutic effect of nisin Z on subclinical mastitis in lactating cows. Antimicrob Agents Chemother 51:3131–3135.  https://doi.org/10.1128/AAC.00629-07 CrossRefGoogle Scholar
  14. 14.
    Mantovani HC, Kam DK, Ha JK, Russell JB (2001) The antibacterial activity and sensitivity of Streptococcus bovis strains isolated from the rumen of cattle. FEMS Microbiol Ecol 37:223–229.  https://doi.org/10.1111/j.1574-6941.2001.tb00869.x Google Scholar
  15. 15.
    Naghmouchi K, Kheadr E, Lacroix C, Fliss I (2007) Class I/Class IIa bacteriocin cross-resistance phenomenon in Listeria monocytogenes. Food Microbiol 24:718–727.  https://doi.org/10.1016/j.fm.2007.03.012 CrossRefGoogle Scholar
  16. 16.
    Houlihan AJ, Russell JB (2006) Factors affecting the activity of bovicin HC5, a bacteriocin from Streptococcus bovis HC5: release, stability and binding to target bacteria. J Appl Microbiol 100:168–174.  https://doi.org/10.1111/j.1365-2672.2005.02745.x CrossRefGoogle Scholar
  17. 17.
    Houlihan AJ, Mantovani HC, Russell JB (2004) Effect of pH on the activity of bovicin HC5, a bacteriocin from Streptococcus bovis HC5. FEMS Microbiol Lett 231:27–32.  https://doi.org/10.1016/S0378-1097(03)00922-4 CrossRefGoogle Scholar
  18. 18.
    Paiva AD, Breukink E, Mantovani HC (2011) Role of lipid II and membrane thickness in the mechanism of action of the lantibiotic bovicin HC5. Antimicrob Agents Chemother 55:5284–5293.  https://doi.org/10.1128/AAC.00638-11 CrossRefGoogle Scholar
  19. 19.
    Pimentel-Filho NJ, Mantovani HC, Diez-Gonzalez F, Vanetti MCD (2013) Inhibition of Listeria and Staphylococcus aureus by bovicin HC5 and nisin combination in milk. J Agric Sci 5:188.  https://doi.org/10.5539/jas.v5n8p188 Google Scholar
  20. 20.
    Prudencio CV, Mantovani HC, Cecon PR, Vanetti MC (2015) Differences in the antibacterial activity of nisin and bovicin HC5 against Salmonella Typhimurium under different temperature and pH conditions. J Appl Microbiol 118:18–26.  https://doi.org/10.1111/jam.12680 CrossRefGoogle Scholar
  21. 21.
    Brito MAVP, Brito JRF (1999) Diagnóstico microbiológico da mastite. Juiz de Fora, MG: EMBRAPA Gado de Leite. EMBRAPA Gado de Leite Circular Técnica, 55Google Scholar
  22. 22.
    Brito MAVP, Brito JRF, Ribeiro MT, Veiga VM (1999) Padrão de infecção intramamária em rebanhos leiteiros: exame de todos os quartos mamários das vacas em lactação. Arq Bras Med Ver Zoo 51:129–135CrossRefGoogle Scholar
  23. 23.
    Mantovani HC, Russell JB (2003) Inhibition of Listeria monocytogenes by bovicin HC5, a bacteriocin produced by Streptococcus bovis HC5. Int J Food Microbiol 89:77–83.  https://doi.org/10.1016/S0168-1605(03)00110-7 CrossRefGoogle Scholar
  24. 24.
    De Man JC, Rogosa M, Sharpe ME (1960) A medium for the cultivation of lactobacilli. J Appl Microbiol 23:130–135.  https://doi.org/10.1111/j.1365-2672.1960.tb00188.x Google Scholar
  25. 25.
    Lima JR, Ribon Ade O, Russell JB, Mantovani HC (2009) Bovicin HC5 inhibits wasteful amino acid degradation by mixed ruminal bacteria in vitro. FEMS Microbiol Lett 292:78–84.  https://doi.org/10.1111/j.1574-6968.2008.01474.x CrossRefGoogle Scholar
