Abstrakt

Salmonella spp. is capable of adhering and forming a biofilm on materials of different kinds during their life cycle, contaminating the food chain, thus representing a potential danger for consumers. This review discusses the ability of Salmonella to form biofilm as the main obstacle to reducing the prevalence of these pathogens in food production. The components of Salmonella biofilm, such as cellulose, curli fimbriae, outer membrane proteins (OMPs) and their molecular bases are described, as well as various Salmonella morphotypes (rdar, bdar, pdar and saw). OMPs play very important roles in the cells of Salmonella strains, because they are at the interface between the pathogenic cells and the host tissue and they can contribute to adherence, colonization, virulence and biofilm formation. Furthermore, the importance of quorum sensing is discussed as a crucial factor regulating the properties of biofilm formation and pathogenicity. To further illustrate that biofilm formation is a mechanism used by Salmonella to adapt to various environments, the resistance of Salmonella biofilms against different stress factors including antimicrobials (disinfectants, antibiotics and plant extracts) is described.

Przypisy

• 1. Ahmer B.M.: Cell-to-cell signalling in Escherichia coli and Salmonellaenterica. Mol. Microbiol., 2004; 52: 933–945
  Google Scholar
• 2. Ahmer B.M., van Reeuwijk J., Timmers C.D., Valentine P.J., HeffronF.: Salmonella typhimurium encodes a SdiA homolog, a putativequorum sensor of the LuxR family, that regulates genes on the virulenceplasmid. J. Bacteriol., 1998; 180: 1185–1193
  Google Scholar
• 3. Arnold J.W., Yates I.E.: Interventions for control of Salmonella:Clearance of microbial growth from rubber picker fingers. Poult.Sci., 2009; 88: 1292–1298
  Google Scholar
• 4. Bai A.J., Rai V.R.: Bacterial quorum sensing and food industry.Compr. Rev. Food Sci. Food Saf., 2011; 10: 183–193
  Google Scholar
• 5. Barnhart M.M., Chapman M.R.: Curli biogenesis and function.Annu. Rev. Microbiol., 2006; 60: 131–147
  Google Scholar
• 6. Bazargani M.M., Rohloff J.: Antibiofilm activity of essential oilsand plant extracts against Staphylococcus aureus and Escherichia colibiofilms. Food Control, 2016; 61: 156–164
  Google Scholar
• 7. Boddicker J.D., Ledeboer N.A., Jagnow J., Jones B.D.: Clegg, S.: Differentialbinding to and biofilm formation on, Hep-2 cells by Salmonellaenetrica Serovar Typhimurium is dependent upon allelic variation in thefimH gene of the fim gene cluster. Mol. Microbiol., 2002; 45: 1255–1265
  Google Scholar
• 8. Bouwman C.W., Kohli M., Killoran A., Touchie G.A., Kadner R.J.,Martin N.L.: Characterization of SrgA, a Salmonella enetrica SerovarTyphimurium virulence plasmid-encoded paralogue of the disulphideoxidoreductase DsbA, essential for biogenesis of plasmid-encodedfimbriae. J. Bacteriol., 2003; 185, 991–1000
  Google Scholar
• 9. Bower C.K., Daeschel M.A.: Resistance responses of microorganismsin food environments. Int. J. Food Microbiol., 1999; 50: 33–44
  Google Scholar
• 10. Capita R., Alonso-Calleja C.: Antibiotic-resistant bacteria: A challengefor the food industry. Crit. Rev. Food Sci. Nutr., 2013; 53: 11–48
  Google Scholar
• 11. Collinson S.K., Clouthier S.C., Doran J.L., Banser P.A., Kay W.W.:Salmonella enteritidis agfBAC operon encoding thin, aggregative fimbriae.J. Bacteriol., 1996; 178: 662–667
  Google Scholar
