Quorum-Sensing Regulation of Constitutive Plantaricin by Lactobacillus plantarum Strains under a Model System for Vegetables and Fruits

Applied and Environmental Microbiology

Volumn 80, Issue 2, 2014, Pages 777-787

  Rizzello, Carlo G ^a   Filannino, Pasquale ^a   Di Cagno, Raffaella ^a   Calasso, Maria ^a   Gobbetti, Marco ^a  

^a UNIVERSITY OF BARI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-MICROBIAL ACTIVITY; ANTIMICROBIAL COMPOUNDS; LACTOBACILLUS PLANTARUM; MASS SPECTROMETRY ANALYSIS; REAL-TIME PCR ASSAY; REGULATORY MECHANISM; REVERSE PHASE HIGH-PERFORMANCE LIQUID CHROMATOGRAPHY; VEGETABLES AND FRUITS;

ALGAE; BACILLI; FRUITS; GENES; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MICROORGANISMS; PEPTIDES; POLYMERASE CHAIN REACTION; POLYSACCHARIDES;

VEGETABLES;

BACTERIUM; BIOASSAY; FRUIT; GENE EXPRESSION; GROWTH RATE; POLYMERASE CHAIN REACTION; REAL TIME; VEGETABLE;

ANTIINFECTIVE AGENT; BACTERIOCIN; PLANTARICIN JK;

ANANAS; ARTICLE; BACTERIAL GENE; CARROT; ELECTROSPRAY MASS SPECTROMETRY; FRUIT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; LACTOBACILLUS PLANTARUM; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; QUORUM SENSING; VEGETABLE;

ANANAS; ANTI-INFECTIVE AGENTS; BACTERIOCINS; DAUCUS CAROTA; FRUIT; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; LACTOBACILLUS PLANTARUM; QUORUM SENSING; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; VEGETABLES;

EID: 84892460001     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03224-13     Document Type: Article

References (75)

