Skip to main content
SpringerLink
Log in

Bacteriocinogenic Bacteria Isolated from Raw Goat Milk and Goat Cheese Produced in the Center of México

  • Original Article
  • Published:
Indian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Currently, there are few reports on the isolation of microorganisms from goat milk and goat cheese that have antibacterial activity. In particular, there are no reports on the isolation of microorganisms with antibacterial activity from these products in central Mexico. Our objective was to isolate bacteria, from goat products, that synthesized antimicrobial peptides with activity against a variety of clinically significant bacteria. We isolated and identified Lactobacillus rhamnosus, L. plantarum, L. pentosus, L. helveticus and Enterococcus faecium from goat cheese, and Aquabacterium fontiphilum, Methylibium petroleiphilum, Piscinobacter aquaticus and Staphylococcus xylosus from goat milk. These bacteria isolated from goat cheese were able to inhibit Staphylococcus aureus, Bacillus cereus, Escherichia coli, Listeria monocytogenes, L. inoccua, Pseudomona aeruginosa, Shigella flexneri, Serratia marcescens, Enterobacter cloacae and Klebsiella pneumoniae. In addition, bacteria from goat milk showed inhibitory activity against B. cereus, L. lactis, E. coli, S. flexneri, E. cloacae and K. pneumonia; S. aureus, L. innocua, S. agalactiae and S. marcescens. The bacteriocins produced by these isolates were shown to be acid stable (pH 2–6) and thermotolerant (up to 100 °C), but were susceptible to proteinases. When screened by PCR for the presence of nisin, pediocin and enterocin A genes, none was found in isolates recovered from goat milk, and only the enterocin A gene was found in isolates from goat cheese.

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

Similar content being viewed by others

References

  1. Escareño L, Salinas-González H, Wurzinger M, Iñiguez L, Solkner J, Meza-Herrera C (2013) Dairy goat production system. Status quo, perspectives and challenges. Trop Anim Health Prod 45:17–34. doi:10.1007/s11250-012-0246-6

    Article  PubMed  Google Scholar 

  2. Gómez-Ruiz WJ, Pinos-Rodríguez JM, Aguirre-Rivera JR, García-López JC (2012) Analysis of a goat milk cheese industry in a desert rangeland of Mexico. Pastor Res Policy Pract 2:2–11. doi:10.1186/2041-7136-2-5

    Article  Google Scholar 

  3. Quigley L, O’Sullivan O, Stanton C, Beresford TP, Ross RP, Fitzgerald GF, Cotter PD (2013) The complex microbiota of raw milk. FEMS Microbiol Rev 37:664–698. doi:10.1111/1574-6976

    Article  CAS  PubMed  Google Scholar 

  4. Nikolic M, Terzic-Vidojevic A, Jovcic B, Begovic J, Golic N, Topisirovic L (2008) Characterization of lactic acid bacteria isolated from Bukuljac, a homemade goat’s milk cheese. Int J Food Microbiol 122:162–170. doi:10.1016/j.ijfoodmicro.2007.11.075

    Article  CAS  PubMed  Google Scholar 

  5. Perin LM, Nero LA (2014) Antagonistic lactic acid bacteria isolated from goat milk and identification of a novel nisin variant Lactococcus lactis. BMC Microbiol 14:36. doi:10.1186/1471-2180-14-36

    Article  PubMed  PubMed Central  Google Scholar 

  6. Ekici K, Bozkurt H, Isleyici O (2004) Isolation of some pathogens from raw milk of different milch animals. Pak J Nutr 3:161–162. doi:10.3923/pjn.2004.161.162

    Article  Google Scholar 

  7. Drider D, Fimland G, Hechard Y, McMullen LM, Prevost H (2006) The continuing story of class IIa bacteriocins. Microbiol Mol Biol Rev 70:564–582. doi:10.1128/MMBR.00016-05

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Rodríguez E, González B, Gaya P, Nuñez M, Medina M (2000) Diversity of bacteriocins produced by lactic acid bacteria isolated from raw milk. Int Dairy J 10:7–15. doi:10.1016/S0958-6946(00)00017-0

