Lactobacillus salivarius: Bacteriocin and probiotic activity

Food Microbiology

Volumn 36, Issue 2, 2013, Pages 296-304

  Messaoudi, S ^a,b,c   Manai, M ^c   Kergourlay, G ^a,b   Prevost H ^a,b   Connil, N ^e   Chobert, J M ^d   Dousset, X ^a,b  

^a LUNAM UNIVERSITÉ   (France)

^b CEMAGREF   (France)

^c FACULTÉ DES SCIENCES DE TUNIS   (Tunisia)

^d INRA   (France)

^e UNIVERSITÉ DE ROUEN   (France)

Author keywords

Bacteriocins; Food safety; Lactobacillus salivarius; Probiotic

Indexed keywords

ANTIINFECTIVE AGENT; BACTERIOCIN; PROBIOTIC AGENT;

ANIMAL; CHICKEN; FOOD SAFETY; GASTROINTESTINAL TRACT; GENETICS; HUMAN; IMMUNOLOGY; ISOLATION AND PURIFICATION; LACTOBACILLUS; LACTOBACILLUS SALIVARIUS; METABOLISM; MICROBIOLOGY; REVIEW;

BACTERIOCINS; FOOD SAFETY; LACTOBACILLUS SALIVARIUS; PROBIOTIC;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIOCINS; CHICKENS; GASTROINTESTINAL TRACT; HUMANS; LACTOBACILLUS; PROBIOTICS;

EID: 84880660392     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2013.05.010     Document Type: Review

References (82)

