Skip to main content
SpringerLink
Log in

Biofilm-producing abilities of Salmonella strains isolated from Turkey

  • Section Cellular and Molecular Biology
  • Published:
Biologia Aims and scope Submit manuscript

Abstract

In the present study the biofilm-forming characteristics of 99 serotyped (DMC strains) and 41 genus level-identified (IS strains) Salmonella strains originating from Turkey were investigated. The strains were selected based on their ability to show the biofilm morphotype on Congo red agar plates. In addition, all strains were evaluated with regard to properties related to forming pellicle structures, physical differences of pellicles, any changes in the media associated with the formation of pellicles, and the presence of cellulose within the formed biofilm matrix as determined using 366 nm UV light. The Salmonella Typhimurium DMC4 strain was the best producer of biofilm grown on polystyrene microtiter plates (optical density at 595 nm: 3.418). In subsequent experiments industrial process conditions were used to investigate different morphotyped Salmonella strains’ biofilm-forming capability on stainless steel, a commonly preferred surface for the food industries, and on polystyrene surfaces. The effect of other important industrial conditions, such as temperature (5, 20, 37°C), pH (4.5, 5.5, 6.5, 7.4) and NaCl concentration (0.5, 1.5, 5.5, 10.5%) on the production of biofilm of the different morphotyped Salmonella strains (DMC4; red, dry and rough morphotyped S. Typhimurium, DMC12; brown, dry and rough morphotyped S. Infantis, DMC13; pink, dry and rough morphotyped S. subsp. Roughform) were also assessed. On the other hand, pH values exhibited variable effects on biofilm-forming features for different Salmonella strains on both polystyrene and stainless steel surfaces.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

te]bdar, brown:

dry and rough

cfu:

colony forming unit

CR:

Congo red

LB:

Luria Bertani

OD:

optical density

pdar, pink:

dry and rough

rdar, red:

dry and rough

saw:

smooth and white

sbam, smooth:

brown and mucoid

References

  • Agbaje M., Begum R.H., Oyekunle M.A., Ojo O. E. & Adenubi O.T. 2011. Evolution of Salmonella nomenclature a critical note. Folia Microbiol. 56: 497–503.

    Article  CAS  Google Scholar 

  • Anriany Y.A., Weiner R.M., Johnson J.A., De Rezende C.E. & Joseph S.W. 2001. Salmonella enterica serovar Typhimurium DT104 displays a rugose phenotype. Appl. Environ. Microbiol. 67: 4048–4056.

    Article  PubMed  CAS  Google Scholar 

  • Avsaroglu M.D., Helmuth R., Junker E., Hertwig S., Schroter A., Akcelik M., Bozooglu F. & Guerra B. 2007. Plasmid-mediated quinolone resistance conferred by qnrS1 in Salmonella enterica serovar Virchow isolated from Turkish food avian origin. J. Antimicrob. Chemother. 60: 1146–1150.

    Article  PubMed  CAS  Google Scholar 

  • Barnhart M.M. & Chapman M.R. 2006. Curli biogenesis and function. Annu. Rev. Microbiol. 60: 131–147.

    Article  PubMed  CAS  Google Scholar 

  • Bereksi N., Gavini F., Benezech T. & Faille C. 2007. Growth, morphology and surface properties of Listeria monocytogenes Scott A and LO28 under saline and acid environments. J. Appl. Microbiol. 92: 556–565.

    Article  Google Scholar 

  • Borucki M.K., Peppin J., White D., Loge D. & Call F.D.R. 2003. Variation in biofilm formation among strains of Listeria monocytogenes. Appl. Environ. Microbiol. 69: 7336–7342.

    Article  PubMed  CAS  Google Scholar 

  • Brown M.L., Aldrich H.C. & Gauthier J.J. 1995. Relationship between glycocalyx and povidone-iodine resistance in Pseudomonas aeruginosa (ATCC 27853) biofilms. Appl. Environ. Microbiol. 61: 187–193.

