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Jurado Gámez, H. ., & Fajardo Argoti, C. . (2017). Determination of the probiotic in vitro effect of Lactobacillus gasseri on a Staphylococcus epidermidis strain. Biosalud, 16(2), 53–69. https://doi.org/10.17151/biosa.2017.16.2.6
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Abstract
Due to the characteristic probiotic properties of lactic acid bacteria such as the generation of compounds derived from fermentation, which can inhibit multiple pathogenic organisms to create an unfavorable environment for them and finally to be used as an alternative to the use of drugs to treat and prevent various diseases. The present study sought to assess probiotic characteristics of L. gasseri on S. epidermidis under in vitro conditions. The susceptibility of both strains to different antibiotics, the inhibitory effect of L. gasseri and supernatant on S. epidermidis, and the growth of the lactic strain at different pH, temperature, bile salts and bovine bile were determined. The fermentation kinetics was established, and the count of viable microorganisms in plaque, pH, sugar consumption, consumption of protein and percentage of lactic acid was defined. Finally, peptides and lactic acid were determined using HPLC-DAD for L. gasseri, and in the case of amino acids in the supernatant, these were determined with HPLC-PDA for the two strains. The resistance of both strains to the antibiotics gentamicin and dicloxacillin was found. The lactic strain and the supernatant inhibited the growth of S. epidermidis. The growth was suitable for the different variables with values between 1.8 x 109 and 3.0 x 1012 CFU/150 µl. The exponential phase was observed at 12 hours with a value of 3 x 1011 CFU/150 µl, with values of 4.296, 1.26%, 2.032 mg/l and 0.65 mg/l for pH, lactic acid, sugar consumption and protein consumption, respectively. Finally, the peptide VAL-TIR-VAL with a value of 0.73 mg/ml, 11.7 g/l of lactic acid, and the amino acid tyrosine were identified in the supernatant of L. gasseri by HPLC-DAD. The results show that Lactobacillus gasseri have probiotic characteristics on S. epidermidis under in vitro conditions.
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References
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3. Treven P, Turkova K, Trmcic A, Obermajer T, Rogelj I. Matijasic BB. Detection and quantification of probiotic strain Lactobacillus gasseri K7 in faecal samples by targeting bacteriocin genes. Folia Microbiol. 2013 (Praha); 58:623–630.
4. Yanagibashi T, Hosono A, Oyama A, Tsuda M, Hachimura S et al. Bacteroides induce higher IgA production than Lactobacillus by increasing activation-induced cytidine deaminase expression in B cells in murine Peyer’s patches. Biosci Biotechnol Biochem 2009; 73: 372–377 (traducido por los autores).
5. Taponen S, Pyörälä S. Coagulase-negative staphylococci as cause of bovine mastitis-Not so different from Staphylococcus aureus. 2009.
6. Sawant AA, Gillespie BE, Oliver SP Antimicrobial susceptibility of coagulase-negative Staphylococcus species isolated from bovine milk. 2008.
7. Crueger W, Crueger A. (1993). Biotecnología: manual de microbiología industrial. 3 ed. España: Ed. Acribia. 220 p.
8. Jurado-Gámez H, Calpa-Yama F, Chaspuengal-Tulcán A.. Determinación in vitro de la acción probiótica de Lactobacillus plantarum sobre Yersinia pseudotuberculosis aislada de Cavia porcellus. Rev. Fac. Med. Vet. Zoot. 2014; 61: 241-257.
9. Bauer AW, Kirby WM, Sherris JC, Turck M. (1966). Antibiotic susceptibility testing by a standardizedsingle disk method. American Journal of Clinical Pathology, 45, 493.
10. Tagg J, Mcgiven A. Assay system for Bacteriocins. Appl. Environ. Microb. 1971; 21: 943.
11. Klaenhammer TR. Genetics of bacteriocins produced by lactic acid bacteria FEMS Microbiology Reviews 1993; 12(1-3): 39-85.
12. Cai Y, Benno Y, Nakase T, Oh T. Specific probiotic characterization of Weissella hellenica DS-12 isolated from flounder intestine. J Gen Appl Microbiol. 1998; 44: 311-316.
