Skip to main content

Advertisement

SpringerLink
Log in

Potential use of Bacillus thuringiensis bacteriocins to control antibiotic-resistant bacteria associated with mastitis in dairy goats

  • Published:
Folia Microbiologica Aims and scope Submit manuscript

Abstract

Mastitis caused by microbial infections in dairy goats reduces milk yield, modifies milk composition, and potentially contributes to morbidity in herds and consumers of dairy products. Microorganisms associated with mastitis in dairy goats are commonly controlled with antibiotics, but it is known that continued use of these chemical agents promotes antibiotic resistance among bacterial populations. Recently, it has been shown that bacteriocins of Bacillus thuringiensis inhibit growth of food-borne pathogens and also bacteria associated with bovine mastitis. However, there is no report on their ability to inhibit microorganisms linked to mastitis in dairy goats. In this study, using 16S rDNA and ITS regions of rDNA, we identified nine bacterial isolates and an encapsulated yeast associated with mastitis in dairy goats. Enterococcus durans, Brevibacillus sp., and Staphylococcus epidermidis 2 were resistant to, respectively, 75, ~67, ~42, and ~42 % of the antibiotics screened. In addition, 60 % of the bacterial isolates were resistant to penicillin, ampicillin, vancomycin, and dicloxacillin. Importantly, 60 % of the isolates were inhibited by the bacteriocins, but S. epidermidis 1, Enterobacter sp., Escherichia vulneris, and Cryptococcus neoformans were not susceptible to these antimicrobial peptides. Using Brevibacillus sp. and Staphylococcus chromogenes as indicator bacteria, we show that peptides of ~10 kDa that correspond to the molecular mass of bacteriocins used in this study are responsible for the inhibitory activity. Our results demonstrate that multiple antibiotic-resistant bacteria associated with subclinical mastitis in dairy goats from Guanajuato, Mexico, are susceptible to bacteriocins produced by B. thuringiensis.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Barboza-Corona JE, Vazquez-Acosta H, Bideshi DK, Salcedo-Hernández R (2007) Bacteriocin-like inhibitor substances produced by Mexican strains of Bacillus thuringiensis. Arch Microbiol 187:117–126

    Article  PubMed  CAS  Google Scholar 

  • Barboza-Corona JE, de la Fuente-Salcido N, Alva-Murillo N, Ochoa-Zarsoza A, Lopez-Meza JE (2009) Activity of bacteriocins synthesized by Bacillus thuringiensis against Staphylococcus aureus isolates associated to bovine mastitis. Vet Microbiol 138:179–183

    Article  PubMed  CAS  Google Scholar 

  • Barron-Bravo OG, Gutierrez-Chavez AJ, Angel-Sahagun CA, Montaldo HH, Shepard L, Valencia-Posadas M (2013) Losses in milk yield, fat and protein contents according to different levels of somatic cell count in dairy goats. Small Rumin Res 113:421–431

    Article  Google Scholar 

  • Bernacka H (2006) Cytological quality of goat milk on the basis of the somatic cell count. J Cent Eur Agr 7:773–778

    Google Scholar 

  • Bose T, Reese AJ, Ory JJ, Janbon G, Doerin TL (2003) A yeast under cover: the capsule of Cryptococcus neoformans. Eukaryot Cell 2:655–663

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bottone EJ (1980) Cryptococcus neoformans: pitfalls in diagnosis through evaluation of gram-stained smears of purulent exudates. J Clin Microbiol 12:790–791

    PubMed  PubMed Central  CAS  Google Scholar 

  • Bourabah A, Ayad A, Boukraa L, Hammoudi SM, Benbarek H (2013) Prevalence and etiology of subclinical mastitis in goats of the Tiaret region, Algeria. Global Vet 11:604–608

    Google Scholar 

  • Castañeda-Ramirez C, Cortes-Rodriguez V, de la Fuente-Salcido N, Bideshi DK, Barboza-Corona JE (2011) Isolation of Salmonella spp. from lettuce and evaluation of its susceptibility to novel bacteriocins synthesized by Bacillus thuringiensis and antibiotics. J Food Prot 74:274–278

    Article  PubMed  CAS  Google Scholar 

  • Chu C, Yu C, Lee L, Su Y (2012) Genetically divergent methicillin-resistant Staphylococcus aureus and sec-dependent mastitis of dairy goats in Taiwan. BMC Vet Res 8:39

    Article  PubMed  PubMed Central  Google Scholar 

  • Cladera-Oliva F, Caron GR, Brandelli A (2004) Bacteriocin-like substance production by Bacillus licheniformis strain P40. Lett Appl Microbiol 38:251–256

    Article  CAS  Google Scholar 

  • Cotter PD, Ross RP, Hill C (2013) Bacteriocins—a viable alternative to antibiotics? Nature Rev Microbiol 11:95–105