1. Allison G., Fremaux C., Klaenhammer T. Expansion of bacteriocin activity and host range upon complementation of two peptides encoded within the lactacin F operon. Journal Of Bacteriology 1994, 176:2235-2241.
2. Anderssen E.L., Diep D.B., Nes I.F., Eijsink V.G.H., Nissen-Meyer J. Antagonistic activity of Lactobacillus plantarum C11: two new two-peptide bacteriocins, plantaricins EF and JK, and the induction factor plantaricin A. Applied and Environmental Microbiology 1998, 64:2269-2272.
3. Balakrishnan M., Simmonds R.S., Kilian M., Tagg J.R. Different bacteriocin activities of Streptococcus mutans reflect distinct phylogenetic lineages. Journal of Medical Microbiology 2002, 51:941-948.
4. Barrett E., Hayes M., O'Connor P., Gardiner G., Fitzgerald G.F., Stanton C., Ross R.P., Hill C. Salivaricin P, one of a family of two-component antilisterial bacteriocins produced by intestinal isolates of Lactobacillus salivarius. Applied and Environmental Microbiology 2007, 73:3719-3723.
5. Belguesmia Y., Nagmhmouchi K., Chihib N., Drider D. Class IIa bacteriocins: current knowledge and perspectives. Prokaryotic Antimicrobial Peptides 2011, 171-196. Springer, france. D. Drider, S. Rubuffat (Eds.).
6. Bennett P.M. Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteria. British Journal of Pharmacology 2008, 153:S347-S357.
7. Borriello S.P., Hammes W.P., Holzapfel W., Marteau P., Schrezenmeir J., Vaara M., Valtonen V. Safety of probiotics that contain lactobacilli or bifidobacteria. Clinical Infectious Diseases 2003, 36:775-780.
8. Busarcevic M., Dalgalarrondo M. Purification and genetic characterisation of the novel bacteriocin LS2 produced by the human oral strain Lactobacillus salivarius BGHO1. International Journal of Antimicrobial Agents 2012, 40:127-134.
9. Busarcevic M., Kojic M., Dalgalarrondo M., Chobert J.M., Haertlé T., Topisirovic L. Purification of bacteriocin LS1 produced by human oral isolate Lactobacillus salivarius BGHO1. Oral Microbiology and Immunology 2008, 23:254-258.
10. Calo-Mata P., Arlindo S., Boehme K., Miguel T., Pascoal A., Barros-Velazquez J. Current applications and future trends of lactic acid bacteria and their bacteriocins for the biopreservation of aquatic food products. Food and Bioprocess Technology 2008, 1:43-63.
11. Casey P.G., Casey G.D., Gardiner G.E., Tangney M., Stanton C., Ross R.P., Hill C., Fitzgerald G.F. Isolation and characterization of anti-Salmonella lactic acid bacteria from the porcine gastrointestinal tract. Letters in Applied Microbiology 2004, 39:431-438.
12. Corr S.C., Li Y., Riedel C.U., O'Toole P.W., Hill C., Gahan C.G. Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:7617-7621.
13. Cotter P.D., Hill C., Ross R.P. Bacteriocins: developing innate immunity for food. Nature Reviews Microbiology 2005, 3:777-788.
14. Cuozzo S.A., Castellano P., Sesma F.J.M., Vignolo G.M., Raya R.R. Differential roles of the two-component peptides of lactocin 705 in antimicrobial activity. Current Microbiology 2003, 46:180-183.
15. Delves-Broughton J. Nisin and its application as a food preservative. Journal of the Society of Dairy Technology 1990, 43.
16. Diep D.B., Axelsson L., Grefsli C., Nes I.F. The synthesis of the bacteriocin sakacin A is a temperature-sensitive process regulated by a pheromone peptide through a three-component regulatory system. Microbiology 2000, 146:2155-2160.
17. Diep D.B., Straume D., Kjos M., Torres C., Nes I.F. An overview of the mosaic bacteriocin pln loci from Lactobacillus plantarum. Peptides 2009, 30:1562-1574.
18. Dobson A., Cotter P., Ross P., Hill C. Bacteriocin production: a probiotic trait?. Applied and Environmental Microbiology 2012, 78:1-6.