    PubMed  CAS  Google Scholar 

  • Cegelski L., Pinkner J.S., Hammer N.D., Cusumano C.K., Hung C.S., Chorel E., Aberg V., Walker J.N., Seed P.C., Almqvist F., Chapman M.R. & Hultgren S.J. 2009. Small-molecule inhibitors target Escherichia coli amyloid biogenesis and biofilm formation. Nat. Chem. Biol. 5: 913–919.

    Article  PubMed  CAS  Google Scholar 

  • Chavant P., Martinie B., Meylheuc T., Marie-Noëlle B.F. & Hebraud M. 2001. Listeria monocytogenes LO28: surface physicochemical properties and ability to form biofilms at different temperatures and growth phases. Appl. Environ. Microbiol. 68: 728–737.

    Article  Google Scholar 

  • Costerton J.W. 1995. Overwiev of microbial biofilms. J. Ind. Microbiol. 15: 137–140.

    Article  PubMed  CAS  Google Scholar 

  • Costerton J.W., Stewart P.S. & Greenberg E.P. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284: 1318–1322.

    Article  PubMed  CAS  Google Scholar 

  • Crump J.A., Griffin P.M. & Angulo F.J. 2002. Bacterial contamination of animal feed and its relationship to human foodborne illness. J. Food Safety 35: 859–865.

    Google Scholar 

  • Dhaliwal D.S., Cordier J.L. & Cox L.J. 1992. Impedimetric evaluation of the efficiency of disinfectants against biofilms. Lett. Appl. Microbiol. 15: 217–221.

    Article  CAS  Google Scholar 

  • Dhir V.K. & Dodd C.E.R. 1995. Susceptibility of suspended and surface-sttached Salmonella enteritidis to biocides and elevated temperatures. Appl. Environ. Microbiol. 61: 1731–1738.

    PubMed  CAS  Google Scholar 

  • Di Bonaventura G., Piccolomini R., Paludi D., D’Orio V., Vergara A., Conter M. & Ianieri A. 2007. Influence of temperature on biofilm formation by Listeria monocytogenes on various foodcontact surfaces: relationship with motility and cell surface hydrophobicity. J. Appl. Microbiol. 104: 1552–1564.

    Article  Google Scholar 

  • Doyle M.E. & Glass K.A. 2010. Sodium reduction and ıts effect on food safety, food quality, and human health. Comp. Rev. Food Sci. Food Safety 9: 44–56.

    Article  CAS  Google Scholar 

  • Flint S.H., Bremer P.J & Brooks J.D. 1996. Biofilms in dairy manufacturing plant description, current concerns and methods of control. Biofouling 11: 81–97.

    Article  Google Scholar 

  • Giaouris E., Chorianoupoulos N. & Nychas G.J.E. 2005. Effect of temperature, pH, and water activity on biofilm formation by Salmonella enterica Enteritidis PT4 on stainless steel surfaces as ındicated by the bead vortexing method and conductance measurements. J. Food Prot. 68: 2149–2154.

    PubMed  CAS  Google Scholar 

  • Gilbert P., Allison D.G. & McBain A.J. 2002. Biofilms in vitro and in vivo: do singular mechanisms imply cross-resistance? J. Appl. Microbiol. 92: 98–110.

    Article  Google Scholar 

  • Gophna U., Barlev M., Seijffers R., Oelschlager T.A., Hacker J. & Ron E.Z. 2001. Curli fibers mediate internalization of Escherichia coli by eukaryotic cells. Infect. Immun. 69: 2659–2665.

    Article  PubMed  CAS  Google Scholar 

  • Gorski L., Palumbo J.D. & Mandrell R.E. 2002. Attachment of Listeria monocytogenes to radish tissue is dependent upon temperature and flagellar motility. Appl. Environ. Microbiol. 69: 258–266.

    Article  Google Scholar 

  • Herwald H., Mörgelin M., Olsen A., Rhen M., Dahlbäck B., Müller-Ester W. & Björck L. 1998. Activation of the contactphase system on bacterial surfaces — a clue to serious complications in infectious diseases. Nat. Med. 4: 298–302.

