Characterisation of biofilms formed by Lactobacillus plantarum WCFS1 and food spoilage isolates

International Journal of Food Microbiology

Volumn 207, Issue , 2015, Pages 23-29

  Fernández Ramírez, Mónica D ^a,b   Smid, Eddy J ^a,b   Abee, Tjakko ^a,b   Nierop Groot, Masja N ^a,b  

^a TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Biofilm; Dispersion; Food spoilage; Lactobacillus plantarum

Indexed keywords

CELL DNA; CRYSTAL VIOLET; DEOXYRIBONUCLEASE I; GLUCOSE; MANGANESE; PROTEINASE K; PEPTIDE HYDROLASE;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIABILITY; BACTERIUM ISOLATE; BACTERIUM ISOLATION; BIOFILM; CELL COUNT; CELL DEATH; CONTROLLED STUDY; DISPERSION; ENVIRONMENTAL FACTOR; ENZYME THERAPY; EXTRACELLULAR DNA; EXTRACELLULAR MATRIX; FOOD INDUSTRY; FOOD SPOILAGE; INCUBATION TEMPERATURE; LACTOBACILLUS PLANTARUM; NONHUMAN; BACTERIAL PHENOMENA AND FUNCTIONS; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; PROCEDURES; TEMPERATURE;

LACTOBACILLUS PLANTARUM;

BACTERIAL PHYSIOLOGICAL PHENOMENA; BIOFILMS; FOOD-PROCESSING INDUSTRY; GENTIAN VIOLET; LACTOBACILLUS PLANTARUM; PEPTIDE HYDROLASES; TEMPERATURE;

EID: 84928884144     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2015.04.030     Document Type: Article

References (56)