    Article  CAS  Google Scholar 

  • de la Fuente-Salcido N, Alanis-Guzman MG, Bideshi DK, Salcedo-Hernandez R, Bautista-Justo M, Barboza-Corona JE (2008) Enhanced synthesis and antimicrobial activities of bacteriocins produced by Mexican strains of Bacillus thuringiensis. Arch Microbiol 190:633–640

    Article  PubMed  CAS  Google Scholar 

  • de la Fuente-Salcido NM, Barboza-Corona JE, Espino-Monzon AN, Pacheco-Cano RD, Balagurusamy N, Bideshi DK, Salcedo-Hernandez R (2012) Expanding the use of a fluorogenic method to determine activity and mode of action of Bacillus thuringiensis bacteriocins against gram-positive and gram-negative bacteria. Sci World J 2012:503269

    Google Scholar 

  • Delgado A, Brito D, Fevereiro P, Tenreiro R, Peres C (2005) Bioactivity quantification of crude bacteriocins solutions. J Microbiol Meth 62:121–124

    Article  CAS  Google Scholar 

  • Escareño L, Salinas-Gonzalez H, Wirzinger M, Iñiguez L, Sölkner J, Meza-Herrera C (2013) Dairy goat production systems: status quo, perspectives and challenges. Trop Anim Health Prod 45:17–34

    Article  PubMed  Google Scholar 

  • Federici BA (2005) Insecticidal bacteria: an overwhelming success for invertebrate pathology. J Invertebr Pathol 89:30–38

    Article  PubMed  Google Scholar 

  • Fujita SI, Senda Y, Nakaguchi S, Hashimoto T (2001) Multiplex PCR using internal transcribed spacer 1 and 2 regions for rapid detection and identification of yeast strains. J Clin Microbiol 39:3617–3622

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Haenlein GFW (2002) Relationship of somatic cell counts in goat milk to mastitis and productivity. Small Rumin Res 45:163–178

    Article  Google Scholar 

  • Islam A, Samad A, Rahman AKMA (2012) Prevalence of subclinical caprine mastitis in Bangladesh based on parallel interpretation of three screening tests. Inter J Anim Vet Adv 4:225–228

    Google Scholar 

  • Leitner G, Merin U, Silanikove N (2004) Changes in milk composition as affected by subclinical mastitis in goats. J Dairy Sci 87:1719–1726

    Article  PubMed  CAS  Google Scholar 

  • León-Galván MF, Carbajal N, Frickey T, Santos L (2009) Microbial identification of the Nichupte-Bojorquez coastal lagoon in Cancun, Mexico. Aquatic Ecol 43:197–205

    Article  CAS  Google Scholar 

  • León-Galván MF, Barboza-Corona JE, Lechuga-Arana AA, Valencia-Posadas M, Aguayo DD, Cedillo-Pelaez C, Martínez-Ortega EA, Gutierrez-Chavez AJ (2015) Molecular detection and sensitivity to antibiotics and bacteriocins of pathogens isolates from bovine mastitis in family dairy herds of central Mexico. BioMed Res Int 2015:615153

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moroni P, Pisoni G, Antonini M, Ruffo G, Carli S, Varisco G, Boettcher P (2005) Subclinical mastitis and antimicrobial susceptibility of Staphylococcus caprae and Staphylococcus epidermis isolated from two Italian goat herds. J Dairy Sci 88:1694–1704

    Article  PubMed  CAS  Google Scholar 

  • Ndegwa EN, Mulei CM, Munyua SJ (2001) Prevalence of microorganisms associated with udder infection in Dairy goats on small scale farms in Kenyae. J S Afr Vet Assoc 72:97–98

    Article  PubMed  CAS  Google Scholar 

  • Paik HD, Bae SS, Park H, Pan JG (1997) Identification and partial characterization of tochicin, a bacteriocin produced by Bacillus thuringiensis subsp. tochigiensis. J Ind Microbiol Biotechnol 19:294–298

    Article  PubMed  CAS  Google Scholar 

  • Pal M, Randhawa HS (1976) Caprine mastitis due to Cryptococcus neoformans. Sabouraudia 14:261–263

    Article  PubMed  CAS  Google Scholar 

  • Persson Y, Olofsson I (2011) Direct and indirect measurement of somatic cell count as indicator of intramammary infection in dairy goats. Acta Vet Scand 53:15

    Article  PubMed  PubMed Central  Google Scholar 

  • Pieterse R, Todorov SD, Dicks LM (2008) Bacteriocin ST91KM, produced by Streptococcus gallolyticus subsp. macedonicus ST91KM, is a narrow-spectrum peptide active against bacteria associated with mastitis in dairy cattle. Can J Microbiol 54:525–531