1. Nissen-Meyer J, Nes IF. 1997. Ribosomally synthesized antimicrobial peptides: their function, structure, biogenesis, and mechanism of action. Arch. Microbiol. 167:67-77.
2. Jack R, Tagg JR, Ray B. 1995. Bacteriocins of Gram-positive bacteria. Microbiol. Rev. 59:171-200.
3. Klaenhammer TR. 1993. Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol. Rev. 12:39-86.
4. Tagg JR, Dajani AS, Wannamaker LW. 1976. Bacteriocins of grampositive bacteria. Bacteriol. Rev. 40:722-756.
5. Daeschel MA. 1993. Applications and interactions of bacteriocins from lactic acid bacteria in foods and beverages, p 63-91. In Hoover DG, Steenson LR (ed), Bacteriocins of lactic acid bacteria. Academic Press, Inc., New York, NY.
6. de Vuyst L, Vandamme EJ. 1994. Antimicrobial potential of lactic acid bacteria, p 91-142. In de Vuyst L, Vandamme EJ (ed), Bacteriocins of lactic acid bacteria: microbiology, genetics and applications. Blackie Academic & Professional, London, United Kingdom.
7. Cotter PD, Hill C, Ross RP. 2005. Bacteriocins: developing innate immunity for food. Nat. Rev. Microbiol. 3:777-788. http://dx.doi.org/10.1038/nrmicro1273.
8. Heng NCK, Wescombre PA, Burton JP, Jack RW, Tagg JR. 2007. The diversity of bacteriocins in gram-positive bacteria, p 45-92. In Bacteriocins. Springer, Berlin, Germany.
9. Eijsink VGH, Axelsson L, Diep DB, Havarstein LS, Holo H, Nes IF. 2002 Production of class II bacteriocins by lactic acid bacteria; an example of biological warfare and communication. Antonie van Leeuwenhoek 81: 639-654. http://dx.doi.org/10.1023/A:1020582211262.
10. Ennahar S, Sashihara T, Sonomoto K, Ishizaki A. 2000. Class IIa bacteriocins: biosynthesis, structure and activity. FEMS Microbiol. Rev. 24:85- 106. http://dx.doi.org/10.1016/S0168-6445(99)00031-5.
11. Havarstein LS, Diep DB, Nes IF. 1995. A family of bacteriocin ABC transporters carry out proteolytic processing of their substrates concomitant with export. Mol. Microbiol. 16:229-240.
12. Callewaert R, De Vuyst L. 2000. Bacteriocin production with Lactobacillus amylovorus DCE 471 is improved and stabilized by fed-batch fermentation. Appl. Environ. Microbiol. 66:606-613. http://dx.doi.org/10.1128/AEM.06.606-613.2000.
13. Son MR, Shchepetov M, Adrian PV, Madhi SA, de Gouveia L, von Gottberg A, Klugman KP, Weiser JN, Dawida S. 2011. Conserved mutations in the pneumococcal bacteriocin transporter gene, blpA, result in a complex population consisting of producers and cheaters. mBio 2(5): 1-9. http://dx.doi.org/10.1128/mBio.00179-11.
14. Kleerebezem M, Quadri LEN, Kuipers OP, de Vos WM. 1997. Quorum sensing by peptide pheromones and two-component signal-transduction systems in gram-positive bacteria. Mol. Microbiol. 24:895-904.
15. Kleerebezem M, Quadri LEN. 2001. Peptide pheromone-dependent regulation of antimicrobial peptide production in Gram-positive bacteria: a case of multicellular behavior. Peptides 22:1579-1596. http://dx.doi.org/10.1016/S0196-9781(01)00493-4.
16. Nes IF, Eijsink VGH. 1999. Regulation of group II peptide bacteriocin synthesis by quorum sensing mechanisms, p 175-192. In Dunny GM, Winans SC (ed), Cell-cell signaling in bacteria. American Society for Microbiology, Washington, DC.
17. Diep DB, Havarstein LS, Nes IF. 1995. A bacteriocin-like peptide induces bacteriocin synthesis in Lactobacillus plantarum C11. Mol. Microbiol. 18: 631-639.
18. Diep DB, Axelsson L, Grefsli C, Nes IF. 2000. The synthesis of the bacteriocin sakacin A is a temperature-sensitive process regulated by a pheromone peptide through a three-component regulatory system. Microbiology 146:2155-2160.