19. Dunne C., O'Mahony L., Murphy L., Thornton G., Morrissey D., O'Halloran S., Feeney M., Flynn S., Fitzgerald G., Daly C., Kiely B., O'Sullivan G.C., Shanahan F., Collins J.K. Invitro selection criteria for probiotic bacteria of human origin: correlation with invivo findings. The American Journal of Clinical Nutrition 2001, 73:386s-392s.
20. Eijsink V.G., Skeie M., Middelhoven P.H., Brurberg M.B., Nes I.F. Comparative studies of class IIa bacteriocins of lactic acid bacteria. Applied and Environmental Microbiology 1998, 64:3275-3281.
21. Fayol-Messaoudi D., Berger C.N., Coconnier-Polter M.H., Lievin-Le Moal V., Servin A.L. pH-, lactic acid-, and non-lactic acid-dependent activities of probiotic Lactobacilli against Salmonella enterica serovar Typhimurium. Applied and Environmental Microbiology 2005, 71:6008-6013.
22. Fehrenbach E., Niess A.M., Veith R., Dickhuth H.-H., Northoff H. Changes of HSP72-expression in leukocytes are associated with adaptation to exercise under conditions of high environmental temperature. Journal of Leukocyte Biology 2001, 69:747-754.
23. Flynn S., van Sinderen D., Thornton G.M., Holo H., Nes I.F., Collins J.K. Characterization of the genetic locus responsible for the production of ABP-118, a novel bacteriocin produced by the probiotic bacterium Lactobacillus salivarius subsp. salivarius UCC118. Microbiology 2002, 148:973-984.
24. Galvez A., Abriouel H., Lopez R.L., Ben Omar N. Bacteriocin-based strategies for food biopreservation. International Journal of Food Microbiology 2007, 120:51-70.
25. Garneau S., Martin N.I., Vederas J.C. Two-peptide bacteriocins produced by lactic acid bacteria. Biochimie 2002, 84:577-592.
26. Helwig U., Lammers K.M., Rizzello F., Brigidi P., Rohleder V., Caramelli E., Gionchetti P., Schrezenmeir J., Foelsch U.R., Schreiber S., Campieri M. Lactobacilli, bifidobacteria and E.coli nissle induce pro- and anti-inflammatory cytokines in peripheral blood mononuclear cells. World Journal of Gastroenterology 2006, 12:5978-5986.
27. Jos F.J.G., Koninkxa J., Tooten Peter C.J., Malagob J. Probiotic bacteria induced improvement of the mucosal integrity of enterocyte-like Caco-2 cells after exposure to Salmonella enteritidis 857. Journal of Functional Foods 2010, 2:225-235.
28. Kirtzalidou E., Pramateftaki P., Kotsou M., Kyriacou A. Screening for lactobacilli with probiotic properties in the infant gut microbiota. Anaerobe 2011, 17:440-443.
29. Klaenhammer T.R. Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiology Reviews 1993, 12:39-85.
30. Klingberg T.D., Pedersen M.H., Cencic A., Budde B.B.r Application of measurements of transepithelial electrical resistance of intestinal epithelial cell monolayers to evaluate probiotic activity. Applied and Environmental Microbiology 2005, 71:7528-7530.
31. Lammers K.M., Helwig U., Swennen E., Rizzello F., Venturi A., Caramelli E., Kamm M.A., Brigidi P., Gionchetti P., Campieri M. Effect of probiotic strains on interleukin 8 production by HT29/19A cells. The American Journal of Gastroenterology 2002, 97:1182-1186.
32. Lara-Villoslada F., Sierra S., Diaz-Ropero M.P., Olivares M., Xaus J. Safety assessment of the human milk-isolated probiotic Lactobacillus salivarius CECT5713. Journal of Dairy Science 2007, 90:3583-3589.
33. Lavoie J.N., Gingras-Breton G., Tanguay R.M., Landry J. Induction of Chinese hamster HSP27 gene expression in mouse cells confers resistance to heat shock. HSP27 stabilization of the microfilament organization. Journal of Biological Chemistry 1993, 268:3420-3429.
34. Lee Y.K., Puong K.Y., Ouwehand A.C., Salminen S. Displacement of bacterial pathogens from mucus and Caco-2 cell surface by lactobacilli. Journal of Medical Microbiology 2003, 52:925-930.
35. Mack D.R., Ahrne S., Hyde L., Wei S., Hollingsworth M.A. Extracellular MUC3 mucin secretion follows adherence of Lactobacillus strains to intestinal epithelial cells invitro. Gut 2003, 52:827-833.