    Article  PubMed  CAS  Google Scholar 

  • Raynal-Ljutovac K, Pirisi A, de Cremoux R, Gonzalo C (2007) Somatic cells of goat and sheep milk: analytical, sanitary, productive and technological aspects. Small Rumin Res 68:126–144

    Article  Google Scholar 

  • Ryan MP, Meaney WJ, Ross RP, 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • Thomas P (2006) Isolation an ethanol-tolerant endospore-forming gram-negative Brevibacillus sp. as a convert contaminant in grape tissue cultures. J Appl Microbiol 101:764–774

    Article  PubMed  CAS  Google Scholar 

  • Twomey DP, Wheelock AI, Flynn J, Meaney WJ, Hill C, Ross RP (2000) Protection against Staphylococcus aureus mastitis in dairy cows using a bismuth-based teat seal containing the bacteriocin, lacticin 3147. J Dairy Sci 83:1981–1988

    Article  PubMed  CAS  Google Scholar 

  • Ukuku DO, Shelef LA (1997) Sensitivity of six strains of Listeria monocytogenes to nisin. J Food Prot 60:867–869

    CAS  Google Scholar 

  • Varella-Coelho ML, Santos-Nascimento JD, Fagundes PC, Madureira DJ, Oliveira SS, de Paiva V, Brito MA, Freire Bastos Mdo C (2007) Activity of staphylococcal bacteriocins against Staphylococcus aureus and Streptococcus agalactiae involved in bovine mastitis. Res Microbiol 158:625–630

    Article  PubMed  CAS  Google Scholar 

  • Viguier C, Arora S, Gilmartin N, Welbeck K, O’Kennedy R (2009) Mastitis detection: current trends and future perspectives. Trends Biotechnol 27:486–493

    Article  PubMed  CAS  Google Scholar 

  • Yount NY, Yeaman MR (2005) Immunocontinuum: perspectives in antimicrobial peptides mechanisms of action and resistance. Protein Pept Lett 12:49–67

    Article  PubMed  CAS  Google Scholar 

  • Yount NY, Yeaman MR (2013) Peptide antimicrobials: cell wall as a bacterial target. Ann NY Acad Sci 1277:127–138

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by Grants from the Universidad de Guanajuato (project 24/2011) and Fundación Guanajuato Produce A.C. Mexico (project FGP 583/12) to J. E. Barboza-Corona and M. Valencia-Posadas, respectively. E.A. Martínez-Ortega is an undergraduate student supported by the Universidad de Guanajuato. We thank Dr. Luz Edith Casados-Vázquez and Jaime J. Badajoz-Martínez from Universidad de Guanajuato for their technical support during this study. We appreciate the facilities provided by the producers for this study as well.

Conflict of interest

The authors declare that they have competing interests.

Author information

Authors and Affiliations

  1. Departamento de Agronomía, División de Ciencias de la Vida, Universidad de Guanajuato Campus Irapuato-Salamanca, Guanajuato, 36500, Mexico

    A. J. Gutiérrez-Chávez, E. A. Martínez-Ortega & M. Valencia-Posadas

  2. Departamento de Alimentos, División de Ciencias de la Vida, Universidad de Guanajuato Campus Irapuato-Salamanca, Guanajuato, 36500, Mexico

    M. F. León-Galván & J. E. Barboza-Corona

  3. Posgrado en Biociencias Irapuato, División de Ciencias de la Vida, Universidad de Guanajuato Campus Irapuato-Salamanca, Guanajuato, 36500, Mexico

    A. J. Gutiérrez-Chávez, M. Valencia-Posadas, M. F. León-Galván & J. E. Barboza-Corona

  4. Escuela de Ciencias Biológicas, Aniversidad Autónoma de Coahuila, Torreón, Coahuila, 27104, Mexico

    N. M. de la Fuente-Salcido

  5. Department of Natural and Mathematical Sciences, California Baptist University, 8432 Magnolia Avenue, Riverside, CA, 92504, USA

    D. K. Bideshi

  6. Department of Entomology, University of California, Riverside, Riverside, CA, 92521, USA

    D. K. Bideshi

Authors
  1. A. J. Gutiérrez-Chávez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. A. Martínez-Ortega
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Valencia-Posadas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. F. León-Galván
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. N. M. de la Fuente-Salcido
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. D. K. Bideshi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. E. Barboza-Corona
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. E. Barboza-Corona.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gutiérrez-Chávez, A.J., Martínez-Ortega, E.A., Valencia-Posadas, M. et al. Potential use of Bacillus thuringiensis bacteriocins to control antibiotic-resistant bacteria associated with mastitis in dairy goats. Folia Microbiol 61, 11–19 (2016). https://doi.org/10.1007/s12223-015-0404-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12223-015-0404-0

Keywords

Search

Navigation