19. Eijsink VGH, Brurberg MB, Middelhoven PH, Nes IF. 1996. Induction of bacteriocin production in Lactobacillus sake by a secreted peptide. J. Bacteriol. 178:2232-2237.
20. Bárcena JMB, Sineriz F, De Llano DG, Rodrìguez A, Suàrez JE. 1998. Chemostat production of plantaricin C by Lactobacillus plantarum LL441. Appl. Environ. Microbiol. 64:3512-3514.
21. Fan L, Truelstrup Hansen L. 2012. Fermentation and biopreservation of plant based foods with lactic acid bacteria, p 35-48. In Hui YH (ed), Handbook of plant-based fermented food and beverage technology, 2nd ed. CRC Press, Boca Raton, FL.
22. Bringel F, Curk MC, Hubert JC. 1996. Characterization of lactobacilli by Southern-type hybridization with a Lactobacillus plantarum pyrDFE probe. Int. J. Syst. Bacteriol. 46:588-594.
23. Di Cagno R, Coda R, De Angelis M, Gobbetti M. 2013. Exploitation of vegetables and fruits through lactic acid fermentation. Food Microbiol. 33:1-10. http://dx.doi.org/10.1016/j.fm.2012.09.003.
24. Sturme MHJ, Francke C, Siezen RJ, de Vos WM, Kleerebezem M. 2007. Making sense of quorum sensing in lactobacilli: a special focus on Lactobacillus plantarum WCFS1. Microbiology 153:3939-3947. http://dx.doi.org/10.1099/mic.0.2007/012831-0.
25. Diep DB, Havarstein LS, Nes IF. 1996. Characterization of the locus responsible for the bacteriocin production in Lactobacillus plantarum C11. J. Bacteriol. 178:4472-4483.
26. Maldonado A, Ruiz-Barba JL, Jimenez-Diaz R. 2003. Purification and genetic characterization of plantaricin NC8, a novel coculture-inducible two-peptide bacteriocin from Lactobacillus plantarum NC8. Appl. Environ. Microbiol. 69:383-389. http://dx.doi.org/10.1128/AEM.69.1.383-389.2003.
27. Remiger A, Ehrmann MA, Vogel RF. 1996. Identification of bacteriocinencoding genes in lactobacilli by polymerase chain reaction (PCR). Syst. Appl. Microbiol. 19:28-34.
28. Diep DB, Myhre R, Johnsborg O, Aakra A, Nes IF. 2003. Inducible bacteriocin production in Lactobacillus is regulated by differential expression of the pln operons and by two antagonizing response regulators, the activity of which is enhanced upon phosphorylation. Mol. Microbiol. 47: 483-494. http://dx.doi.org/10.1046/j.1365-2958.2003.03310.x.
29. Diep DB, Straume D, Kjos M, Torres C, Nes IF. 2009. An overview of the mosaic bacteriocin pln loci from Lactobacillus plantarum. Peptides 30: 1562-1574. http://dx.doi.org/10.1016/j.peptides.2009.05.014.
30. Fuqua C, Parsek MR, Greenberg EP. 2001. Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu. Rev. Genet. 35:439-468. http://dx.doi.org/10.1146/annurev.genet.35.102401.090913.
31. Siragusa S, De Angelis M, Calasso M, Campanella D, Minervini F, Di Cagno R, Gobbetti M. 11 November 2013. Metabolic and proteomic profiling of Lactobacillus plantarum strains during growth under food-like conditions. Proteomics pii:S1874-S3919(13)00559 -9. [Published ahead of print.] http://dx.doi.org/10.1016/j.prot.2013.11.003.
32. Di Cagno R, Surico RF, Siragusa S, De Angelis M, Paradiso A, Minervini F, De Gara L, Gobbetti M. 2008. Selection and use of autochthonous mixed starter for lactic acid fermentation of carrots, French beans or marrows. Int. J. Food Microbiol. 127:220-228. http://dx.doi.org/10.1016/j.ijfoodmicro.2008.07.010.
33. Di Cagno R, Surico RF, Paradiso A, De Angelis M, Salmon JC, Buchin S, De Gara L, Gobbetti M. 2009. Effect of autochthonous lactic acid bacteria starters on health-promoting and sensory properties of tomato juices. Int. J. Food Microbiol. 128:473-483. http://dx.doi.org/10.1016/j.ijfoodmicro.2008.10.017.