1. Abee T., Kovacs A.T., Kuipers O.P., van der Veen S. Biofilm formation and dispersal in Gram-positive bacteria. Curr. Opin. Biotechnol. 2011, 22:172-179.
2. Adlerberth I., Ahrne S., Johansson M.L., Molin G., Hanson L.A., Wold A.E. A mannose-specific adherence mechanism in Lactobacillus plantarum conferring binding to the human colonic cell line HT-29. Appl. Environ. Microbiol. 1996, 62:2244-2251.
3. Bartowsky E.J., Henschke P.A. Acetic acid bacteria spoilage of bottled red wine - a review. Int. J. Food Microbiol. 2008, 125:60-70.
4. Bjorkroth K.J., Korkeala H.J. Lactobacillus fructivorans spoilage of tomato ketchup. J. Food Prot. 1996, 60:505-509.
5. Bjorkroth K.J., Korkeala H.J. Use of rRNA gene restriction patterns to evaluate lactic acid bacterium contamination of vacuum-packaged sliced cooked whole-meat product in a meat processing plant. Appl. Environ. Microbiol. 1997, 63:448-453.
6. Boesten R.J., de Vos W.M. Interactomics in the human intestine: lactobacilli and bifidobacteria make a difference. J. Clin. Gastroenterol. 2008, 42(Suppl. 3 Pt 2):S163-S167.
7. Branda S.S., Chu F., Kearns D.B., Losick R., Kolter R. A major protein component of the Bacillus subtilis biofilm matrix. Mol. Microbiol. 2006, 59:1229-1238.
8. Bridier A., Briandet R., Thomas V., Dubois-Brissonnet F. Resistance of bacterial biofilms to disinfectants: a review. Biofouling 2011, 27:1017-1032.
9. Buckenhüskes H.J. Selection criteria for lactic acid bacteria to be used as starter cultures for various food commodities. FEMS Microbiol. Rev. 1993, 12:253-271.
10. Caplice E., Fitzgerald G.F. Food fermentations: role of microorganisms in food production and preservation. Int. J. Food Microbiol. 1999, 50:131-149.
11. Carpentier B., Cerf O. Biofilms and their consequences, with particular reference to hygiene in the food industry. J. Appl. Bacteriol. 1993, 75:499-511.
12. Chenoll E., Carmen Macian M., Aznar R. Lactobacillus tucceti sp. nov., a new lactic acid bacterium isolated from sausage. Syst. Appl. Microbiol. 2006, 29:389-395.
13. Chmielewski R.A.N., Frank J.F. Biofilm formation and control in food processing facilities. Compr. Rev. Food Sci. Food Saf. 2003, 2:22-32.
14. Cucarella C., Solano C., Valle J., Amorena B., Lasa Í., Penadés J.R. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J. Bacteriol. 2001, 183:2888-2896.
15. Davey M.E., O'Toole G.A. Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 2000, 64:847-867.
16. Espinosa-Urgel M., Salido A., Ramos J.L. Genetic analysis of functions involved in adhesion of Pseudomonas putida to seeds. J. Bacteriol. 2000, 182:2363-2369.
17. FAO Global Food Losses and Food Waste - Extent, Causes and Prevention, Rome 2011.
18. Hall-Stoodley L., Nistico L., Sambanthamoorthy K., Dice B., Nguyen D., Mershon W.J., Johnson C., Hu F.Z., Stoodley P., Ehrlich G.D., Post J.C. Characterization of biofilm matrix, degradation by DNase treatment and evidence of capsule downregulation in Streptococcus pneumoniae clinical isolates. BMC Microbiol. 2008, 8:173.
19. Harmsen M., Lappann M., Knochel S., Molin S. Role of extracellular DNA during biofilm formation by Listeria monocytogenes. Appl. Environ. Microbiol. 2010, 76:2271-2279.
20. Jahn A., Griebe T., Nielsen P.H. Composition of Pseudomonas putida biofilms: accumulation of protein in the biofilm matrix. Biofouling 1999, 14:49-57.
21. Kadam S.R., den Besten H.M., van der Veen S., Zwietering M.H., Moezelaar R., Abee T. Diversity assessment of Listeria monocytogenes biofilm formation: impact of growth condition, serotype and strain origin. Int. J. Food Microbiol. 2013, 165:259-264.
22. Kleerebezem M., Boekhorst J., van Kranenburg R., Molenaar D., Kuipers O.P., Leer R., Tarchini R., Peters S.A., Sandbrink H.M., Fiers M.W., Stiekema W., Lankhorst R.M., Bron P.A., Hoffer S.M., Groot M.N., Kerkhoven R., de Vries M., Ursing B., de Vos W.M., Siezen R.J. Complete genome sequence of Lactobacillus plantarum WCFS1. Proc. Natl. Acad. Sci. 2003, 100:1990-1995.
23. Kubota H., Senda S., Nomura N., Tokuda H., Uchiyama H. Biofilm formation by lactic acid bacteria and resistance to environmental stress. J. Biosci. Bioeng. 2008, 106:381-386.
24. Kubota H., Senda S., Tokuda H., Uchiyama H., Nomura N. Stress resistance of biofilm and planktonic Lactobacillus plantarum subsp. plantarum JCM 1149. Food Microbiol. 2009, 26:592-597.
25. Kurtzman C.P., Rogers R., Hesseltine C.W. Microbiological spoilage of mayonnaise and salad dressings. Appl. Environ. Microbiol. 1971, 21:870-874.
26. Latasa C., Roux A., Toledo-Arana A., Ghigo J.-M., Gamazo C., Penades J.R., Lasa I. BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. Mol. Microbiol. 2005, 58:1322-1339.
27. Lebeer S., De Keersmaecker S.C., Verhoeven T.L., Fadda A.A., Marchal K., Vanderleyden J. Functional analysis of luxS in the probiotic strain Lactobacillus rhamnosus GG reveals a central metabolic role important for growth and biofilm formation. J. Bacteriol. 2007, 189:860-871.
28. Lebeer S., Verhoeven T.L., Perea Velez M., Vanderleyden J., De Keersmaecker S.C. Impact of environmental and genetic factors on biofilm formation by the probiotic strain Lactobacillus rhamnosus GG. Appl. Environ. Microbiol. 2007, 73:6768-6775.