  26. 26.
    Hoover DG, Harlander SK (1993) Screening methods for detecting bacteriocin activity. In: In: Hoover DG, Steenson L.R. (eds) Bacteriocins of lactic acid bacteria. vol Food science and technology. Academic Press, San Diego, pp 23–39Google Scholar
  27. 27.
    Ferri M, Ranucci E, Romagnoli P, Giaccone V (2017) Antimicrobial resistance: a global emerging threat to public health systems. Crit Rev Food Sci Nutr 57:2857–2876.  https://doi.org/10.1080/10408398.2015.1077192 CrossRefGoogle Scholar
  28. 28.
    Ceotto-Vigoder H, Marques SLS, Santos INS, Alves MDB, Barrias ES, Potter A, Alviano DS, Bastos MCF (2016) Nisin and lysostaphin activity against preformed biofilm of Staphylococcus aureus involved in bovine mastitis. J Appl Microbiol 121:101–114.  https://doi.org/10.1111/jam.13136 CrossRefGoogle Scholar
  29. 29.
    Klostermann K, Crispie F, Flynn J, Meaney WJ, Paul Ross R, Hill C (2010) Efficacy of a teat dip containing the bacteriocin lacticin 3147 to eliminate Gram-positive pathogens associated with bovine mastitis. J Dairy Res 77:231–238.  https://doi.org/10.1017/S0022029909990239 CrossRefGoogle Scholar
  30. 30.
    Helander IM, von Wright A, Mattila-Sandholm TM (1997) Potential of lactic acid bacteria and novel antimicrobials against Gram-negative bacteria. Trends Food Sci Technol 8:146–150.  https://doi.org/10.1016/S0924-2244(97)01030-3 CrossRefGoogle Scholar
  31. 31.
    Coelho MLV, Nascimento JdS, Fagundes PC, Madureira DJ, Oliveira SSd, Vasconcelos MAdPB, Freire MdCdB (2007) Activity of staphylococcal bacteriocins against Staphylococcus aureus and Streptococcus agalactiae involved in bovine mastitis. Res Microbiol 158:625–630.  https://doi.org/10.1016/j.resmic.2007.07.002 CrossRefGoogle Scholar
  32. 32.
    Pyörälä S, Taponen S (2009) Coagulase-negative staphylococci-emerging mastitis pathogens. Vet Microbiol 134:3–8.  https://doi.org/10.1016/j.vetmic.2008.09.015 CrossRefGoogle Scholar
  33. 33.
    Persson Waller K, Aspán A, Nyman A, Persson Y, Grönlund Andersson U (2011) CNS species and antimicrobial resistance in clinical and subclinical bovine mastitis. Vet Microbiol 152:112–116.  https://doi.org/10.1016/j.vetmic.2011.04.006 CrossRefGoogle Scholar
  34. 34.
    Taponen S, Nykäsenoja S, Pohjanvirta T, Pitkälä A, Pyörälä S (2016) Species distribution and in vitro antimicrobial susceptibility of coagulase-negative staphylococci isolated from bovine mastitic milk. Acta Vet Scand 58:12.  https://doi.org/10.1186/s13028-016-0193-8 CrossRefGoogle Scholar
  35. 35.
    Srednik ME, Tremblay YDN, Labrie J, Archambault M, Jacques M, Fernández Cirelli A, Gentilini ER (2017) Biofilm formation and antimicrobial resistance genes of coagulase-negative staphylococci isolated from cows with mastitis in Argentina. FEMS Microbiol Lett 364:fnx001.  https://doi.org/10.1093/femsle/fnx001 CrossRefGoogle Scholar
  36. 36.
    Bastos MCF, Coelho MLV, Santos OCS (2015) Resistance to bacteriocins produced by Gram-positive bacteria. Microbiology 161:683–700.  https://doi.org/10.1099/mic.0.082289-0 CrossRefGoogle Scholar
  37. 37.