36. Madi A., Lakhdari O., Blottiere H.M., Guyard-Nicodeme M., Le Roux K., Groboillot A., Svinareff P., Dore J., Orange N., Feuilloley M.G., Connil N. The clinical Pseudomonas fluorescens MFN1032 strain exerts a cytotoxic effect on epithelial intestinal cells and induces Interleukin-8 via the AP-1 signaling pathway. BMC Microbiology 2010, 10:215.
37. Malago J.J., Koninkx J.F., van Dijk J.E. The heat shock response and cytoprotection of the intestinal epithelium. Cell Stress Chaperones 2002, 7:191-199.
38. Malago J., Tooten P., Koninkx J.F. Anti-inflammatory properties of probiotic bacteria on Salmonella-induced IL-8 synthesis in enterocyte-like Caco-2 cells. Beneficial Microbes 2010, 1:121-130.
39. Maldonado J., Lara-Villoslada F., Sierra S., Sempere L., Gomez M., Rodriguez J., Boza J., Xaus J., Olivares M. Safety and tolerance of the human milk probiotic strain Lactobacillus salivarius CECT5713 in 6-month-old children. Nutrition 2010, 26:1082-1087.
40. Marciset O., Jeronimus-Stratingh M.C., Mollet B., Poolman B. Thermophilin 13, a nontypical antilisterial poration complex bacteriocin, that functions without a receptor. Journal of Biological Chemistry 1997, 272:14277-14284.
41. Martan R., Jiménez E., Olivares M., Marin M.L., Fernandez L., Xaus J., Rodriguez J.M. Lactobacillus salivarius CECT 5713, a potential probiotic strain isolated from infant feces and breast milk of a mother-child pair. International Journal of Food Microbiology 2006, 112:35-43.
42. Marteau P., Minekus M., Havenaar R., Huis in't Veld J.H. Survival of lactic acid bacteria in a dynamic model of the stomach and small intestine: validation and the effects of bile. Journal of Dairy Science 1997, 80:1031-1037.
43. Martin-Visscher L.A., Van Bleulkum M.J., Vederas J.C. Class IIc or circular bacteriocins. Prokaryotic Antimicrobial Peptides 2011, 213-236. Springer, France. D. Drider, S. Rebuffat (Eds.).
44. McCormick J.K., Poon A., Sailer M., Gao Y., Roy K.L., McMullen L.M., Vederas J.C., Stiles M.E., Van Belkum M.J. Genetic characterization and heterologous expression of brochocin-C, an antibotulinal, two-peptide bacteriocin produced by Brochothrix campestris ATCC 43754. Applied and Environmental Microbiology 1998, 64:4757-4766.
45. Messaoudi S., Kergourlay G., Dalgalarrondo M., Choiset Y., Ferchichi M., Prévost H., Pilet M.-F., Chobert J.-M., Manai M., Dousset X. Purification and characterization of a new bacteriocin active against Campylobacter produced by Lactobacillus salivarius SMXD51. Food Microbiology 2012 (a), 32:129-134.
46. Messaoudi S., Kergourlay G., Rossero A., Ferchichi M., Prevost H., Drider D., Manai M., Dousset X. Identification of lactobacilli residing in chicken ceca with antagonism against Campylobacter. International Microbiology 2011, 14:103-110.
47. Messaoudi S., Madi A., Prévost H., Feuilloley M., Manai M., Dousset X., Connil N. Invitro evaluation of the probiotic potential of Lactobacillus salivarius SMXD51. Anaerobe 2012 (b), 18:584-589.
48. Miyauchi E., O'Callaghan J., Buttó L.F., Hurley G.i., Melgar S., Tanabe S., Shanahan F., Nally K., O'Toole P.W. Mechanism of protection of transepithelial barrier function by Lactobacillus salivarius: strain dependence and attenuation by bacteriocin production. American Journal of Physiology - Gastrointestinal and Liver Physiology 2012, 303:G1029-G1041.
49. Moll G., Hildeng-Hauge H., Nissen-Meyer J., Nes I.F., Konings W.N., Driessen A.J.M. Mechanistic properties of the two-component bacteriocin lactococcin G. Journal of Bacteriology 1998, 180:96-99.
50. Moll G.N., van den Akker E., Hauge H.H., Nissen-Meyer J., Nes I.F., Konings W.N., Driessen A.J.M. Complementary and overlapping selectivity of the two-peptide bacteriocins plantaricin EF and JK. Journal of Bacteriology 1999, 181:4848-4852.