34. Di Cagno R, Cardinali G, Minervini G, Antonielli L, Rizzello CG, Ricciuti P, Gobbetti M. 2010. Taxonomic structure of the yeasts and lactic acid bacteria microbiota of pineapple (Ananas comosus L. Merr.) and use of autochthonous starters for minimally processing. Food Microbiol. 27: 381-389. http://dx.doi.org/10.1016/j.fm.2009.11.012.
35. Di Cagno R, Mazzacane F, Rizzello CG, Vincentini O, Silano M, Giuliani G, De Angelis M, Gobbetti M. 2010. Synthesis of isoflavone aglycones and equol in soy milks fermented by food-related lactic acid bacteria and their effect on human intestinal Caco-2 cells. J. Agric. Food Chem. 58:10338-10346. http://dx.doi.org/10.1021/jf101513r.
36. Vitali B, Minervini G, Rizzello CG, Spisni E, Maccaferri S, Brigidi P, Gobbetti M, Di Cagno R. 2012. Novel probiotic candidates for humans isolated from raw fruits and vegetables. Food Microbiol. 31:116-125. http://dx.doi.org/10.1016/j.fm.2011.12.027.
37. Schillinger U, Lucke FK. 1989. Antibacterial activity of Lactobacillus sakei isolated from meat. Appl. Environ. Microbiol. 55:1901-1906.
38. Atanassova M, Choiset Y, Dalgalarrondo M, Chobert JM, Dousset X, Ivanova I, Haertle T. 2003. Isolation and partial biochemical characterization of a proteinaceous anti-bacteria and anti-yeast compound produced by Lactobacillus paracasei subsp. paracasei strain M3. Int. J. Food Microbiol. 87:63-73. http://dx.doi.org/10.1016/S0168-1605(03)00054-0.
39. Jacxsens L, Devlieghere F, Ragaert P, Vanneste E, Debevere J. 2003. Relation between microbiological quality, metabolite production and sensory quality of equilibrium modified atmosphere packaged fresh-cut produce. Int. J. Food Microbiol. 83:263-280. http://dx.doi.org/10.1016/S0168-1605(02)00376-8.
40. Sathe SJ, Nawani NN, Dhakephalkar PK, Kapadnis BP. 2007. Antifungal lactic acid bacteria with potential to prolong shelf-life of fresh vegetables. J. Appl. Microbiol. 103:2622-2628. http://dx.doi.org/10.1111/j.1365-2672.2007.03525.x.
41. Rojo-Bezares B, Sáenz Y, Navarro L, Jiménez-Díaz RW, Zarazaga M, Ruiz-Larrea F, Torres C. 2008. Characterization of a new organization of the plantaricin locus in the inducible bacteriocin-producing Lactobacillus plantarum J23 of grape must origin. Arch. Microbiol. 189:491-499. http://dx.doi.org/10.1007/s00203-007-0342-6.
42. Church FC, Swaisgood HE, Porter DH, Catignani GL. 1983. Spectrophotometric assay using o-phthaldialdehyde for determination of proteolysis in milk and isolated milk proteins. J. Dairy Sci. 66:1219-1227. http://dx.doi.org/10.3168/jds.S0022-0302(83)81926-2.
43. De Los Reyes-Gavilán CG, Limsowtin GKY, Tailliez P, Séchaud L, Accolas J. 1992. A Lactobacillus helveticus-specific DNA probe detects restriction fragment length polymorphisms in this species. Appl. Environ. Microbiol. 58:3429-3432.
44. Perkin-Elmer Corporation. 1997. Applied Biosystem Prism 7700 sequence detection system user bulletin 2. The Perkin-Elmer Corporation, Norwalk, CT.
45. Walters M, Sircili MP, Speradio V. 2006. AI-3 synthesis is not dependent on luxS in Escherichia coli. J. Bacteriol. 188:5668-5681. http://dx.doi.org/10.1128/JB.00648-06.
46. Gu G, Luo Z, Cevallos-Cevallos JM, Adams P, Vellidis G, Wright A, van Bruggen AH. 2013. Factors affecting the occurrence of Escherichia coli O157 contamination in irrigation ponds on produce farms in the Suwannee River Watershed. Can. J. Microbiol. 59:175-182. http://dx.doi.org/10.1139/cjm.2012-00599.
