Research Article
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Year 2021, Volume: 25 Issue: 1, 12 - 21, 01.02.2021
https://doi.org/10.16984/saufenbilder.793400

Abstract

References

  • [1] F. Scheutz and N. A. Strockbine, “Genus I Escherichia”. In: Garrity, GM, Brenner DJ, Krieg NR, Staley JT. (Eds.), Bergey’s manual of systematic bacteriology 2 (Part B). Springer, New York, pp. 607- 623, 2005.
  • [2] A.K. Bhunia, “Foodborne microbial pathogens: mechanisms and pathogenesis,” Springer, New York, 2008.
  • [3] WHO, “Home/Newsroom/Fact sheets/Detail/E. coli, 7 February 2018,”https://www.who.int/news-room/fact-sheets/detail/e-coli2018, 2018.
  • [4] G. I. Balali, D. Dekugmen, V. G. A. Dela, and P. Adjei-Kusi, “Microbial contamination, an increasing threat to the consumption of fresh fruits and vegetables in Today’s world,” International Journal of Microbiology, Article ID 3029295, 2020.
  • [5] FAO, “Increasing fruit and vegetable consumption becomes a global priority,” http://www.fao.org/english/newsroom/focus/2003/fruitveg1.htm, 2003.
  • [6] M. T. Jay, M. Cooley, D. Carychao, G. W. Wiscomb, R. A. Sweitzer, and L. Crawford-Miksza, “Escherichia coli O157:H7 in feral swine near spinach fields and cattle, central California coast,” Emerging Infectious Diseases, vol. 13, pp. 1908–1911, 2007.
  • [7] I. Friesema, G. Sigmundsdottir, K. van der Zwaluw, A. Heuvelink, B. Schimmer, C. de Jager, B. Rump, H. Briem, H. Hardardottir, A. Atladottir, E. Gudmundsdottir, and W. van Pelt, “An international outbreak of shiga toxin-producing Escherichia coli O157 infection due to lettuce, September–October 2007” Surveillance and outbreak reports, vol. 13, no. 50, pp. 1–5, 2008.
  • [8] R. B. Slayton, G. Turabelidze, S. D. Bennett, C. A. Schwensohn, A. Q. Yaffee, F. Khan, C. Butler, E. Trees, T. L. Ayers, M. L. Davis, A. S. Laufer, S. Gladbach, I. Williams, and L. B. Gieraltowski, “Outbreak of shiga toxin-producing Escherichia coli (STEC) O157:H7 associated with romaine lettuce consumption, 2011,” PLoS One vol. 8, no.2, e55300, 2013.
  • [9] CDC, “Outbreak of E. coli Infections Linked to Romaine Lettuce Final Update,” Available: https://www.cdc.gov/ecoli/2019/o157h7-11-19/index.html, 2020.
  • [10] CDC, “Multistate outbreak of shiga toxin-producing Escherichia coli O121 infections linked to raw clover sprouts (Final Update),” Available:https://www.cdc.gov/ecoli/2014/o121-05-14/index.html, 2014.
  • [11] K.M. Herman, A.J. Hall, and L. H. Gould, “Outbreaks attributed to fresh leafy vegetables, United States, 1973–2012,” Epidemiology and Infection, vol. 20, pp. 1–11, 2015.
  • [12] CDC, “Outbreak of E. coli Infections Linked to Romaine Lettuce,” Available: https://www.cdc.gov/ecoli/2018/o157h7-11-18/index.html, 2018.
  • [13] E. Giaouris, E. Heir, M. Desvaux, M. Hebraud, T. Moretro, S. Langsrud, A. Doulgeraki, G-J. Nychas, M. Kacaniova, K. Czaczyk, H. Olmez, and M. Simoes, “Intra- and inter-species interactions within biofilms of important foodborne bacterial pathogens,” Frontiers in Microbiology, vol. 6, no. 841, 2015.
  • [14] G. I. Balali, D. Dekugmen, V. G. A. Dela, and P. Adjei-Kusi, “Microbial contamination, an increasing threat to the consumption of fresh fruits and vegetables in Today’s world,” International Journal of Microbiology, Article ID 3029295, 2020.
  • [15] L. L. Nesse, C. Sekse, K. Berg, K.C. Johannesen, H. Solheim, L. K. Vestby, and A. M. Urdahlb, “Potentially pathogenic Escherichia coli can form a biofilm under conditions relevant to the food production chain,” Applied and Environmental Microbiology, vol. 80, no. 7, pp. 2042–9, 2014.
  • [16] U. Romling, W. D. Sierralta, K. Eriksson, and S. Normark, “Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter,” Molecular Microbiology, vol. 28, pp. 249-264, 1998.
  • [17] W. Bokranz, X. Wang, H. Tschape, and U. Römling, “Expression of cellulose and curli fimbriae by Escherichia coli isolated from the gastrointestinal tract,” Journal of Medical Microbiology, vol. 54, pp. 1171–1182, 2005.
  • [18] X. Zogaj, M. Nimtz, M. Rohde,W. Bokranz, and U. Romling, “The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix,” Molecular Microbiology, vol. 39, pp. 1452–1463, 2001.
  • [19] J. Schiebel, A. Bohm, J. Nitschke, M. Burdukiewicz, J. Weinreich, A. Ali, D. Roggenbuck, S. Rödiger, and P. Schieracka, “Genotypic and phenotypic characteristics associated with biofilm formation by human clinical Escherichia coli isolates of different pathotypes,” Applied and Environmental Microbiology, vol. 83, no. 24, e01660-17, 2017.
  • [20] F.M. Ausubel, R.E. Kingston RE, R. Brent, D. D. Moore, J. Seidman , J.A. Smith, K. Struhl, “Current protocols in molecular biology,” Greene Publishing Associates & Wiley Interscience, New York, 1991.
  • [21] J. Chen and M.W. Griffiths, “PCR differentiation of Escherichia coli from other Gram negative bacteria using primers derived from the nucleotide sequences flanking the gene encoding the universal stress protein,” Letters in Applied Microbiology, vol. 27, pp. 369–371, 1998.
  • [22] S. Stepanovic, D. Vukovic, I. Dakic, B. Savic, and M. Svabic-Vlahovic, “A modified microtiter-plate test for quantification of Staphylococcal biofilm formation,” Journal of Microbiological Methods, vol. 40, pp. 175–179, 2000.
  • [23] S. Stepanovic, D. Vukovic, V. Hola, G. D. Bonaventura, S. Djukic, I. Cirkovic, and F. Ruzicka, “Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci,” APMIS, vol. 115, pp. 891–899, 2007.
  • [24] E. Walencka, S. Rozalska, B. Sadowska, and B. Rozalska, “The influence of Lactobacillus acidophilus-derived surfactants on Staphylococcal adhesion and biofilm formation,” Folia Microbiology, vol. 53, pp. 61–66, 2008.
  • [25] Y.T Wu, H. Zhu, M. Willcox, and F. Stapleton, F, “Removal of biofilm from contact lens storage cases,” Investigative Ophthalmology and Visual Science, vol. 51, pp. 6329-6333, 2010.
  • [26] M. Dubravka, P. Bojana, V. Maja, and T. Dalibor, and P. Vladimir, “Investigation of biofilm formation and phylogenetic typing of Escherichia coli strains isolated from milk of cows with mastitis,” Acta Veterinaria-Beograd, vol. 65, no. 2, pp. 202-216, 2015.
  • [27] R. Marti, M. Schmid, S. Kulli, K. Schneeberger, J. Naskova, S. Knochel, C. H. Ahrens, J. Hummerjohanna, “Biofilm formation potential of heat-resistant Escherichia coli dairy isolates and the complete genome of multidrug- resistant, heat-resistant strain fam21845,” Applied and Environmental Microbiology, vol. 83, no. 15, e00628-17, 2017.