13. Cai Y, Suyanandana P, Saman P, Benno Y. Classification and characterization of lactic acid bacteria isolated from the intestines of common carp and freshwater prawns. J Gen Appl Microbiol. 1999; 45: 177-184.
14. Dahl T, Midden W, Hartman P. (1989). Comparison of Killing of Gram-negative and Gram-positive Bacteria by Pure Singlet Oxygen. J Bacteriol. 171: 2188-2194.
15. Lanara, laboratório de referência animal. Métodos analíticos oficiáis para controle de produtos de origem animal e seus ingredientes. Ii- Métodos físico e químicos. Mel. Ministério da Agricultura. Brasília. 1981. 2 (25): 1-15.
16. Dubois M, Gilles K, Hamilton J, Rebers P, Smith F. Colorimetric method for determination of sugar and related substances. Anal Chem. 1956; 28:350-356.
17. Lowry O, Rosebroug N, Far A, Randall Rj. Protein measurement with the folin phenol reagent. J. Biological. Chemistry. 1951; 193: 265-75.
18. Teuber M, Meile L, Schwarz F. Acquired antibiotic resistance in lactic acid bacteria from food. Antonie van Leeuwenhoek 1999; 76 115-137.
19. Salyers AA, Gupta A, Wang Y. Human intestinal bacteria as reservoirs for antibiotic resistance genes. Trends Microbiol. 2004; 12 412–41610.1016/j.tim.2004.07.004
20. Hambleton P, Turnbull PCB. Anthrax vaccine development: a continuing story. Adv. Biotechnol. Processes. 1990; 13:105–122.
21. Zhou JS, Pillidge CJ, Gopal, PK, Gill HS. Antibiotic susceptibility profiles of new probiotic Lactobacillus and Bifidobacterium strains. International Journal of Food Microbiology 2005; 98(2), 211-217.
22. Benavides-Plascencia L, Aldama-Ojeda LA, Vázquez JH. Vigilancia de los niveles de uso de antibióticos y perfiles de resistencia bacteriana en hospitales de tercer nivel de la Ciudad de México. Salud Pública de México 2005; 47(3), 219-226.
23. Maranan MC, Moreira B, Boyle-Vavra S, Daum RS. Antimicrobial resistance in staphylococci: epidemiology, molecular mechanisms, and clinical relevance. Infectious Disease Clinics of North America 1997; 11(4), 813-849.
24. Rolfe DR. The role of probiotic cultures in the control of gastrointestinal health. J. Nutr. 2000; 130:396.
25. De Vuyst L. Growth kinetics and production of probiotic lactic acid bacteria strains: limitations and breakthroughs. Med. Fac. Landbouww. Univ. Gent. 1998; 63/4b:1511.
26. Feria Cáceres PF. Aislamiento y caracterización Bacteriocinas producidas por Lactobacillus plantarum LPBM10 en suero de leche. Tesis Msc Biotecnología. Universidad Nacional de Colombia, Facultad de Ciencias. Medellín - Colombia, 2007. p 84,
27. Jurado-Gámez H, Guzmán-Insuasty M, Jarrín-Jarrín V. Determinación de la cinética, pruebas de crecimiento y efecto de inhibición in vitro de Lactobacillus lactis en Staphylococcus aureus, Staphylococcus epidermidis, Streptococcus agalactiae y Escherichia coli. Rev. Med. Vet. Zoot. 2015; 62: 40-56.
28. Leveau JY, Bouix M. Microbiología industrial: Los microorganismos de interés industrial. Ed. Acribia. Zaragoza, España. 2000. pp. 167-187, 206, 227-242.
29. Urbanska A, Bhathena J, Prakash S. Live encapsulated Lactobacillus acidophilus cells in yogurt for therapeutic oral delivery: Preparation and in vitro analysis of alginate-chitosan microcapsules. Canadian Journal of Physiology and Pharmacology 2007; 85(9):884-893.
30. Ávila J, Ávila M, Tovar B, Brizuela M, Perazzo Y, Hernández H. Capacidad probiótica de cepas del género Lactobacillus extraídas del tracto intestinal de animales de granja. Revista Científica 2010; 20(2), 161-170.
31. Del Piano M, Morelli L, Strozzi G, Allesina S, Barba M, Deidda F et al. Probiotics: From research to consumer. Digest. Liver Dis. 2006; 38(2): 248-255.
32. De Roissart H, Luquet FM. Bacteries lactiques Aspects Fondamentaux et Technologiques. 2 Ed. France: Lorica. 1994.
33. Prescott LM, Harley JP, Klein, DA. Microbiología. 4a ed., Ed. McGraw-Hill Interamericana. Zaragoza, España. 1999. pp. 515-518.
34. Klingberg TD.; Axelsson, L.; Naterstad, K.; Elsser, D. y Budde, B.B. (2005). Identification of potential probiotic starter cultures for scandinavian-type fermented sausages. International Journal of Food Microbiology, vol. 105, no. 3, p. 419-431,
35. Mora N, García A. Susceptibilidad de bacterias ácido lácticas (BAL) frente a diversos antibióticos. [Tesis Licenciado Química en Alimentos]. [Hidalgo, México] Universidad Autónoma del Estado de Hidalgo. 2007.
36. Jin LZ, Ho YW, Abdullah N, Jalaludin S. Acid and bile tolerance of Lactobacillus isolated from chicken intestine. Lett Appl Microbiol. 1998; 27:183-185.
37. Ronka E, Malinen E, Saarela M, Rinta-Koski M, Aarnikunnas J, Palva. A. Probiotic and milk technological properties of Lactobacillus brevis. Int. J. Food Microbiol. 2003; 83:63-7
38. Corcoran BM, Ross RP, Fitzgerald GF, Stanton C. Comparative survival of probiotic lactobacilli spraydried in the presence of prebiotic substances. J. Appl. Microbiol. 2004; 96:1024-1039
39. Pérez-Luyo A. Probióticos: ¿Una alternativa en la prevención de la caries dental? Rev Estomatol Herediana. [Internet]. [Citado 2013 abril 10]; 2008. 18 (1): 65-68. Disponible en: http://www.upch.edu.pe/vrinve/dugic/revistas/index.php/REH/article/viewF ile/1856/1865.
40. Dellaglio F, Felis GE, Torriani S, Sørensen K, Johansen E. Genomic characterisation of starter cultures. Probiotic Dairy Products 2005; 16-38.
41. Jurado-Gámez HA, Romero-Benavides DA, Morillo-Garcés JA. Inhibición de Lactobacillus gasseri sobre Yersinia pseudotuberculosis en condiciones in vitro. Revista de la Facultad de Medicina Veterinaria y Zootecnia 2016; 63(2), 95-112.
42. Mishra C, Lambert J. Production of antimicro- bial substances by probiotics. Asian Pacific J Clinic Nutr. 1996.
43. González A, Vaccari G, Dosi E, Trilli A, Rossi M, Matteuzzi D. Enhanced production of L(+) – lactic acid in chemostat by Lactobacillus casei DSM 20011 using ion – exchange resins and cross – flow filtration in a fully automated pilot plant controlled via. Biotechnology and Bioengineering 2000; 67(2): 147 – 156.
44. Foo EL, Griffin HG, Mollby R, Hedén CG. (Editors). The Lactic Acid Bacteria. Horizon Scientific Press. United Kingdom, 1993. pp. 89 – 91.
45. Leblanc JG, Matar C, Valdez JC, Leblanc J, Perdigon G. Immunomodulatory effects of peptidic fractions issued from milk fermented with Lactobacillus helveticus. Journal of Dairy Science 2002; 85:2733- 2742
46. Kawai Y, et al. Gassericin A; an uncommon cyclic bactericon produced by Lactobacillus gasseri LA39 linked at N- and C- terminal ends. Biosci Biotechnol Biochem. 1998; 62:2438-2440.
47. Trabi M, Craik Dj. Circular proteins-no end in sight. Trends Biochem. 2002. Sci. 27: 132-138.
48. Rivas L, Andreu D. Péptidos antimicrobianos eucarióticos: una nueva alternativa en clínica. Enferm. Infecc. Microbiol. Clin. 2003; 21: 358-365.
49. Maqueda M, Sánchez-Hidalgo M, Fernández M, Montalbán-López M, Valdivia E, Martínez-Bueno M. Genetic features of circular bacteriocins produced by Gram-positive bacteria. FEMS Microbiol Rev. 2008; 32:2-22.
50. Montalbán-López M, Sánchez-Hidalgo M, Cebrián R, Maqueda M. Discovering the bacterial circular proteins: bacteriocins, cyanobactins, and pilins. J Biol Chem. 2012; 287:27007- 27013
51. Sivonen K, Leikoski N, Fewer DP, Jokela J. Cyanobactins–ribosomal cyclic peptides produced by cyanobacteria. Appl. Microbiol. Biotechnol. 2010; 86:1213–1225.
2. Selle K, Klaenhammer TR. Genomic and Phenotypic Evidence for Probiotic Influences of Lactobacillus Gasseri on Human Health. FEMS Microbiology Reviews 2013; 37(6) 915-935.
3. Treven P, Turkova K, Trmcic A, Obermajer T, Rogelj I. Matijasic BB. Detection and quantification of probiotic strain Lactobacillus gasseri K7 in faecal samples by targeting bacteriocin genes. Folia Microbiol. 2013 (Praha); 58:623–630.
4. Yanagibashi T, Hosono A, Oyama A, Tsuda M, Hachimura S et al. Bacteroides induce higher IgA production than Lactobacillus by increasing activation-induced cytidine deaminase expression in B cells in murine Peyer’s patches. Biosci Biotechnol Biochem 2009; 73: 372–377 (traducido por los autores).
5. Taponen S, Pyörälä S. Coagulase-negative staphylococci as cause of bovine mastitis-Not so different from Staphylococcus aureus. 2009.
6. Sawant AA, Gillespie BE, Oliver SP Antimicrobial susceptibility of coagulase-negative Staphylococcus species isolated from bovine milk. 2008.
7. Crueger W, Crueger A. (1993). Biotecnología: manual de microbiología industrial. 3 ed. España: Ed. Acribia. 220 p.
8. Jurado-Gámez H, Calpa-Yama F, Chaspuengal-Tulcán A.. Determinación in vitro de la acción probiótica de Lactobacillus plantarum sobre Yersinia pseudotuberculosis aislada de Cavia porcellus. Rev. Fac. Med. Vet. Zoot. 2014; 61: 241-257.
9. Bauer AW, Kirby WM, Sherris JC, Turck M. (1966). Antibiotic susceptibility testing by a standardizedsingle disk method. American Journal of Clinical Pathology, 45, 493.
10. Tagg J, Mcgiven A. Assay system for Bacteriocins. Appl. Environ. Microb. 1971; 21: 943.
11. Klaenhammer TR. Genetics of bacteriocins produced by lactic acid bacteria FEMS Microbiology Reviews 1993; 12(1-3): 39-85.
12. Cai Y, Benno Y, Nakase T, Oh T. Specific probiotic characterization of Weissella hellenica DS-12 isolated from flounder intestine. J Gen Appl Microbiol. 1998; 44: 311-316.
13. Cai Y, Suyanandana P, Saman P, Benno Y. Classification and characterization of lactic acid bacteria isolated from the intestines of common carp and freshwater prawns. J Gen Appl Microbiol. 1999; 45: 177-184.
14. Dahl T, Midden W, Hartman P. (1989). Comparison of Killing of Gram-negative and Gram-positive Bacteria by Pure Singlet Oxygen. J Bacteriol. 171: 2188-2194.
15. Lanara, laboratório de referência animal. Métodos analíticos oficiáis para controle de produtos de origem animal e seus ingredientes. Ii- Métodos físico e químicos. Mel. Ministério da Agricultura. Brasília. 1981. 2 (25): 1-15.
16. Dubois M, Gilles K, Hamilton J, Rebers P, Smith F. Colorimetric method for determination of sugar and related substances. Anal Chem. 1956; 28:350-356.
17. Lowry O, Rosebroug N, Far A, Randall Rj. Protein measurement with the folin phenol reagent. J. Biological. Chemistry. 1951; 193: 265-75.
18. Teuber M, Meile L, Schwarz F. Acquired antibiotic resistance in lactic acid bacteria from food. Antonie van Leeuwenhoek 1999; 76 115-137.
19. Salyers AA, Gupta A, Wang Y. Human intestinal bacteria as reservoirs for antibiotic resistance genes. Trends Microbiol. 2004; 12 412–41610.1016/j.tim.2004.07.004
20. Hambleton P, Turnbull PCB. Anthrax vaccine development: a continuing story. Adv. Biotechnol. Processes. 1990; 13:105–122.
21. Zhou JS, Pillidge CJ, Gopal, PK, Gill HS. Antibiotic susceptibility profiles of new probiotic Lactobacillus and Bifidobacterium strains. International Journal of Food Microbiology 2005; 98(2), 211-217.
22. Benavides-Plascencia L, Aldama-Ojeda LA, Vázquez JH. Vigilancia de los niveles de uso de antibióticos y perfiles de resistencia bacteriana en hospitales de tercer nivel de la Ciudad de México. Salud Pública de México 2005; 47(3), 219-226.
23. Maranan MC, Moreira B, Boyle-Vavra S, Daum RS. Antimicrobial resistance in staphylococci: epidemiology, molecular mechanisms, and clinical relevance. Infectious Disease Clinics of North America 1997; 11(4), 813-849.
24. Rolfe DR. The role of probiotic cultures in the control of gastrointestinal health. J. Nutr. 2000; 130:396.
25. De Vuyst L. Growth kinetics and production of probiotic lactic acid bacteria strains: limitations and breakthroughs. Med. Fac. Landbouww. Univ. Gent. 1998; 63/4b:1511.
26. Feria Cáceres PF. Aislamiento y caracterización Bacteriocinas producidas por Lactobacillus plantarum LPBM10 en suero de leche. Tesis Msc Biotecnología. Universidad Nacional de Colombia, Facultad de Ciencias. Medellín - Colombia, 2007. p 84,
27. Jurado-Gámez H, Guzmán-Insuasty M, Jarrín-Jarrín V. Determinación de la cinética, pruebas de crecimiento y efecto de inhibición in vitro de Lactobacillus lactis en Staphylococcus aureus, Staphylococcus epidermidis, Streptococcus agalactiae y Escherichia coli. Rev. Med. Vet. Zoot. 2015; 62: 40-56.
28. Leveau JY, Bouix M. Microbiología industrial: Los microorganismos de interés industrial. Ed. Acribia. Zaragoza, España. 2000. pp. 167-187, 206, 227-242.
29. Urbanska A, Bhathena J, Prakash S. Live encapsulated Lactobacillus acidophilus cells in yogurt for therapeutic oral delivery: Preparation and in vitro analysis of alginate-chitosan microcapsules. Canadian Journal of Physiology and Pharmacology 2007; 85(9):884-893.
30. Ávila J, Ávila M, Tovar B, Brizuela M, Perazzo Y, Hernández H. Capacidad probiótica de cepas del género Lactobacillus extraídas del tracto intestinal de animales de granja. Revista Científica 2010; 20(2), 161-170.
31. Del Piano M, Morelli L, Strozzi G, Allesina S, Barba M, Deidda F et al. Probiotics: From research to consumer. Digest. Liver Dis. 2006; 38(2): 248-255.
32. De Roissart H, Luquet FM. Bacteries lactiques Aspects Fondamentaux et Technologiques. 2 Ed. France: Lorica. 1994.
33. Prescott LM, Harley JP, Klein, DA. Microbiología. 4a ed., Ed. McGraw-Hill Interamericana. Zaragoza, España. 1999. pp. 515-518.