51. Neville B., O'Toole P. Probiotic properties of Lactobacillus salivarius and closely related Lactobacillus species. Future Microbiology 2010, 5:759-774.
52. Nissen-Meyer J., Holo H., Havarstein L.S., Sletten K., Nes I.F. Anovel lactococcal bacteriocin whose activity depends on the complementary action of two peptides. Journal of Bacteriology 1992, 174:5686-5692.
53. Nissen-Meyer J., Rogne P., Oppegard C., Haugen H.S., Kristiansen P.E. Structure-function relationships of the non-lanthionine-containing peptide (class II) bacteriocins produced by gram-positive bacteria. Current Pharmaceutical Biotechnology 2009, 10:19-37.
54. O'Flaherty S., Klaenhammer T.R. The role and potential of probiotic bacteria in the gut, and the communication between gut microflora and gut/host. International Dairy Journal 2009, 20:262-268.
55. O'Shea E.F., O'Connor P.M., Raftis E.J., O'Toole P.W., Stanton C., Cotter P.D., Ross R.P., Hill C. Production of multiple bacteriocins from a single locus by gastrointestinal strains of Lactobacillus salivarius. Journal of Bacteriology 2011, 193:6973-6982.
56. O'Sullivan L., Ross R.P., Hill C. Potential of bacteriocin-producing lactic acid bacteria for improvements in food safety and quality. Biochimie 2002, 84:593-604.
57. Ocana V., Pesce de Ruiz Holgado A., Nader-Macas M. Characterization of a bacteriocin-like substance produced by a vaginal Lactobacillus salivarius strain. Applied and Environmental Microbiology 1999, 65:5631-5635.
58. Ohland C.L., MacNaughton W.K. Probiotic bacteria and intestinal epithelial barrier function. American Journal of Physiology - Gastrointestinal and Liver Physiology 2010, 298:G807-G819.
59. Olivares M., Diaz-Ropero M.P., Martin R., Rodriguez J.M., Xaus J. Antimicrobial potential of four Lactobacillus strains isolated from breast milk. Journal of Applied Microbiology 2006, 101:72-79.
60. Oppegard C., Rogne P., Emanuelsen L., Kristiansen P.E., Fimland G., Nissen-Meyer J. The two-peptide class II bacteriocins: structure, production, and mode of action. Journal of Molecular Microbiology and Biotechnology 2007, 13:210-219.
61. Papagianni M. Ribosomally synthesized peptides with antimicrobial properties: biosynthesis, structure, function, and applications. Biotechnology Advances 2003, 21:465-499.
62. Pérez-Cano F.J., Dong H., Yaqoob P. Invitro immunomodulatory activity of Lactobacillus fermentum CECT5716 and Lactobacillus salivarius CECT5713: two probiotic strains isolated from human breast milk. Immunobiology 2010, 215:996-1004.
63. Peschel A., Sahl H.G. The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nature Reviews Microbiology 2006, 529-536.
64. Pilasombut K., Sakpuaram T., Wajjwalku W., Nitisinprasert S., Swetwiwathana A., Zendo T., Fujita K., Nakayama J., Sonomoto K. Purification and amino acid sequence of a bacteriocins produced by Lactobacillus salivarius K7 isolated from chicken intestine. Nutraceutical and Functional Food 2006, 28:121-131.
65. Pridmore R.D., Pittet A.C., Praplan F., Cavadini C. Hydrogen peroxide production by Lactobacillus johnsonii NCC 533 and its role in anti-Salmonella activity. FEMS Microbiology Letters 2008, 283:210-215.
66. Reid G. The importance of guidelines in the development and application of probiotics. Current Pharmaceutical Design 2005, 11:11-16.
67. Riboulet-Bisson E., Sturme M.H.J., Jeffery I.B., O'Donnell M.M., Neville B.A., Forde B.M., Claesson M.J., Harris H., Gardiner G.E., Casey P.G., Lawlor P.G., O'Toole P.W., Ross R.P. Effect of Lactobacillus salivarius bacteriocin Abp118 on the mouse and pig intestinal microbiota. PLoS One 2012, 7:e31113.