    Article  PubMed  CAS  Google Scholar 

  • Holah J.T., Higgs C., Robinson S., Worthington D. & Spenceley H. 1990. A conductance-based surface disinfection test for food hygiene. Lett. Appl. Microbiol. 11: 255–259.

    Article  Google Scholar 

  • Hood S.K. & Zottola E.A. 1997. Adherence to stainless steel by foodborne microorganisms during growth in model food systems. Int. J. Food Microbiol. 37: 145–153.

    Article  PubMed  CAS  Google Scholar 

  • Humphrey T.J., Slater E., McAlpine K., Rowbury R.J. & Gilbert R.J. 1995. Salmonella enteritidis phage type 4 isolates more tolerant of heat, acid, or hydrogen peroxide also survive longer on surfaces. Appl. Environ. Microbiol. 61: 3161–3164.

    PubMed  CAS  Google Scholar 

  • Jones K., Bradshaw S.B. 1996. Biofilm formation by the Enterobacteriaceae: a comparison between Salmonella enteritidis, Escherichia coli and a nitrogen-fixing strain of Klebsiella pneumoniae. J. Appl. Microbiol. 80: 458–464.

    Article  CAS  Google Scholar 

  • Knight G.C. & Craven H.M. 2010. A model system for evaluating surface disinfection in dairy factory environments. Int. J. Food Microbiol. 137: 161–167.

    Article  PubMed  CAS  Google Scholar 

  • Kumar C.G. & Anand S.K. 1998. Significance of microbial biofilms in food industry: a review. Int. J. Food Microbiol. 42: 9–27.

    Article  PubMed  CAS  Google Scholar 

  • Lunden J.M., Miettinen M.K., Autio T.J. & Korkeala H.J. 2000. Persistent Listeria monocytogenes strains show enhanced adherence to food contact surface after short contact times. J. Food Prot. 63: 1204–1207.

    PubMed  CAS  Google Scholar 

  • Lundmark K., Westermark G.T., Olsen A. & Westermark P. 2004. Protein fibrils in nature can enhance amyloid protein A amyloidosis in mice: Cross-seeding as a disease mechanism. Proc. Natl. Acad. Sci. USA 102: 6098–6102.

    Article  Google Scholar 

  • Moretro T., Midtgaard E.S., Nesse L.L. & Langsrud S. 2003. Susceptibility of Salmonella isolated from fish feed factories to disinfectants and air-drying at surfaces. Vet. Microbiol. 94: 207–217.

    Article  PubMed  CAS  Google Scholar 

  • Morin P., Camper A., Jones W., Gatel D. & Goldman J.C. 1996. Colonization and disinfection of biofilms hosting coliformcolonized carbon fines. Appl. Environ. Microbiol. 62: 4428–4432.

    PubMed  CAS  Google Scholar 

  • Olsen A., Jonsson A. & Normark S. 1989. Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 338: 652–655.

    Article  PubMed  CAS  Google Scholar 

  • Rainey P.B. & Travisano M. 1998. Adaptive radiation in an heterogeneous environment. Nature 394: 69–72.

    Article  PubMed  CAS  Google Scholar 

  • Römling U. & Rohde M. 1999. Flagella modulate the multicellular behavior of Salmonella typhimurium on the community level. FEMS Microbiol. Lett. 180: 91–102.

    Article  PubMed  Google Scholar 

  • Römling U., Sierralta W.D., Eriksson K., Normark S 1998. Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol. Microbiol. 28: 249–264.

    Article  PubMed  Google Scholar 

  • Ryu J.H. & Beuchat L.R. 2005. Biofilm formation by Escherichia coli O157:H7 on stainless steel: effect of exopolysaccharide and curli production on its resistance to chlorine. Appl. Environ. Microbiol. 71: 247–254.

    Article  PubMed  CAS  Google Scholar 

  • Sauer K., Rickard A.H. & Davies D.G. 2007. Biofilm and biocomplexity. Features 2: 347–353.