• 12. Cookson A.L., Cooley W.A., Woodward M.J.: The role of type 1and curli fimbriae of Shiga toxin-producing Escherichia coli in adherenceto abiotic surfaces. Int. J. Med. Microbiol., 2002; 292: 195–205
  Google Scholar
• 13. Costerton J.W., Lewandowski Z., Caldwell D.E., Korber D.R., Lappin-Scot H.M.: Microbial biofilms. Annu. Rev. Microbiol., 1995; 49:711–745
  Google Scholar
• 14. European Food Safety Authority, European Centre for DiseasePrevention and Control: The European Union summary report ontrends and sources of zoonoses, zoonotic agents and food-borneoutbreaks in 2016. EFSA J., 2017; 15: 5077
  Google Scholar
• 15. Gerstel U., Park C., Römling U.: Complex regulation of csgDpromoter activity by global regulatory proteins. Mol. Microbiol.,2003; 49: 639–654
  Google Scholar
• 16. Halatasi K., Oikonomou I., Lambiri M., Mandilara G., Vatopoulus,A., Kyriacou A.: PCR detection Salmonella spp. using primerstargeting the quorum sensing gene sdiA. FEMS Microbiol. Lett., 2006;259: 201–207
  Google Scholar
• 17. Hammar M., Bian Z., Normark S.: Nucleator-dependent intercellularassembly of adhesive curli organelles in Escherichia coli. Proc.Natl. Acad. Sci. USA, 1996; 93: 6562–6566
  Google Scholar
• 18. Herwald H., Mörgelin M., Olsén A., Rhen M., Dahlbäck B., Müller-Esterl W., Björck L.: Activation of the contact-phase system onbacterial surfaces – a clue to serious complications in infection diseases.Nat. Med., 1998; 4: 298–302
  Google Scholar
• 19. Hood S.K., Zottola E.A.: Adherence to stainless steel by foodbornemicroorganisms during growth in model food systems. Int. J. FoodMicrobiol., 1997; 37: 145–153
  Google Scholar
• 20. Janssens J.C., Steenackers H., Robbijns S., Gellens E., Levin J.,Zhao H., Hermans K., De Coster D., Verhoeven T.L., Marchal K., VanderleydenJ., De Vos D.E., De Keersmaecker S.C.: Brominated furanonesinhibit biofilm formation of Salmonella enterica serovar Typhimurium.Appl. Enviorn. Microbiol., 2008; 74: 6639–6648
  Google Scholar
• 21. Joseph B., Otta S.K., Karunasagar I., Karunasagar I.: Biofilm formationby Salmonella spp. on food contact surfaces and their sensitivityto sanitizers. Int. J. Food Microbiol., 2001; 64: 367–372
  Google Scholar
• 22. Karampoula F., Giaouris E., Deschamps J., Doulgeraki A.I., NychasG.J., Dubois-Brissonnet F.: Hydrosol of Thymbra capitata is a highlyefficient biocide against Salmonella enetrica serowar Typhimuriumbiofilms. Appl. Environ Microbiol., 2016; 82: 5309–5319
  Google Scholar
• 23. Korber D.R.; Choi A., Wolfaardt G.M., Ingham S.C., Caldwell D.E.:Substratum topography influences susceptibility of Salmonella enteritidisbiofilms to trisodium phosphate. App. Environ. Microbiol.,1997; 63: 3352–3358
  Google Scholar
• 24. Lamas A., Fernandez-No I.C., Miranda J.M., Vázquez B., Cepeda A.,Franco C.M.: Biofilm formation and morphotypes of Salmonella entericasubsp. arizonae differs from those of other Salmonella enterica subspeciesin isolates from poultry houses. J. Food. Prot., 2016; 79: 1127–1134
  Google Scholar
• 25. Lamas A., Miranda J.M., Vázquez B., Cepeda A., Franco C.M.:Biofilm formation, phenotypic production of cellulose and geneexpression in Salmonella enterica decrease under anaerobic conditions.Int. J. Food. Microbiol., 2016; 238: 63–67
  Google Scholar
• 26. Lamas A., Regal P., Vázquez B., Miranda J.M., Cepeda A., FrancoC.M.: Salmonella and Campylobacter biofilm formation: a comparativeassessment from farm to fork. J. Sci. Food Agric., 2018; 98: 4014–4023
  Google Scholar