47. Maatta J, Lehto M, Kuisma R, Kymäläinen HR, Mäki M. 2013. Microbiological quality of fresh-cut carrots and process waters. J. Food Prot. 76:1240-1244. http://dx.doi.org/10.43515/0362-028X.JFP-12-550.
48. Franco W, Pérez-Díaz IM. 2013. Microbial interactions associated with secondary cucumber fermentation. J. Appl. Microbiol. 114:161-172. http://dx.doi.org/10.1111/jam.12022.
49. Hayashi H, Sakamoto M, Kitahara M, Benno Y. 2006. Diversity of the Clostridiumn coccoides group in human fecal microbiota as determined by 16S rRNA gene library. FEMS Microbiol. Lett. 257:202-207. http://dx.doi.org/10.1111/j/1574-6968.2006.00171.x.
50. Deak T, Farkas J. 2013. Spoilage microorganisms, p 66-83. In Microbiology of thermally preserved foods canning: novel and physical methods. DeStech Publications Inc., Lancaster, PA.
51. Vendan RT, Yu YJ, Lee SH, Rhee YH. 2010. Diversity of endophytic bacteria in ginseng and their potential for plant growth promotion. J. Microbiol. 48:559-565. http://dx.doi.org/10.1007/s12275-010-0082-1.
52. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(ΔΔCT) method. Methods 25:402-408. http://dx.doi.org/10.1006/meth.2001.1262.
53. Desroche N, Beltramo C, Guzzo J. 2005. Determination of an internal control to apply reverse transcription quantitative PCR to study stress response in the lactic acid bacterium Oenococcus oeni. J. Microbiol. Methods 60:325-333. http://dx.doi.org/10.1016/j.mimet.2004.10.010.
54. Prins WA, Botha M, Botes M, de Kwaadsteniet M, Endo A, Dicks LMT. 2010. Lactobacillus plantarum 24, isolated from the Marula Fruit (Sclerocarya birrea), has probiotic properties and harbors genes encoding the production of three bacteriocins. Curr. Microbiol. 61:584-589. http://dx.doi.org/10.1007/s00284-010-9656-8.
55. Doulgeraki AI, Paraskevopoulos N, Nychas GJE, Panagou EZ. 2013. An in vitro study of Lactobacillus plantarum strains for the presence of plantaricin genes and their potential control of the table olive microbiota. Antonie van Leeuwenhoek 103:821-832. http://dx.doi.org/10.1007/s10482-012-9864-2.
56. Maldonado A, Jimenez-Díaz R, Ruiz-Barba JL. 2004. Induction of plantaricin production in Lactobacillus plantarum NC8 after coculture with specific Gram-positive bacteria is mediated by an autoinduction mechanism. J. Bacteriol. 186:1556-1564. http://dx.doi.org/10.1128/JB.186.5.1556-1564.2004.
57. Maldonado-Barragán A, Caballero-Guerrero B, Lucena-Padrós H, Ruiz-Barba JL. 2013. Induction of bacteriocin production by coculture is widespread among plantaricin-producing Lactobacillus plantarum strains with different regulatory operons. Food Microbiol. 33:40-47. http://dx.doi.org/10.1016/j.fm.2012.08.009.
58. Rizzello CG, Coda R, Sánchez Macías D, Pinto D, Marzani B, Filannino P, Giuliani G, Paradiso VM, Di Cagno R, Gobbetti M. 2013. Lactic acid fermentation as a tool to enhance the functional features of Echinacea spp. Microb. Cell Fact. 12:44-59. http://dx.doi.org/10.1186/1475-2859-12-44.
59. Maldonado-Barragán A, Ruiz-Barba JL, Jimenez-Díaz R. 2009. Knockout of three-component regulatory systems reveals that the apparently constitutive plantaricin-production phenotype shown by Lactobacillus plantarum on solid medium is regulated via quorum sensing. Int. J. Food Microbiol. 130:35-42. http://dx.doi.org/10.1016/j.ijfoodmicro.2008.12.033.
60. Saucier L, Poon A, Stiles ME. 1995. Induction of bacteriocin in Carnobacterium piscicola LV17. J. Appl. Bacteriol. 78:684-690. http://dx.doi.org/10.1111/j.1365-2672.1995.tb03116.x.
61. Korber DR, Lawrence JR, Lappin-Scott HM, Costerton JW. 1995. Growth of microorganisms on surfaces, p 15-45. In Lappin-Scott HM, CostertonJW(ed), Microbial biofilms, plant and microbial biotechnology research series, vol 5. University Press, Cambridge, United Kingdom.
