Antibacterial activities of coagulase-negative staphylococci from bovine teat apex skin and their inhibitory effect on mastitis-related pathogens

Journal of Applied Microbiology

Volumn 116, Issue 5, 2014, Pages 1084-1093

  Braem, G ^a   Stijlemans, B ^a,b   Van Haken, W ^a   De Vliegher, S ^c   De Vuyst, L ^a   Leroy, F ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

Bacteriocin; Mastitis; Staphylococcus; Udder health

Indexed keywords

BACTERIA; CHROMATOGRAPHY; GROWTH KINETICS;

ANTI-BACTERIAL ACTIVITY; BACTERIOCINS; CATION EXCHANGES; DAIRY COW; INHIBITORY EFFECT; MASTITI; NUKACIN; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; UDDER HEALTH;

PATHOGENS;

BACTERIOCIN; NUKACIN 3299; NUKACIN ISK 1; NUKACIN L217; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; COAGULASE;

ANTIMICROBIAL ACTIVITY; BACTERIUM; CATTLE; ENZYME ACTIVITY; INHIBITOR; ION EXCHANGE; PATHOGEN; POLYMERASE CHAIN REACTION; REACTION KINETICS; SKIN;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL GENE; COAGULASE NEGATIVE STAPHYLOCOCCUS; CONTROLLED STUDY; DAIRY CATTLE; MASTITIS; MICROBIAL COMMUNITY; MINIMUM INHIBITORY CONCENTRATION; NIPPLE; NONHUMAN; NUKA GENE; PATHOGENESIS; POLYMERASE CHAIN REACTION; REVERSED PHASE LIQUID CHROMATOGRAPHY; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS AURICULARIS; STAPHYLOCOCCUS CAPITIS; STAPHYLOCOCCUS CHROMOGENES; STAPHYLOCOCCUS COHNII; STAPHYLOCOCCUS EPIDERMIDIS; STAPHYLOCOCCUS HAEMOLYTICUS; STAPHYLOCOCCUS HOMINIS; STAPHYLOCOCCUS PASTEURI; STAPHYLOCOCCUS SAPROPHYTICUS; STAPHYLOCOCCUS SCHLEIFERI; STAPHYLOCOCCUS SCIURI; STAPHYLOCOCCUS SIMULANS; STAPHYLOCOCCUS WARNERI; STAPHYLOCOCCUS XYLOSUS; STREPTOCOCCUS DYSGALACTIAE; STREPTOCOCCUS UBERIS; ANIMAL; ANTIBIOSIS; BOVINAE; BOVINE MASTITIS; CHEMISTRY; DRUG EFFECTS; FEMALE; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; PHYSIOLOGY; SKIN; STREPTOCOCCUS; UDDER;

BOVINAE; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS CHROMOGENES; STREPTOCOCCUS DYSGALACTIAE; STREPTOCOCCUS UBERIS;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIBIOSIS; BACTERIOCINS; CATTLE; COAGULASE; FEMALE; MAMMARY GLANDS, ANIMAL; MASTITIS, BOVINE; SKIN; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS;

EID: 84898409363     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12447     Document Type: Article

References (46)