• 27. Latasa C., Roux A., Toledo-Arana A., Ghigo J.M., Gamazo C., PenadésJ.R., Lasa I.: BapA, a large secreted protein required for biofilmformation and host colonization of Salmonella enterica serovarEnteritidids. Mol. Microbiol., 2005; 58: 1322–1339
  Google Scholar
• 28. Ledeboer N.A., Frye J.G., McClelland M., Jones B.D.: Salmonellaenetrica serovar Typhimurium requires the Lpf, Pef and Tafi fimbriaefor biofilm formation on Hep-2 tissue culture cells and chicken intestinalepithelium. Infect. Immun., 2006; 74: 3156–3169
  Google Scholar
• 29. Ledeboer N.A., Jones B.D.: Exopolysaccharide sugars contributeto biofilm formation by Salmonella enterica serovar Typhimurium onHep-2 cells and chickens intestinal epithelium. J. Bacteriol., 2005;187: 3214–3226
  Google Scholar
• 30. Lianou A., Koutsoumanis K.P.: Strain variability of the biofilm-forming ability of Salmonella enterica under various environmentalconditions. Int. J. Food Microbiol., 2012; 160: 171–178
  Google Scholar
• 31. MacKenzie K.D., Palmer M.B., Köster W.L., White A.P.: Examiningthe link between biofilm formation and the ability of pathogenicSalmonella strains to colonize multiple host species. Front.Vet. Sci., 2017; 4: 138
  Google Scholar
• 32. Majtán J., Majtánová L., Xu M., Majtán V.: In vitro effects subinhibitoryconcentrations of antibiotics on biofilm formation by clinicalstrains of Salmonella enetrica serovar Typhimurium isolates inSlovakia. J. App. Mirobiol., 2008; 104: 1294–1301
  Google Scholar
• 33. Malcova M., Karasova D., Rychlik I.: aroA and aroD mutations influencebiofilm formation in Salmonella Enteritidis. FEMS Microbiol.Lett., 2009; 291: 44–49
  Google Scholar
• 34. Mangalappalli-Illathu A.K., Korber D.R.: Adaptive resistance anddifferential protein expression of Salmonella enterica serovar Enteritidisbiofilms exposed to benzalkonium chloride. Antimicrob. AgentsChemother., 2006; 50: 3588–3596
  Google Scholar
• 35. Markland S., Ingram D., Kniel K.E., Sharma M.: Water for agriculture:The convergence of sustainability and safety. Microbiol.Spectr., 2017; 5: PFS-0014–2016
  Google Scholar
• 36. Michael B., Smith J.N., Swith S., Heffron F., Ahmer B.M.: SdiA ofSalmonella enterica is a LuxR homolog that detects mixed microbialcommunities. J. Bacteriol., 2001; 183: 5733–5742
  Google Scholar
• 37. Nicholson B., Low D.: DNA methylation-dependent regulation of pefexpression in Salmonella typhimurium. Mol. Microbiol., 2000; 35: 728–742
  Google Scholar
• 38. Oh S.Y., Yun W., Lee J.H., Lee C.H., Kwak W.K. Cho J.H.: Effects ofessential oil (blended and single essential oils) on anti-biofilm formationof Salmonella and Escherichia coli. J. Anim. Sci. Technol., 2017; 59: 4
  Google Scholar
• 39. Olsén A., Herwald H., Wikström M., Persson K., Mattson E., BjörckL.: Identification of two protein-binding and functional regions ofcurli, a surface organelle and virulence determinant of Escherichiacoli. J. Biol. Chem., 2002; 277: 34568–34572
  Google Scholar
• 40. Olsén A., Jonsson A., Normark S.: Fibronectin binding mediatedby a novel class of surface organelles on Escherichia coli. Nature,1989; 338: 652–655
  Google Scholar
• 41. Olson M.E., Ceri H., Morck D.W., Buret A.G., Read R.R.: Biofilmbacteria: formation and comparative susceptibility to antibiotics.Can. J. Vet. Res., 2002; 66: 86–92
  Google Scholar
• 42. Papavasileiou K., Papavasileiou E., Tseleni-Kotsovii A., BersimisS., Nicolaou C. Ioannidis A., Chatzipanagiotou S.: Comparative antimicrobialsusceptibility of biofilm versus planktonic forms of Salmonellaenterica strains isolated from children with gastroenteritis.Eur. J. Clin. Microbiol. Infect. Dis., 2010; 29: 1401–1405