29. Lee I.C., Tomita S., Kleerebezem M., Bron P.A. The quest for probiotic effector molecules - unraveling strain specificity at the molecular level. Pharmacol. Res. 2013, 69:61-74.
30. Lemon K.P., Earl A.M., Vlamakis H.C., Aguilar C., Kolter R. Biofilm development with an emphasis on Bacillus subtilis. Curr. Top. Microbiol. Immunol. 2008, 1-16. (2008/05/06 ed).
31. Lequette Y., Boels G., Clarisse M., Faille C. Using enzymes to remove biofilms of bacterial isolates sampled in the food-industry. Biofouling 2010, 26:421-431.
32. Leroy F., De Vuyst L. Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci. Technol. 2004, 15:67-78.
33. Lorca G., Torino M.I., Font de Valdez G., Ljungh Å. Lactobacilli express cell surface proteins which mediate binding of immobilized collagen and fibronectin. FEMS Microbiol. Lett. 2002, 206:31-37.
34. Lyhs U., Korkeala H., Vandamme P., Björkroth J. Lactobacillus alimentarius: a specific spoilage organism in marinated herring. Int. J. Food Microbiol. 2001, 64:355-360.
35. Mann E.E., Rice K.C., Boles B.R., Endres J.L., Ranjit D., Chandramohan L., Tsang L.H., Smeltzer M.S., Horswill A.R., Bayles K.W. Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS One 2009, 4:e5822.
36. Merritt J.H., Kadouri D.E., O'Toole G.A. Growing and analyzing static biofilms. Current Protocols in Microbiology 2005, John Wiley & Sons, Inc.
37. Muscariello L., Marino C., Capri U., Vastano V., Marasco R., Sacco M. CcpA and three newly identified proteins are involved in biofilm development in Lactobacillus plantarum. J. Basic Microbiol. 2013, 53:62-71.
38. Neville B.A., Forde B.M., Claesson M.J., Darby T., Coghlan A., Nally K., Ross R.P., O'Toole P.W. Characterization of pro-inflammatory flagellin proteins produced by Lactobacillus ruminis and related motile lactobacilli. PLoS One 2012, 7(7):e40592.
39. O'Toole G.A., Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 1998, 30:295-304.
40. O'Toole G., Kaplan H.B., Kolter R. Biofilm formation as microbial development. Annu. Rev. Microbiol. 2000, 54:49-79.
41. Pratt L.A., Kolter R. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol. Microbiol. 1998, 30:285-293.
42. Samelis J., Kakouri A., Rementzis J. Selective effect of the product type and the packaging conditions on the species of lactic acid bacteria dominating the spoilage microbial association of cooked meats at 4°C. Food Microbiol. 2000, 17:329-340.
43. Sanders J.W., Oomes S.J.C.M., Membré J.M., Wegkamp A., Wels M. Biodiversity of spoilage lactobacilli: phenotypic characterisation. Food Microbiol. 2014, 45:34-44. Part A.
44. Simões M., Simões L.C., Vieira M.J. A review of current and emergent biofilm control strategies. LWT Food Sci. Technol. 2010, 43:573-583.
45. Somers E.B., Johnson M.E., Wong A.C. Biofilm formation and contamination of cheese by nonstarter lactic acid bacteria in the dairy environment. J. Dairy Sci. 2001, 84:1926-1936.
46. Stoodley P., Sauer K., Davies D.G., Costerton J.W. Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 2002, 56:187-209.
47. Tallon R., Arias S., Bressollier P., Urdaci M.C. Strain- and matrix-dependent adhesion of Lactobacillus plantarum is mediated by proteinaceous bacterial compounds. J. Appl. Microbiol. 2007, 102:442-451.
48. Tendolkar P.M., Baghdayan A.S., Gilmore M.S., Shankar N. Enterococcal surface protein, Esp, enhances biofilm formation by Enterococcus faecalis. Infect. Immun. 2004, 72:6032-6039.
49. Toledo-Arana A., Valle J., Solano C., Arrizubieta M.J., Cucarella C., Lamata M., Amorena B., Leiva J., Penades J.R., Lasa I. The enterococcal surface protein, Esp, is involved in Enterococcus faecalis biofilm formation. Appl. Environ. Microbiol. 2001, 67:4538-4545.
50. Tuomola E.M., Ouwehand A.C., Salminen S.J. Chemical, physical and enzymatic pre-treatments of probiotic lactobacilli alter their adhesion to human intestinal mucus glycoproteins. Int. J. Food Microbiol. 2000, 60:75-81.
51. Turroni F., Ventura M., Butto L.F., Duranti S., O'Toole P.W., Motherway M.O., van Sinderen D. Molecular dialogue between the human gut microbiota and the host: a Lactobacillus and Bifidobacterium perspective. Cell. Mol. Life Sci. 2014, 71:183-203.
52. van der Veen S., Abee T. Mixed species biofilms of Listeria monocytogenes and Lactobacillus plantarum show enhanced resistance to benzalkonium chloride and peracetic acid. Int. J. Food Microbiol. 2011, 144:421-431.
53. van Houdt R., Michiels C.W. Biofilm formation and the food industry, a focus on the bacterial outer surface. J. Appl. Microbiol. 2010, 109:1117-1131.
54. Vatanyoopaisarn S., Nazli A., Dodd C.E., Rees C.E., Waites W.M. Effect of flagella on initial attachment of Listeria monocytogenes to stainless steel. Appl. Environ. Microbiol. 2000, 66:860-863.
55. Watnick P., Kolter R. Biofilm, city of microbes. J. Bacteriol. 2000, 182:2675-2679.
56. Wegkamp A., Teusink B., de Vos W.M., Smid E.J. Development of a minimal growth medium for Lactobacillus plantarum. Lett. Appl. Microbiol. 2010, 50:57-64.