    Article  Google Scholar 

  9. Barrón-Bravo OG, Gutierrez-Chavez AJ, Angel Sahagún 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. doi:10.1016/j.smallrumres.2013.04.003

    Article  Google Scholar 

  10. León-Galván MF, Barboza-Corona JE, Lechuga-Arana A, 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 isolated from bovine mastitis in family dairy herds of Central Mexico. Biomed Res Int 2015:615153. doi:10.1155/2015/615153

    Article  PubMed  PubMed Central  Google Scholar 

  11. Callon C, Duthoit F, Delbes C, Ferrand M, Le Frileux Y, de Cremoux R, Montel MC (2007) Stability of microbiol communities in goat milk during a lactation year: molecular approaches. Syst Appl Microbiol 30:547–560. doi:10.1016/j.syapm.2007.05.004

    Article  CAS  PubMed  Google Scholar 

  12. Barboza-Corona JE, Vázquez-Acosta H, Bideshi-Dennis K, Salcedo-Hernández R (2007) Bacteriocin-like inhibitor substances produced by Mexican strains of Bacillus thuringiensis. Arch Microbiol 187:117–126. doi:10.1007/s00203-006-0178-5

    Article  CAS  PubMed  Google Scholar 

  13. Pospiech A, Neumann B (1995) A versatil quick-prep of genomic DNA from Gram-positive bacteria. Trends Genet 11:217–218. doi:10.1016/S0168-9525(00)89052-6

    Article  CAS  PubMed  Google Scholar 

  14. León-Galván MF, Carbajal N, Frickey T, Santos L (2009) Microbial identification of the Nichupte-Bojorquez coastal lagoon in Cancun, Mexico. Aquat Ecol 43:197–205. doi:10.1007/s10452-008-9171-1

    Article  Google Scholar 

  15. Suwanjinda D, Eames C, Panbangred W (2007) Screening of lactic acid bacteria for bacteriocins by microbiological and PCR methods. Biochem Mol Biol Educ 35:364–369. doi:10.1002/bmb.84

    Article  CAS  PubMed  Google Scholar 

  16. Rogers AM, Montville TJ (1991) Improved agar diffusion assay for nisin quantification. Food Biotechnol 5:161–168. doi:10.1080/08905439109549799

    Article  CAS  Google Scholar 

  17. Annamalai N, Manivasagan P, Balasubramanian T, Vijayalakshmi S (2009) Enterocin from Enterococcus faecium isolated from mangrove environment. Afr J Biotechnol 8:6311–6316. doi:10.5897/AJB2009.000-9478

    CAS  Google Scholar 

  18. Alonso-Calleja C, Carballo J, Capita R, Bernardo A, García-López ML (2002) Changes in the microflora of Valdeteja raw goat’s milk cheese throughout manufacturing and ripening. LWT Food Sci Technol 35:222–232. doi:10.1006/fstl.2001.0842

    Article  CAS  Google Scholar 

  19. Martínez JM, Kok J, Sanders JW, Hernández PE (2000) Heterologous coproduction of enterocin A and pediocin PA-1 by Lactococcus lactis: detection by specific peptide-directed antibodies. Appl Environ Microbiol 66:3543–3549. doi:10.1128/AEM.66.8.3543-3549.2000

    Article  PubMed  PubMed Central  Google Scholar 

  20. Rehaiem A, Pérez Guerra N, Ben Belgacema Z, Fajardo Bernárdez P, Pastrana Castro L, Manaia M (2011) Enhancement of enterocin A production by Enterococcus faecium MMRA and determination of its stability to temperature and pH. Biochem Eng J 56:94–106. doi:10.1016/j.bej.2011.05.012

    Article  CAS  Google Scholar 

  21. Lin MC, Jiang SR, Chou JH, Arun AB, Young CC, Chen WM (2009) Aquabacterium fontiphilum sp. nov. isolated from spring water. Int J Syst Evol Microbiol 59:681–685. doi:10.1099/ijs.0.000745-0