62. Miller MB, Bassler BL. 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55:165-199. http://dx.doi.org/10.1146/annurev.micro.55.1.165.
63. Chao L, Levin BR. 1981. Structured habitats and the evolution of anticompetitor toxins in bacteria. Proc. Natl. Acad. Sci. U. S. A. 78:6324- 6328.
64. Maldonado A, Ruiz-Barba JL, Jiménez-Díaz R. 2004. Production of plantaricin NC8 by Lactobacillus plantarum NC8 is induced in the presence of different types of Gram-positive bacteria. Arch. Microbiol. 181:8- 16. http://dx.doi.org/10.1007/s00203-003-0606-8.
65. Ben Omar N, Abriouel H, Keleke S, Sanchez Valenzuela A, Martinez- Canamero M, Lucas Lopez R, Ortega E, Galvez A. 2008. Bacteriocinproducing Lactobacillus strains isolated from poto poto, a Congolese fermented maize product, and genetic fingerprinting of their plantaricin operons. Int. J. Food Microbiol. 30:18-25. http://dx.doi.org/10.1016/j.ijfoodmicro.2008.05.037.
66. Hurtado A, Reguant C, Bordons A, Rozés N. 2011. Expression of Lactobacillus pentosus B96 bacteriocin genes under saline stress. Food Microbiol. 28:1339-1344. http://dx.doi.org/10.1016/j.fm.2011.06.004.
67. Jiménez-Díaz R, Rios-Sánchez RM, Desmazeaud M, Ruiz-Barba JL, Piard JC. 1993. Plantaricins S and T, two new bacteriocins produced by Lactobacillus plantarum LPCO10 isolated from a green olive fermentation. Appl. Environ. Microbiol. 59:1416-1424.
68. Holo H, Jeknic Z, Daeschel M, Stevanovic S, Nes IF. 2001. Plantaricin W from Lactobacillus plantarum belongs to a new family of two-peptide lantibiotics. Microbiology 147:643-651.
69. Sáenz Y, Rojo-Bezares B, Navarro L, Díez L, Somalo S, Zarazaga M, Ruiz-Larrea F, Torres C. 2009. Genetic diversity of the pln locus among oenological Lactobacillus plantarum strains. Int. J. Food Microbiol. 134: 176-183. http://dx.doi.org/10.1016/j.ijfoodmicro.2009.06.004.
70. Anderssen EL, Diep DB, Nes IF, Eijsink VGH, Nissen-Meyer J. 1998. Antagonistic activity of Lactobacillus plantarum C11: two new two-peptide bacteriocins, plantaricins EF and JK, and the induction factor plantaricin A. Appl. Environ. Microbiol. 64:2269-2272.
71. Nissen-Meyer J, Oppegård C, Rogne P, Haugen HS, Kristiansen PE. 2010 Structure and mode of action of the two-peptide (class-IIb) bacteriocins. Probiotics Antimicrob. Proteins 2:52-60. http://dx.doi.org/10.1007/s12602-009-9021-z.
72. Minervini F, Algaron F, Rizzello CG, Fox PF, Monnet V, Gobbetti M. 2003 Angiotensin I-converting-enzyme-inhibitory and antibacterial peptides from Lactobacillus helveticus PR4 proteinase-hydrolyzed caseins of milk from six species. Appl. Environ. Microbiol. 69:5297-5305. http://dx.doi.org/10.1128/AEM.69.9.5297-5305.2003.
73. Garneau S, Martin NI, Vederas JC. 2002. Two peptide bacteriocins produced by lactic acid bacteria. J. Biochem. 84:577-592. http://dx.doi.org/10.1016/S0300-9084(02)01414-1.
74. Hauge Hauge HH, Mantzilas D, Moll GN, Konings WN, Driessen AJM, Eijsink VGH, Nissen-Meyer J. 1998. Plantaricin A is an amphiphilic R-helical bacteriocin-like pheromone which exerts antimicrobial and pheromone activities through different mechanisms. Biochemistry 37: 16026-16032. http://dx.doi.org/10.1021/bi981532j.
75. Rojo-Bezares B, Saenz Y, Navarro L, Zarazaga M, Ruiz-Larrea F, Torres C. 2007. Coculture-inducible bacteriocin activity of Lactobacillus plantarum strain J23 isolated from grape must. Food Microbiol. 24:482-491. http://dx.doi.org/10.1016/j.fm.2006.09.003.