  Google Scholar
• 43. Paz-Méndez A.M., Lamas A., Vázquez B., Miranda J.M., CepedaA., Franco C.M.: Effect of food residues in biofilm formation on stainlesssteel and polystyrene surfaces by Salmonella enterica strainsisolated from poultry houses. Foods, 2017; 6: E106
  Google Scholar
• 44. Proctor M.E., Hamacher M., Tortorello M.L., Archer J.R., DavisJ.P.: Multistate outbreak of Salmonella serovar Muenchen infectionsassociated with alfalfa sprouts grown from seeds pretreated withcalcium hypochlorite. J. Clin. Microbiol., 2001; 39: 3461–3465
  Google Scholar
• 45. Prouty A.M., Gunn J.S.: Comparative analysis of Salmonella entericaserovar Typhimurium biofilm formation on gallstones and onglass. Infect. Immun., 2003; 71: 7154–7158
  Google Scholar
• 46. Raghunathan D., Wells T.J., Morris F.C., Shaw R. Bobat K., PetersS.E., Paterson G.K., Jensen K.T., Leyton D.L., Blair J.M., BrowningD.F., Pravin J., Flores-Langarica A., Hitchcock J.R., Moraes C.T., et al.:SadA, a trimeric autotransporter from Salmonella enterica serovarTyphimurium, can promote biofilm formation and provides limitedprotection against infection. Infect. Immun., 2011; 79: 4342–4352
  Google Scholar
• 47. Römling U.: Molecular biology of cellulose production in bacteria.Res. Microbiol., 2002; 153: 205–212
  Google Scholar
• 48. Römling U., Bokranz W., Rabsch W., Zogaj X., Nimtz M., TschäpeH.: Occurence and regulation of the multicellular morphotype inSalmonella serovars important in human disease. Int. J. Med. Microbiol.,2003; 293: 273–285
  Google Scholar
• 49. Römling U., Rhode M., Olsén, A., Normark S., Reinköster J.: AgfD,the checkpoint of multicellular and aggregative behaviour in Salmonellatyphimurium regulates at least two independent pathways. Mol.Microbiol., 2000; 36: 10–23
  Google Scholar
• 50. Sivapalasingam S., Barrett E., Kimura A., Van Duyne S., De WittW., Ying M., Frisch A., Phan Q., Gould E., Shillam P., Reddy V., CooperT., Hoekstra M., Higgins C., Sanders J.P., et al.: A multistate outbreakof Salmonella enterica Serotype Newport infection linked to mangoconsumption: Impact of water-dip disinfestation technology. Clin.Infect. Dis., 2003; 37: 1585–1590
  Google Scholar
• 51. Sjöbring U., Pohl G., Olsén A.: Plasminogen, absorbed byEscherichia coli expressing curli or by Salmonella enteritidisexpressing thin aggregative fimbriae, can be activated by simultaneouslycaptured tissue-type plasminogen activator (t-PA). Mol.Microbiol., 1994; 14: 443–452
  Google Scholar
• 52. Smith J.N., Ahmer B.M.: Detection of other microbial speciesby Salmonella: Expression of the SdiA regulon. J. Bacteriol.,2003; 185: 1357–1366
  Google Scholar
• 53. Solano C., Garcia B., Valle J., Berasain C., Ghigo J.M., GamazoC., Lasa I.: Genetic analysis of Salmonella enteritidis biofilm formation:critical role of cellulose. Mol. Microbiol., 2002; 43: 793–808
  Google Scholar
• 54. Solomon E.B., Niemira B.A., Sapers G.M., Annous B.A.: Biofilmformation, cellulose production, and curli biosynthesis bySalmonella originating from produce, animal, and clinical sources.J. Food Prot., 2005; 68: 906–912
  Google Scholar
• 55. Sperandio V., Torres A.G, Kaper J.B.: Quorum sensing Escherichiacoli regulators B and C (QseBC): A novel two-component regulatorysystem involved in the regulation of flagella and motilityby quorum sensing in E. coli. Mol. Microbiol., 2002; 43: 809–821