    Draper LA, Grainger K, Deegan LH, Cotter PD, Hill C, Ross RP (2009) Cross-immunity and immune mimicry as mechanisms of resistance to the lantibiotic lacticin 3147. Mol Microbiol 71:1043–1054.  https://doi.org/10.1111/j.1365-2958.2008.06590.x CrossRefGoogle Scholar
  38. 38.
    Dunnick JK, O’Leary WM (1970) Correlation of bacterial lipid composition with antibiotic resistance. J Bacteriol 101:892–900Google Scholar
  39. 39.
    Kotilainen P, Huovinen P, Eerola E (1991) Application of gas-liquid chromatographic analysis of cellular fatty acids for species identification and typing of coagulase-negative staphylococci. JCM 29:315–322Google Scholar
  40. 40.
    Brinster S, Lamberet G, Staels B, Trieu-Cuot P, Gruss A, Poyart C (2009) Type II fatty acid synthesis is not a suitable antibiotic target for Gram-positive pathogens. Nature 458:83–86.  https://doi.org/10.1038/nature07772 CrossRefGoogle Scholar
  41. 41.
    Nair N, Biswas R, Götz F, Biswas L (2014) Impact of Staphylococcus aureus on pathogenesis in polymicrobial infections. Infect Immun 82:2162–2169.  https://doi.org/10.1128/iai.00059-14 CrossRefGoogle Scholar
  42. 42.
    Giaouris E, Heir E, Desvaux M, Hébraud M, Møretrø T, Langsrud S, Doulgeraki A, Nychas G-J, Kačániová M, Czaczyk K, Ölmez H, Simões M (2015) Intra- and inter-species interactions within biofilms of important foodborne bacterial pathogens. Front Microbiol 6:841.  https://doi.org/10.3389/fmicb.2015.00841 CrossRefGoogle Scholar
  43. 43.
    Burmølle M, Ren D, Bjarnsholt T, Sørensen SJ (2014) Interactions in multispecies biofilms: do they actually matter? Trends Microbiol 22:84–91.  https://doi.org/10.1016/j.tim.2013.12.004 CrossRefGoogle Scholar
  44. 44.
    Amin AS, Hamouda RH, Abdel-All AAA (2011) PCR assays for detecting major pathogens of mastitis in milk samples. WJDFS 6:199–206.  https://doi.org/10.1007/s11250-009-9360-5 Google Scholar
  45. 45.
    Brumfitt W, Salton MR, Hamilton-Miller JM (2002) Nisin, alone and combined with peptidoglycan-modulating antibiotics: activity against methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci. J Antimicrob Chemother 50:731–734.  https://doi.org/10.1093/jac/dkf190 CrossRefGoogle Scholar
  46. 46.
    Godoy-Santos F, Mendonca LA, Mantovani HC (2015) A central composite rotatable design (CCRD) approach to study the combined effect of antimicrobial agents against bacterial pathogens. World J Microbiol Biotechnol 31:1361–1367.  https://doi.org/10.1007/s11274-015-1884-4 CrossRefGoogle Scholar
  47. 47.
    Cameron DR, Howden BP, Peleg AY (2011) The interface between antibiotic resistance and virulence in Staphylococcus aureus and its impact upon clinical outcomes. Clin Infect Dis 53:576–582.  https://doi.org/10.1093/cid/cir473 CrossRefGoogle Scholar

Copyright information

© Association of Microbiologists of India 2019

Authors and Affiliations

  1. 1.Departamento de MicrobiologiaUniversidade Federal de ViçosaViçosaBrazil
  2. 2.Ministério da Agricultura, Pecuária e Abastecimento (MAPA)BrasíliaBrazil
  3. 3.Departamento de MorfologiaUniversidade Federal de SergipeSão CristóvãoBrazil
  4. 4.EMBRAPA Gado de LeiteJuiz de ForaBrazil

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