1. Allgaier, H., Jung, G., Werner, R.G., Schneider, U. and Zähner, H. (1985) Elucidation of the structure of epidermin, a ribosomally synthesized, tetracyclic heterodetic polypeptide antibiotic. Angew Chem Int Edit 24, 1051-1053.
2. Asaduzzaman, S.M., Nagao, J.-I., Iida, H., Zendo, T., Nakayama, J. and Sonomoto, K. (2009) Nukacin ISK-1, a bacteriostatic lantibiotic. Antimicrob Agents Chemother 53, 3595-3598.
3. Barkema, H.W., Schukken, Y.H. and Zadoks, R.N. (2006) The role of cow, pathogen, and treatment regimen in the therapeutic success of bovine Staphylococcus aureus mastitis. J Dairy Sci 89, 1877-1895.
4. Bastos, M.C.F., Ceotto, H., Coelho, M.L.V. and Nascimento, J.S. (2009) Staphylococcal antimicrobial peptides: relevant properties and potential biotechnological applications. Curr Pharm Biotechnol 10, 38-61.
5. Bradley, A.J. (2002) Bovine mastitis: an evolving disease. Vet J 164, 116-128.
6. 5-PCR fingerprinting for the classification and identification of coagulase-negative Staphylococcus species from bovine milk and teat apices: a comparison of type strains and field isolates. Vet Microbiol 147, 67-74.
7. Braem, G., De Vliegher, S., Verbist, B., Heyndrickx, M., Leroy, F. and De Vuyst, L. (2012) Culture-independent exploration of the teat apex microbiota of dairy cows reveals a wide bacterial species diversity. Vet Microbiol 157, 383-390.
8. Braem, G., De Vliegher, S., Verbist, B., Piessens, V., Van Coillie, E., De Vuyst, L. and Leroy, F. (2013) Unraveling the microbiota of teat apices of clinically healthy lactating dairy cows, with special emphasis on coagulase-negative staphylococci. J Dairy Sci 96, 1499-1510.
9. Burianek, L.L. and Yousef, A.E. (2000) Solvent extraction of bacteriocins from liquid cultures. Lett Appl Microbiol 31, 193-197.
10. Ceotto, H., Holo, H., da Costa, K.F.S., Nascimento, J.S., Salehian, Z., Nes, I.F. and Bastos, M.C.F. (2010) Nukacin 3299, a lantibiotic produced by Staphylococcus simulans 3299 identical to nukacin ISK-1. Vet Microbiol 146, 124-131.
11. Ceotto, H., Da Silva Dias, R.C., Nascimento, J., De Paiva Brito, M.A.V., Giambiagi-Demarval, M. and Bastos, M.C.F. (2012) Aureocin A70 production is disseminated amongst genetically unrelated Staphylococcus aureus involved in bovine mastitis. Lett Appl Microbiol 54, 455-461.
12. Coelho, V.M.L., Nascimento, J.S., Fagundes, P.C., Madureira, D.J., Oliveira, S.S., de Paiva Brito, M.A.V. and Bastos, M.C.F. (2007) Activity of staphylococcal bacteriocins against Staphylococcus aureus and Streptococcus agalactiae involved in bovine mastitis. Res Microbiol 158, 625-630.
13. Cotter, P.D., Hill, C. and Ross, R.P. (2005) Bacteriocins: developing innate immunity for food. Nature Rev Microbiol 3, 777-788.
14. De Vliegher, S., Laevens, H., Devriese, L.A., Opsomer, G., Leroy, J.L., Barkema, H.W. and de Kruif, A. (2003) Prepartum teat apex colonization with Staphylococcus chromogenes in dairy heifers is associated with low somatic cell count in early lactation. Vet Microbiol 92, 245-252.
15. De Vliegher, S., Opsomer, G., Vanrolleghem, A., Devriese, L.A., Sampimon, O.C., Sol, J., Barkema, H.W., Haesebrouck, F. et al. (2004) In vitro growth inhibition of major mastitis pathogens by Staphylococcus chromogenes originating from teat apices of dairy heifers. Vet Microbiol 101, 215-221.
16. De Vuyst, L. and Leroy, F. (2007) Bacteriocins from lactic acid bacteria: production, purification, and food applications. J Mol Microbiol Biotechnol 13, 194-199.
17. Drider, D., Fimland, G., Hechard, Y., McMullen, L.M. and Prevost, H. (2006) The continuing story of class IIa bacteriocins. Microbiol Mol Biol Rev 70, 564-582.
18. Fagundes, P.C., Ceotto, H., Potter, A., de Paiva Brito, M.A.V., Brede, D., Nes, I.F. and Bastos, M.C.F. (2011) Hyicin 3682, a bioactive peptide produced by Staphylococcus hyicus 3682 with potential applications for food preservation. Res Microbiol 162, 1052-1059.
19. Hammami, R., Zouhir, A., Le Lay, C., Ben Hamida, J. and Fliss, I. (2010) BACTIBASE second release: a database and tool platform for bacteriocin characterization. BMC Microbiol 10, 22.
20. Heng, N.C.K. and Tagg, J.R. (2006) What's in a name? Class distinction for bacteriocins. Nat Rev Microbiol 4. doi:10.1038/nrmicro1273-c1031
21. Jack, R.W., Tagg, J.R. and Ray, B. (1995) Bacteriocins of Gram-positive bacteria. Microbiol Rev 59, 171-200.
22. Kies, S., Vuong, C., Hille, M., Peschel, A., Meyer, C., Götz, F. and Otto, M. (2003) Control of antimicrobial peptide synthesis by the agr quorum sensing system in Staphylococcus epidermidis: activity of the lantibiotic epidermin is regulated at the level of precursor peptide processing. Peptides 24, 329-338.
23. Kim, P.I., Sohng, J.K., Sung, C., Joo, H.-S., Kim, E.-M., Yamaguchi, T., Park, D. and Kim, B.-G. (2010) Characterization and structure identification of an antimicrobial peptide, hominicin, produced by Staphylococcus hominis MBBL 2-9. Biochem Biophys Res Co 399, 133-138.