  Google Scholar
• 56. Steenackers H., Hermans K., Vanderleyden J., De KeersmaeckerS.C.J.: Salmonella biofilms: An overview on occurrence, structure,regulation and eradication. Food Res. Inter., 2012; 45: 502–531
  Google Scholar
• 57. Stein R.A.: Super-spreaders in infectious diseases. Int. J. Infect.Dis., 2011; 15: e510–e513
  Google Scholar
• 58. Stepanović S., Cirković L., Ranin L., Svabić-Vlahović M.: Biofilmformation of Salmonella spp. and Listeria monocytogenes onplastic surface. Lett. App. Microbiol., 2004; 38: 428–432
  Google Scholar
• 59. Tabak M., Scher K., Chikindas M.L., Yaron S.: The synergisticactivity of triclosan and ciprofloxacin on biofilms of SalmonellaTyphimurium. FEMS Microbiol. Lett., 2009; 301: 69–76
  Google Scholar
• 60. Tabak M., Scher K., Hartog E., Romling U., Matthews K.R.,Chikindas M.L., Yaron S.: Effects of triclosan on Salmonella typhimuriumat different growth stages and in biofilms. FEMS Microbiol.Lett., 2007; 267: 200–206
  Google Scholar
• 61. Tosun S.Y., Alakavuk D.U., Ulusoy S., Erkan N.: Effects of essentialoils on the survival of Salmonella Enteritidis and Listeriamonocytogenes on fresh Atlantic salmons (Salmo salar) duringstorage at 2±1 oC. J. Food Saf., 2017; 38: e12408
  Google Scholar
• 62. Trevisan D.A., da Silva A.F., Negri M., de Abreu Filho B.A., MachinskiJunior M., Patussi E.V., Campanerut-Sá P.A., Mikcha J.M.: Antibacterialand antibiofilm activity of carvacrol against Salmonellaenterica serotype Typhimurium. Braz. J. Pharm. Sci., 2018; 54: e17229
  Google Scholar
• 63. Vestrheim D.F., Lange H., Nygård K., Borgen K., Wester A.L., KvarmeM.L., Vold L.: Are ready-to-eat salads ready to eat? An outbreak ofSalmonella Coeln linked to imported, mixed, pre-washed and baggedsalad, Norway, November 2013. Epidemiol. Infect., 2016; 144: 1756–1760
  Google Scholar
• 64. Wadamori Y., Gooneratne R., Hussain M.A.: Outbreaks and factorsinfluencing microbiological contamination of fresh produce. J.Sci. Food Agric., 2017; 97: 1396–1403
  Google Scholar
• 65. White A.P. Surette M.G.: Comparative genetics of the rdar morphotypein Salmonella. J. Bacteriol., 2006; 188: 8395–8406
  Google Scholar
• 66. Williams P.: Quorum sensing. Int. J. Med. Microbiol., 2006; 296: 57–59
  Google Scholar
• 67. Wong A.C.: Biofilms in food processing environments. J. DairySci., 1998; 81: 2765–2770
  Google Scholar
• 68. Woolhouse M.E., Dye C., Etard J.F., Smith T., Charlwood J.D., GarnettG.P., Hagan P., Hii J.L., Ndhlovu P.D., Quinnell R.J., Watts C.H.,Chandiwana S.K., Anderson R.M.: Heterogeneities in the transmissionof infectious agents: implications for the design of control programs.Proc. Natl. Acad. Sci. USA, 1997; 94: 338–342
  Google Scholar
• 69. Xavier J.B., Foster K.R.: Cooperation and conflict in microbialbiofilms. Proc. Nat. Acad. Sci. USA, 2007; 104: 876–881
  Google Scholar
• 70. Yaron S., Römling U.: Biofilm formation by enteric pathogensand its role in plant colonization and persistence. Microb Biotechnol.,2014; 7: 496–516
  Google Scholar
• 71. Zhou G.H., Xu X.L., Liu Y.: Preservation technologies for freshmeat – a review. Meat Sci., 2010; 86: 119–128
  Google Scholar
• 72. Zogaj X., Nimtz M., Rohde M., Bokranz W., Römling U.: The multicellularmorphotypes of Salmonella typhimurium and Escherichiacoli produce cellulose as the second component of the extracellularmatrix. Mol. Microbiol., 2001; 39: 1452–1463
  Google Scholar

Pełna treść artykułu