    Google Scholar 

  • Scher K., Römling U. & Yaron S. 2004. Effect of heat, acidifi-cation, and chlorination on Salmonella enterica serovar Typhimurium cells in a biofilm formed at the air-liquid interface. Appl. Environ. Microbiol. 71: 1163–1168.

    Article  Google Scholar 

  • Shi X. & Zhu X. 2009. Biofilm formation and food safety in food industries. Trends Food Sci. Technol. 20: 407–413.

    Article  CAS  Google Scholar 

  • Solano C., Garcia B., Valle J., Berasain C., Ghigo J.M., Gamazo C. & Lasa I. 2002. Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Mol. Microbiol. 43: 793–808.

    Article  PubMed  CAS  Google Scholar 

  • Somers E.B., Schoeni J.L. & Wong A.C.L. 2002. Effect of trisodium phosphate on biofilm and planktonic cells of Campylobacter jejuni, Escherichia coli O157: H7, Listeria monocytogenes and Salmonella typhimurium. Int. J. Food Microbiol. 22: 269–276.

    Article  Google Scholar 

  • Spiers A.J., Bohannon J., Gehrig S.M. & Rainey P.B. 2003. Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose. Mol. Microbiol. 50: 15–27.

    Article  PubMed  CAS  Google Scholar 

  • Spiers A.J., Kahn S.G., Bohannon J., Travisano M. & Rainey P.B. 2002. Adaptive divergence in experimental populations of Pseudomonas fluorescens. I. genetic and phenotypic bases of wrinkly spreader fitness. Genetics 161: 33–46.

    PubMed  CAS  Google Scholar 

  • Stepanovic S., Vukovic D., Dakic I., Savic B. & Svabic-Vlahovic M. 2000. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J. Microbiol. Methods 40: 175–179.

    Article  PubMed  CAS  Google Scholar 

  • Tresse O., Shannon K., Pinon A., Malle P., Vialette M. & Midelet-Bourdin G. 2007. Varaible adhesion of Listeria monocytogenes isolates from food-processing facilities and clinical cases to inert surfaces. J. Food Prot. 70: 1569–1578.

    PubMed  Google Scholar 

  • Vestby L.K., Moretro T., Langsrud S., Heir E. & Nesse L.L. 2009. Biofilm forming abilities of Salmonella are correlated with persistence in fish meal- and feed factories. BMC Vet. Res. 5: 20–26.

    Article  PubMed  Google Scholar 

  • Woodward M.J., Sojka M., Sprigings K.A. & Humphrey T.J. 2000. The role of sef 14 and sef17 fimbriae in the adherence of Salmonella enterica serotype Enteritidis to inanimate surfaces. J. Med. Microbiol. 49: 481–487.

    PubMed  CAS  Google Scholar 

  • Xu H., Zou Y., Lee H. & Ahn J. 2010. Effect of NaCl on the biofilm formation by foodborne pathogens. J. Food Sci. 75: 80–85.

    Article  Google Scholar 

  • Yildiz F.H. & Schoolnik G.K. 1998. Vibrio cholerae O1 El Tor: Identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc. Natl. Acad. Sci. USA 96: 4028–4033.

    Article  Google Scholar 

  • Zogaj X., Nimtz M., Rohde M., Bokranz W. & Römling U. 2001. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol. Microbiol. 39: 1452–1463.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Science, Ankara University, 06100, Tandogan, Ankara, Turkey

    Basar Karaca & Mustafa Akcelik

  2. Biotechnology Institute, Ankara University, 06100, Tandogan, Ankara, Turkey

    Nefise Akcelik

Authors
  1. Basar Karaca
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nefise Akcelik
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mustafa Akcelik
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mustafa Akcelik.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Karaca, B., Akcelik, N. & Akcelik, M. Biofilm-producing abilities of Salmonella strains isolated from Turkey. Biologia 68, 1–10 (2013). https://doi.org/10.2478/s11756-012-0138-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11756-012-0138-2

Key words

Search

Navigation