Molecular Characterization and Biofilm Formation of Escherichia coli from Vegetables

Year 2021, Volume: 25 Issue: 1, 12 - 21, 01.02.2021
https://doi.org/10.16984/saufenbilder.793400

Abstract

Escherichia coli can cause diarrheal and extraintestinal illnesses in humans. Diarrheagenic E. coli can be transmit to human through consumption of contaminated food, including vegetables. Biofilm produced by E. coli during food processing plays a role in development of foodborne illnesses. Vegetables have often been involved in diarrheal E. coli infections. A total of 40 E. coli isolates from vegetables were tested to determine biofilm formation at 12°C, 25°C and 37°C by the crystal violet and MTT assays. All isolates were performed for the production of curli fimbriae and cellulose associated with biofilm formation on Congo red agar. Biofilm formation at 37°C, 25°C and 12°C was detected in 87.5%, 70% and 70% of the isolates, respectively. Biofilm formation among the E. coli isolates using the crystal violet and MTT assays showed a statistically significant difference between 12°C and 25°C as well as 12°C and 37°C (p < 0.05). However, no significant difference between 25 and 37°C (p > 0.05) was obtained. Three different morhotypes (bdar, pdar and saw) were identified based on the expression of curli fimbriae and cellulose. The incidence of the bdar morhotype was 27.5% and 50% at 25°C and 37°C, respectively. Prevalence of the pdar morphotype was 50% and 70% at 25°C and 37°C, respectively. At 25°C, only one isolate (2.5%) showed the saw morphotype. All isolates tested expressed curli fimbriae or cellulose, only three of which were non-biofilm producer using the crystal violet assay. This study demonstrated that the presence of biofilm forming E.coli isolates in vegetables may cause a risk to human health and food safety.

References

  • [1] F. Scheutz and N. A. Strockbine, “Genus I Escherichia”. In: Garrity, GM, Brenner DJ, Krieg NR, Staley JT. (Eds.), Bergey’s manual of systematic bacteriology 2 (Part B). Springer, New York, pp. 607- 623, 2005.
  • [2] A.K. Bhunia, “Foodborne microbial pathogens: mechanisms and pathogenesis,” Springer, New York, 2008.
  • [3] WHO, “Home/Newsroom/Fact sheets/Detail/E. coli, 7 February 2018,”https://www.who.int/news-room/fact-sheets/detail/e-coli2018, 2018.
  • [4] G. I. Balali, D. Dekugmen, V. G. A. Dela, and P. Adjei-Kusi, “Microbial contamination, an increasing threat to the consumption of fresh fruits and vegetables in Today’s world,” International Journal of Microbiology, Article ID 3029295, 2020.
  • [5] FAO, “Increasing fruit and vegetable consumption becomes a global priority,” http://www.fao.org/english/newsroom/focus/2003/fruitveg1.htm, 2003.
  • [6] M. T. Jay, M. Cooley, D. Carychao, G. W. Wiscomb, R. A. Sweitzer, and L. Crawford-Miksza, “Escherichia coli O157:H7 in feral swine near spinach fields and cattle, central California coast,” Emerging Infectious Diseases, vol. 13, pp. 1908–1911, 2007.
  • [7] I. Friesema, G. Sigmundsdottir, K. van der Zwaluw, A. Heuvelink, B. