Use of Lactobacillus plantarum strains as a bio-control strategy against food-borne pathogenic microorganisms

Frontiers in Microbiology

Volumn 7, Issue APR, 2016, Pages

  Arena, Mattia Pia ^a   Silvain, Amandine ^b   Normanno, Giovanni ^a   Grieco, Francesco ^c   Drider, Djamel ^b   Spano, Giuseppe ^a   Fiocco, Daniela ^a  

^a UNIVERSITY OF FOGGIA   (Italy)

^b Université de Lille 1 Sciences et Technologies   (France)

^c CNR   (Italy)

Author keywords

Antimicrobial compounds; Cell free supernatant (CFS); Inhibiting activity; Lactobacillus plantarum; Organic acid; Pathogens

Indexed keywords

CATALASE; PROTEINASE;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CELL FREE SYSTEM; CLUSTER ANALYSIS; CONTROLLED STUDY; ESCHERICHIA COLI; FOOD POISONING; FREEZE DRYING; HEATING; LACTOBACILLUS PLANTARUM; LISTERIA MONOCYTOGENES; NONHUMAN; PH; SALMONELLA ENTERICA SEROVAR ENTERITIDIS; STAPHYLOCOCCUS AUREUS;

EID: 84966349726     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00464     Document Type: Article

References (52)

1. Adebayo, F. A., Afolabi, O. R., and Akintokun, A. K. (2014). Antimicrobial properties of purified bacteriocins produced from Lactobacillus casei and Lactobacillus fermentum against selected pathogenic microorganisms. Br. J. Med. Med. Res. 4, 3415-3431. doi: 10.9734/BJMMR/2014/8584
2. Alakomi, H. L., Skyttä, E., Saarela, M., Mattila-Sandholm, T., Latva-Kala, K., and Helander, I. M. (2000). Lactic acid permeabilizes gram-negative bacteria by disrupting the outer membrane. Appl. Environ. Microbiol. 66, 2001-2005. doi: 10.1128/AEM.66.5.2001-2005.2000
3. Al Kassaa, I., Hamze, M., Hober, D., Chihib, N. E., and Drider, D. (2014). Identification of vaginal lactobacilli with potential probiotic properties isolated from women in North Lebanon. Microb. Ecol. 67, 722-734. doi: 10.1007/s00248-014-0384-7
4. Altay, F., Karbancioglu-Güler, F., Daskaya-Dikmen, C., and Heperkan, D. (2013). A review on traditional Turkish fermented non-alcoholic beverages: microbiota, fermentation process and quality characteristics. Int. J. Food Microbiol. 167, 44-56. doi: 10.1016/j.ijfoodmicro.2013.06.016
5. Annuk, H., Shchepetova, J., Kullisaar, T., Songisepp, E., Zilmer, M., and Mikelsaar, M. (2003). Characterization of intestinal lactobacilli as putative probiotic candidates. J. Appl. Microbiol. 94, 403-412. doi: 10.1046/j.1365-2672.2003.01847.x
6. Arena, M. P., Caggianiello, G., Russo, P., Albenzio, M., Massa, S., Fiocco, D., et al. (2015). Functional starters for functional yogurt. Foods 4, 15-33. doi: 10.3390/foods4010015
7. Arena, M. P., Fiocco, D., Massa, S., Capozzi, V., and Russo, P. (2014). Lactobacillus plantarum as a strategy for an in situ production of vitamin B2. J. Food. Nutr. Disord. S1, 4. doi: 10.4172/2324-9323
8. Batish, V. K., Roy, U., Lal, R., and Grower, S. (1997). Antifungal attributes of lactic acid bacteria-a review. Crit. Rev. Biotechnol. 17, 209-225. doi: 10.3109/07388559709146614
9. Bermudez-Brito, M., Muñoz-Quezada, S., Gomez-Llorente, C., Matencio, E., Bernal, M. J., Romero, F., et al. (2013). Cell-free culture supernatant of Bifidobacterium breve CNCM I-4035 decreases pro-inflammatory cytokines in human dendritic cells challenged with Salmonella typhi through TLR activation. PLoS ONE 8:e59370. doi: 10.1371/journal.pone.0059370
10. Bilkova, A., Sepova, H. K., Bukovsky, M., and Bezakova, L. (2011). Antibacterial potential of lactobacilli isolated from a lamb. Vet. Med. 56, 319-324
11. Cebeci, A., and Gürakan, C. (2003). Properties of potential probiotic Lactobacillus plantarum strains. Food Microbiol. 20, 511-518. doi: 10.1016/S0740-0020(02)00174-0
12. Cortés-Zavaleta, O., López-Malo, A., Hernández-Mendoza, A., and García, H. S. (2014). Antifungal activity of lactobacilli and its relationship with 3-phenyllactic acid production. Int. J. Food Microbiol. 173, 30-35. doi: 10.1016/j.ijfoodmicro.2013.12.016
13. Dalié, D. K. D., Deschamps, A. M., and Richard-Forget, F. (2010). Lactic acid bacteria-Potential for control of mould growth and mycotoxins: a review. Food Control 21, 370-380. doi: 10.1016/j.foodcont.2009.07.011
14. da Silva Sabo, S., Vitolo, M., González, J. M. D., and de Souza Oliveira, R. P. (2014). Overview of Lactobacillus plantarum as a promising bacteriocin producer among lactic acid bacteria. Food Res. Int. 64, 527-536. doi: 10.1016/j.foodres.2014.07.041
15. De Keersmaecker, S. C., Verhoeven, T. L., Desair, J., Marchal, K., Vanderleyden, J., and Nagy, I. (2006). Strong antimicrobial activity of Lactobacillus rhamnosus GG against Salmonella typhimurium is due to accumulation of lactic acid. FEMS Microbiol. Lett. 259, 89-96. doi: 10.1111/j.1574-6968.2006.00250.x
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. doi: 10.1159/000104752
17. Escamilla, J., Lane, M. A., and Maitin, V. (2012). Cell-free supernatants from probiotic Lactobacillus casei and Lactobacillus rhamnosus GG decrease colon cancer cell invasion in vitro. Nutr. Cancer 64, 871-878. doi: 10.1080/01635581.2012.700758
18. Fan, L., and Song, J. (2013). "Antimicrobial microbes-bacteriocin producing lactic acid bacteria", in Microbial pathogens and strategies for combating them: science, technology and education, ed. A. Méndez-Vilas (Badajoz, ES: Formatex Research Center), 899-909
19. Gaudana, S. B., Dhanani, A. S., and Bagchi, T. (2010). Probiotic attributes of Lactobacillus strains isolated from food and of human origin. Br. J. Nutr. 103, 1620-1628. doi: 10.1017/S0007114509993643
20. Georgieva, R., Iliev, I., Haertlé, T., Chobert, J.-M., Ivanova, I., and Danova, S. (2009). Technological properties of candidate probiotic Lactobacillus plantarum strains. Int. Dairy J. 19, 696-702. doi: 10.1016/j.idairyj.2009.06.006
21. Gerbaldo, G. A., Barberis, C., Pascual, L., Dalcero, A., and Barberis, L. (2012). Antifungal activity of two Lactobacillus strains with potential probiotic properties. FEMS Microbiol. Lett. 332, 27-33. doi: 10.1111/j.1574-6968.2012.02570.x
22. Guidone, A., Zotta, T., Ross, R. P., Stanton, C., Rea, M. C., Parente, E., et al. (2014). Functional properties of Lactobacillus plantarum strains: A multivariate screening study. LWT-Food Sci. Tech. 56, 69-76. doi: 10.1016/j.lwt.2013.10.036
23. Guo, X. H., Kim, J. M., Nam, H. M., Park, S. Y., and Kim, J. M. (2010). Screening lactic acid bacteria from swine origins for multistrain probiotics based on in vitro functional properties. Anaerobe 16, 321-326. doi: 10.1016/j.anaerobe.2010.03.006
24. Gupta, R., and Srivastava, S. (2014). Antifungal effect of antimicrobial peptides (AMPs LR14) derived from Lactobacillus plantarum strain LR/14 and their applications in prevention of grain spoilage. Food Microbiol. 42, 1-7. doi: 10.1016/j.fm.2014.02.005
25. Gutiérrez-Larraínzar, M., Rúa, J., Caro, I., de Castro, C., de Arriaga, D., García-Armesto, M. R., et al. (2012). Evaluation of antimicrobial and antioxidant activities of natural phenolic compounds against foodborne pathogens and spoilage bacteria. Food Control 26, 555-563. doi: 10.1016/j.foodcont.2012.02.025
26. Hartmann, H. A., Wilke, T., and Erdmann, R. (2011). Efficacy of bacteriocin-containing cell-free culture supernatants from lactic acid bacteria to control Listeria monocytogenes in food. Int. J. Food Microb. 146, 192-199. doi: 10.1016/j.ijfoodmicro.2011.02.031
27. Herreros, M. A., Sandoval, H., González, L., Castro, J. M., Fresno, J. M., and Tornadijo, M. E. (2005). Antimicrobial activity and antibiotic resistance of lactic acid bacteria isolated from Armada cheese (a Spanish goats' milk cheese). Food Microbiol. 22, 455-459. doi: 10.1016/j.fm.2004.11.007
28. Joong-Su, L., Myung-Jun, C., and Jae-Gu, S. (2013). In vitro evaluation of antimicrobial activity of lactic acid bacteria against Clostridium difficile. Toxicol. Res. 29, 99-106. doi: 10.5487/TR.2013.29.2.099
29. Kecerová, K., Pristaš, P., and Javorskỳ, P. (2004). Bacteriocin production and sensitivity. Folia Microbiol. 49, 172-174. doi: 10.1007/BF02931395
30. Kim, Y., Whang, J. Y., Whang, K. Y., Oh, S., and Kim, S. H. (2008). Characterization of the cholesterol-reducing activity in a cell-free supernatant of Lactobacillus acidophilus ATCC 43121. Biosci. Biotechnol. Biochem. 72, 1483-1490. doi: 10.1271/bbb.70802
31. Kos, B., Beganovic, J., Jurašic, L., Švadumovic, M., Leboš Pavunc, A., Uroic, K., et al. (2011). Coculture-inducible bacteriocin biosynthesis of different probiotic strains by dairy starter culture Lactococcus lactis. Mljekarstvo 61, 273-282
32. Liu, W., Liu, B., Zhu, X., Yu, S., and Shi, X. (2011). Diversity of Salmonella isolates using serotyping and multilocus sequence typing. Food Microbiol. 28, 1182-1189. doi: 10.1016/j.fm.2011.04.001
33. Mayrhofer, S., Domig, K. J., Mair, C., Zitz, U., Huys, G., and Kneifel, W. (2008). Comparison of broth microdilution, Etest, and agar disk diffusion methods for antimicrobial susceptibility testing of Lactobacillus acidophilus group members. Appl. Environ. Microbiol. 74, 3745-3748. doi: 10.1128/AEM.02849-07
34. Mead, P. S., and Griffin, P. M. (1998). Escherichia coli O157:H7. Lancet 352, 1207-1212. doi: 10.1016/S0140-6736(98)01267-7
35. Mu, W., Yu, S., Zhu, L., Zhang, T., and Jiang, B. (2012). Recent research on 3-phenyllactic acid, a broad-spectrum antimicrobial compound. Appl. Microbiol. Biotechnol. 95, 1155-1163. doi: 10.1007/s00253-012-4269-8
36. Neal-McKinney, J. M., Lu, X., Duong, T., Larson, C. L., Call, D. R., Shah, D. H., et al. (2012). Production of organic acids by probiotic lactobacilli can be used to reduce pathogen load in poultry. PLoS ONE 9:e43928. doi: 10.1371/journal.pone.0043928
37. Nousiainen, J., Javanainen, P., Setala, J., and von Wright, A. (2004). "20 Lactic acid bacteria as animal probiotics, " in Lactic Acid Bacteria: Microbial and Functional Aspects, 3rd Edn, eds S. Salminen, A. Ouwehand, and A. von Wright (New York, NY: Marcel Dekker), 547-580
38. Pawlowska, A. M., Zannini, E., Coffey, A., and Arendt, E. K. (2012). "Green preservatives": combating fungi in the food and feed industry by applying antifungal lactic acid bacteria. Adv. Food Nutr. Res. 66, 217-238. doi: 10.1016/B978-0-12-394597-6.00005-7
39. Reis, J. A., Paula, A. T., Casarotti, S. N., and Penna, A. L. B. (2012). Lactic acid bacteria antimicrobial compounds: characteristics and applications. Food Eng. Rev. 4, 124-140. doi: 10.1007/s12393-012-9051-2
40. Rodríguez-Pazo, N., Vázquez-Araújo, L., Pérez-Rodríguez, N., Cortés-Diéguez, S., and Domínguez, J. M. (2013). Cell-free supernatants obtained from fermentation of cheese whey hydrolyzates and phenylpyruvic acid by Lactobacillus plantarum as a source of antimicrobial compounds, bacteriocins, and natural aromas. Appl. Biochm. Biotechnol. 171, 1042-1060. doi: 10.1007/s12010-013-0408-7
41. Saadatzadeh, A., Fazeli, M. R., Jamalifar, H., and Dinarvand, R. (2013). Probiotic properties of Lyophilized cell free extract of Lactobacillus casei. Jundishapur J. Nat. Pharm. Prod. 8, 131-137. doi: 10.17795/jjnpp-8564
42. Saavedra, L., Minahk, C., Holgado, A. P., and Sesma, F. (2004). Enhancement of the enterocin CRL35 activity by a synthetic peptide derived from the NH2-terminal sequence. Antimicrob. Agents Chemother. 48, 2778-2781. doi: 10.1128/AAC.48.7.2778-2781.2004
43. Schillinger, U., and Villareal, J. V. (2010). Inhibition of Penicillium nordicum in MRS medium by lactic acid bacteria isolated from foods. Food Control 21, 107-111. doi: 10.1016/j.foodcont.2008.11.010
44. Sip, A., Wieckowicz, M., Olejnik-Schmidt, A., and Grajek, W. (2012). Anti-Listeria activity of lactic acid bacteria isolated from golka, a regional cheese produced in Poland. Food Control 26, 117-124. doi: 10.1016/j.foodcont.2012.01.014
45. Sobrino-Lopez, A., and Martin-Belloso, O. (2008). Review: use of nisin and other bacteriocins for preservation of dairy products. Int. Dairy J. 18, 329-343. doi: 10.1016/j.idairyj.2007.11.009
46. Šuškovic, J., Kos, B., Beganovic, J., Leboš Pavunc, A., Habjanic, K., and Matošic, S. (2010). Antimicrobial activity-the most important property of probiotic and starter lactic acid bacteria. Food Techn. Biotechnol. 48, 296-307
47. Tejero-Sariñena, S., Barlow, J., Costabile, A., Gibson, G. R., and Rowland, I. (2012). In vitro evaluation of the antimicrobial activity of a range of probiotics against pathogens: evidence for the effects of organic acids. Anaerobe 18, 530-538. doi: 10.1016/j.anaerobe.2012.08.004
48. Tharmaraj, N., and Shah, N. P. (2009). Antimicrobial effects of probiotics against selected pathogenic and spoilage bacteria in cheese-based dips. Int. Food Res. J. 16, 261-276
49. Topisirovic, L., Veljovic, K., Terzic Vidojevic, A., Strahinic, I., and Kojic, M. (2007). Comparative analysis of antimicrobial and proteolytic activity of lactic acid bacteria isolated from Zlatar cheese. Genetika 39, 125-138. doi: 10.2298/GENSR0702125T
50. Toy, N., Özogul, F., and Özogul, Y. (2015). The influence of the cell free solution of lactic acid bacteria on tyramine production by food borne-pathogens in tyrosine decarboxylase broth. Food Chem. 173, 45-53. doi: 10.1016/j.foodchem.2014.10.001
51. Wang, G., Zhao, Y., Tian, F., Jin, X., Chen, H., Liu, X., et al. (2014). Screening of adhesive lactobacilli with antagonistic activity against Campylobacter jejuni. Food Control 44, 49-57. doi: 10.1016/j.foodcont.2014.03.042
52. Zhang, Y., Zhang, L., Du, M., Yi, H., Guo, C., Tuo, Y., et al. (2011). Antimicrobial activity against Shigella sonnei and probiotic properties of wild lactobacilli from fermented food. Microbiol. Res. 167, 27-31. doi: 10.1016/j.micres.2011.02.006