34. Klingberg TD.; Axelsson, L.; Naterstad, K.; Elsser, D. y Budde, B.B. (2005). Identification of potential probiotic starter cultures for scandinavian-type fermented sausages. International Journal of Food Microbiology, vol. 105, no. 3, p. 419-431,
35. Mora N, García A. Susceptibilidad de bacterias ácido lácticas (BAL) frente a diversos antibióticos. [Tesis Licenciado Química en Alimentos]. [Hidalgo, México] Universidad Autónoma del Estado de Hidalgo. 2007.
36. Jin LZ, Ho YW, Abdullah N, Jalaludin S. Acid and bile tolerance of Lactobacillus isolated from chicken intestine. Lett Appl Microbiol. 1998; 27:183-185.
37. Ronka E, Malinen E, Saarela M, Rinta-Koski M, Aarnikunnas J, Palva. A. Probiotic and milk technological properties of Lactobacillus brevis. Int. J. Food Microbiol. 2003; 83:63-7
38. Corcoran BM, Ross RP, Fitzgerald GF, Stanton C. Comparative survival of probiotic lactobacilli spraydried in the presence of prebiotic substances. J. Appl. Microbiol. 2004; 96:1024-1039
39. Pérez-Luyo A. Probióticos: ¿Una alternativa en la prevención de la caries dental? Rev Estomatol Herediana. [Internet]. [Citado 2013 abril 10]; 2008. 18 (1): 65-68. Disponible en: http://www.upch.edu.pe/vrinve/dugic/revistas/index.php/REH/article/viewF ile/1856/1865.
40. Dellaglio F, Felis GE, Torriani S, Sørensen K, Johansen E. Genomic characterisation of starter cultures. Probiotic Dairy Products 2005; 16-38.
41. Jurado-Gámez HA, Romero-Benavides DA, Morillo-Garcés JA. Inhibición de Lactobacillus gasseri sobre Yersinia pseudotuberculosis en condiciones in vitro. Revista de la Facultad de Medicina Veterinaria y Zootecnia 2016; 63(2), 95-112.
42. Mishra C, Lambert J. Production of antimicro- bial substances by probiotics. Asian Pacific J Clinic Nutr. 1996.
43. González A, Vaccari G, Dosi E, Trilli A, Rossi M, Matteuzzi D. Enhanced production of L(+) – lactic acid in chemostat by Lactobacillus casei DSM 20011 using ion – exchange resins and cross – flow filtration in a fully automated pilot plant controlled via. Biotechnology and Bioengineering 2000; 67(2): 147 – 156.
44. Foo EL, Griffin HG, Mollby R, Hedén CG. (Editors). The Lactic Acid Bacteria. Horizon Scientific Press. United Kingdom, 1993. pp. 89 – 91.
45. Leblanc JG, Matar C, Valdez JC, Leblanc J, Perdigon G. Immunomodulatory effects of peptidic fractions issued from milk fermented with Lactobacillus helveticus. Journal of Dairy Science 2002; 85:2733- 2742
46. Kawai Y, et al. Gassericin A; an uncommon cyclic bactericon produced by Lactobacillus gasseri LA39 linked at N- and C- terminal ends. Biosci Biotechnol Biochem. 1998; 62:2438-2440.
47. Trabi M, Craik Dj. Circular proteins-no end in sight. Trends Biochem. 2002. Sci. 27: 132-138.
48. Rivas L, Andreu D. Péptidos antimicrobianos eucarióticos: una nueva alternativa en clínica. Enferm. Infecc. Microbiol. Clin. 2003; 21: 358-365.
49. Maqueda M, Sánchez-Hidalgo M, Fernández M, Montalbán-López M, Valdivia E, Martínez-Bueno M. Genetic features of circular bacteriocins produced by Gram-positive bacteria. FEMS Microbiol Rev. 2008; 32:2-22.
50. Montalbán-López M, Sánchez-Hidalgo M, Cebrián R, Maqueda M. Discovering the bacterial circular proteins: bacteriocins, cyanobactins, and pilins. J Biol Chem. 2012; 287:27007- 27013
51. Sivonen K, Leikoski N, Fewer DP, Jokela J. Cyanobactins–ribosomal cyclic peptides produced by cyanobacteria. Appl. Microbiol. Biotechnol. 2010; 86:1213–1225.
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