24. Klaenhammer, T.R. (1993) Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol Rev 12, 39-85.
25. Lauková, A. and Mareková, M. (1993) Antimicrobial spectrum of bacteriocin-like substances produced by rumen staphylococci. Folia Microbiol 38, 74-76.
26. McDougald, D., Rice, S.A., Barraud, N., Steinberg, P.D. and Kjelleberg, S. (2012) Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal. Nature Rev Microbiol 10, 39-50.
27. Nascimento, J.S., Fagundes, P.C., Brito, M.A.V.P., Santos, K.R.N. and Bastos, M.C.F. (2005) Production of bacteriocins by coagulase-negative staphylococci involved in bovine mastitis. Vet Microbiol 106, 61-71.
28. Nascimento, J.S., Ceotto, H., Nascimento, S.B., Giambiagi-deMarval, M., Santos, K.R.N. and Bastos, M.C.F. (2006) Bacteriocins as alternative agents for control of multiresistant staphylococcal strains. Lett Appl Microbiol 42, 215-221.
29. Nes, I.F. and Holo, H. (2000) Class II antimicrobial peptides from lactic acid bacteria. Pept Sci 55, 50-61.
30. Piepers, S., Opsomer, G., Barkema, H.W., de Kruif, A. and De Vliegher, S. (2010) Heifers infected with coagulase-negative staphylococci in early lactation have less cases of clinical mastitis and a higher milk production in their first lactation than non-infected heifers. J Dairy Sci 93, 2014-2024.
31. Piepers, S., Schukken, Y.H., Passchyn, P. and De Vliegher, S. (2013) The impact of intramammary infection with coagulase-negative staphylococci in early lactating heifers on milk yield throughout first lactation revisited. J Dairy Sci 96, 5095-5105.
32. Piessens, V., Van Coillie, E., Verbist, B., Supré, K., Braem, G., Van Nuffel, A., De Vuyst, L., Heyndrickx, M. et al. (2011) Distribution of coagulase-negative Staphylococcus species from milk and environment of dairy cows differs between herds. J Dairy Sci 94, 2933-2944.
33. Piessens, V., De Vliegher, S., Verbist, B., Braem, G., Van Nuffel, A., De Vuyst, L., Heyndrickx, M. and Van Coillie, E. (2012) Intra-species diversity and epidemiology varies among coagulase-negative Staphylococcus species causing bovine intramammary infections. Vet Microbiol 155, 62-71.
34. Pieterse, R., Todorov, S.D. and Dicks, L.M.T. (2010) Mode of action and in vitro susceptibility of mastitis pathogens to macedocin ST91KM and preparation of a teat seal containing the bacteriocin. Braz J Microbiol 41, 133-145.
35. Ryan, M.P., Meaney, W.J., Ross, R.P. and Hill, C. (1998) Evaluation of lacticin 3147 and a teat seal containing this bacteriocin for inhibition of mastitis pathogens. Appl Environ Microbiol 64, 2287-2290.
36. Sashihara, T., Kimura, H., Higuchi, T., Adachi, A., Matsusaki, H., Sonomoto, K. and Ishizaki, A. (2000) A novel lantibiotic, nukacin ISK-1, of Staphylococcus warneri ISK-1: cloning of the structural gene and identification of the structure. Biosci Biotechnol Biochem 64, 2420-2428.
37. Schillinger, U. and Lücke, F.K. (1989) Antibacterial activity of Lactobacillus sake isolated from meat. Appl Environ Microbiol 55, 1901-1906.
38. Supré, K., Haesebrouck, F., Zadoks, R.N., Vaneechoutte, M., Piepers, S. and De Vliegher, S. (2011) Some coagulase-negative Staphylococcus species affect udder health more than others. J Dairy Sci 94, 2329-2340.
39. Tagg, J.R. and Bannister, L.V. (1979) "Fingerprinting" β-haemolytic streptococci by their production of and sensitivity to bacteriocin-like inhibitors. J Med Microbiol 12, 397-411.
40. Taponen, S. and Pyörälä, S. (2009) Coagulase-negative staphylococci as cause of bovine mastitis - Not so different from Staphylococcus aureus? Vet Microbiol 134, 29-36.
41. Taponen, S., Koort, J., Björkroth, J., Saloniemi, H. and Pyörälä, S. (2007) Bovine intramammary infections caused by coagulase-negative staphylococci may persist throughout lactation according to amplified fragment length polymorphism-based analysis. J Dairy Sci 90, 3301-3307.
42. Thorberg, B.M., Danielsson-Tham, M.L., Emanuelson, U. and Persson Waller, K. (2009) Bovine subclinical mastitis caused by different types of coagulase-negative staphylococci. J Dairy Sci 92, 4962-4970.
43. Wilaipun, P., Zendo, T., Okuda, K., Nakayama, J. and Sonomoto, K. (2008) Identification of the nukacin KQU-131, a new type-A(II) lantibiotic produced by Staphylococcus hominis KQU-131 isolated from Thai fermented fish product (Pla-ra). Biosci Biotechnol Biochem 72, 2232-2235.
44. Wu, J., Hu, S. and Cao, L. (2007) Therapeutic effect of nisin Z on subclinical mastitis in lactating cows. Antimicrob Agents Chemother 51, 3131-3135.
45. Zhao, X. and Lacasse, P. (2008) Mammary tissue damage during bovine mastitis: causes and control. J Anim Sci 86, 57-65.
46. Zouhir, A., Hammami, R., Fliss, I. and Hamida, J. (2010) A new structure-based classification of Gram-positive bacteriocins. Protein J 29, 432-439.