68. Ryan K.A., O'Hara A.M., van Pijkeren J.P., Douillard F.P., O'Toole P.W. Lactobacillus salivarius modulates cytokine induction and virulence factor gene expression in Helicobacter pylori. Journal of Medical Microbiology 2009, 58:996-1005.
69. Ryan M.P., Rea M.C., Hill C., Ross R.P. An application in cheddar cheese manufacture for a strain of Lactococcus lactis producing a novel broad-spectrum bacteriocin, lacticin 3147. Applied and Environmental Microbiology 1996, 62:612-619.
70. Sanders M.E., Akkermans L.M., Haller D., Hammerman C., Heimbach J., Hormannsperger G., Huys G., Levy D.D., Lutgendorff F., Mack D., Phothirath P., Solano-Aguilar G., Vaughan E. Safety assessment of probiotics for human use. Gut Microbes 2010, 1:164-185.
71. Schlee M., Harder J., Köten B., Stange E.F., Wehkamp J., Fellermann K. Probiotic lactobacilli and VSL#3 induce enterocyte β-defensin 2. Clinical & Experimental Immunology 2008, 151:528-535.
72. Sierra S., Lara-Villoslada F., Sempere L., Olivares M., Boza J., Xaus J. Intestinal and immunological effects of daily oral administration of Lactobacillus salivarius CECT5713 to healthy adults. Anaerobe 2010, 16:195-200.
73. Simon L., Fremaux C., Cenatiempo Y., Berjeaud J.M. Sakacin G, a new type of antilisterial bacteriocin. Applied and Environmental Microbiology 2002, 68:6416-6420.
74. Stern N.J., Eruslanov B.V., Pokhilenko V.D., Kovalev Y.N., Volodina L.L., Perelygin V.V., Mitsevich E.V., Mitsevich I.P., Borzenkov V.N., Levchuk V.P., Svetoch O.E., Stepanshin Y.G., Svetoch E.A. Bacteriocins reduce Campylobacter jejuni colonization while bacteria producing bacteriocins are ineffective. Microbial Ecology in Health and Disease 2008, 20:74-79.
75. Stern N.J., Svetoch E.A., Eruslanov B.V., Perelygin V.V., Mitsevich E.V., Mitsevich I.P., Pokhilenko V.D., Levchuk V.P., Svetoch O.E., Seal B.S. Isolation of a Lactobacillus salivarius strain and purification of its bacteriocin, which is inhibitory to Campylobacter jejuni in the chicken gastrointestinal system. Antimicrobial Agents and Chemotherapy 2006, 50:3111-3116.
76. Svetoch E.A., Eruslanov B.V., Levchuk V.P., Perelygin V.V., Mitsevich E.V., Mitsevich I.P., Stepanshin J., Dyatlov I., Seal B.S., Stern N.J. Isolation of Lactobacillus salivarius 1077 (NRRL B-50053) and characterization of its bacteriocin, including the antimicrobial activity spectrum. Applied and Environmental Microbiology 2011, 77:2749-2754.
77. Tichaczek P.S., Vogel R.F., Hammes W.P. Cloning and sequencing of sakP encoding sakacin P, the bacteriocin produced by Lactobacillus sake LTH 673. Microbiology 1994, 140:361-367.
78. Vera Pingitore E., Hébert E.M., Nader-Macías M.E., Sesma F. Characterization of salivaricin CRL 1328, a two-peptide bacteriocin produced by Lactobacillus salivarius CRL 1328 isolated from the human vagina. Research in Microbiology 2009, 160:401-408.
79. Walsh M.C., Gardiner G.E., Hart O.M., Lawlor P.G., Daly M., Lynch B., Richert B.T., Radcliffe S., Giblin L., Hill C., Fitzgerald G.F., Stanton C., Ross P. Predominance of a bacteriocin-producing Lactobacillus salivarius component of a five-strain probiotic in the porcine ileum and effects on host immune phenotype. FEMS Microbiology Ecology 2008, 64:317-327.
80. Wirawan R.E., Klesse N.A., Jack R.W., Tagg J.R. Molecular and genetic characterization of a novel nisin variant produced by Streptococcus uberis. Applied and Environmental Microbiology 2006, 72:1148-1156.
81. Zendo T., Koga S., Shigeri Y., Nakayama J., Sonomoto K. Lactococcin Q, a novel two-peptide bacteriocin produced by Lactococcus lactis QU 4. Applied and Environmental Microbiology 2006, 72:3383-3389.
82. Zhang J., Deng J., Wang Z., Che C., Li Y.F., Yang Q. Modulatory effects of Lactobacillus salivarius on intestinal mucosal immunity of piglets. Current Microbiology 2011, 62:1623-1631.