    Article  CAS  PubMed  Google Scholar 

  22. Stackebrandt E, Verbarg S, Fruhling A, Busse HJ, Tindall BJ (2009) Dissection of the genus Methylibium: reclassification of Methylibium fulvum as Rhizobacter fulvus comb. nov., Methylibium aquaticum as Piscinibacter aquaticus gen. nov., comb. nov. and Methylibium subsaxonicum as Rivibacter subsaxonicus gen. nov., comb. nov. and emended descriptions of the genera Rhizobacter and Methylibium. Int J Syst Evol Microbiol 59:2552–2560. doi:10.1099/ijs.0.008383-0

    Article  CAS  PubMed  Google Scholar 

  23. Schmidt R, Battaglia V, Scow K, Kane S, Hristova KR (2008) Involvement of a novel enzyme, MdpA, in methyl tert-butyl ether degradation in Methylibium petroleiphilum PM1. Appl Environ Microbiol 74:6631–6638. doi:10.1128/AEM.01192-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Koop G, De Vliegher S, De Visscher A, Supré K, Haesebrouck F, Nielen M, van Werven T (2012) Differences between coagulase-negative Staphylococcus species in persistence and in effect on somatic cell count and milk yield in dairy goats. J Dairy Sci 95:5075–5084. doi:10.3168/jds.2012-5615

    Article  CAS  PubMed  Google Scholar 

  25. Broberg A, Jacobsson K, Ström K, Schnürer J (2007) Metabolite profiles of lactic acid bacteria in grass silage. Appl Environ Microbiol 73:5547–5552. doi:10.1128/AEM.02939-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This research was partially supported by Grant from “Universidad de Guanajuato” (project 262/2013) to J. E. Barboza-Corona, and “Fundación Guanajuato Produce AC” (project FGP 583/12) to M. Valencia-Posadas, respectively. O.F. Hernández-Saldaña is a graduate student supported by CONACyT-México. We appreciate the technical support of Daniela Lisseth Contreras-González and Dr. Luz E. Casados-Vázquez from “Universidad de Guanajuato” during the process of this work.

Author information

Authors and Affiliations

  1. División de Ciencias de la Vida, Universidad de Guanajuato, Campus Irapuato-Salamanca (CIS), Ex-Hacienda El Copal km. 9, carretera Irapuato-Silao; A.P. 311, C.P. 36500, Irapuato, Guanajuato, Mexico

    Oscar F. Hernández-Saldaña, Mauricio Valencia-Posadas & José E. Barboza-Corona

  2. Departamento de Alimentos, Universidad de Guanajuato CIS, Ex-Hacienda El Copal km. 9, carretera Irapuato-Silao; A.P. 311, C.P. 36500, Irapuato, Guanajuato, Mexico

    José E. Barboza-Corona

  3. Departamento de Agronomía, Universidad de Guanajuato CIS, Ex-Hacienda El Copal km. 9, carretera Irapuato-Silao; A.P. 311, C.P. 36500, Irapuato, Guanajuato, Mexico

    Mauricio Valencia-Posadas

  4. Escuela de Ciencias Biológicas, Universidad Autónoma de Coahuila, Boulevard Torreón-Matamoros Km. 7.5, Ciudad Universitaria Campus Torreón, C.P. 27104, Torreón, Coahuila, Mexico

    Norma M. de la Fuente-Salcido

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

    Dennis K. Bideshi

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

    Dennis K. Bideshi

  7. Graduate Program in Biosciences, Life Science Division, Universidad de Guanajuato, Ex-Hacienda El Copal km. 9, carretera Irapuato-Silao; A.P. 311, C.P. 36500, Irapuato, Guanajuato, Mexico

    Oscar F. Hernández-Saldaña, Mauricio Valencia-Posadas & José E. Barboza-Corona

Authors
  1. Oscar F. Hernández-Saldaña
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mauricio Valencia-Posadas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Norma M. de la Fuente-Salcido
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dennis K. Bideshi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. José E. Barboza-Corona
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to José E. Barboza-Corona.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 501 kb)

Supplementary material 2 (DOCX 104 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hernández-Saldaña, O.F., Valencia-Posadas, M., de la Fuente-Salcido, N.M. et al. Bacteriocinogenic Bacteria Isolated from Raw Goat Milk and Goat Cheese Produced in the Center of México. Indian J Microbiol 56, 301–308 (2016). https://doi.org/10.1007/s12088-016-0587-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12088-016-0587-3

Keywords

Search

Navigation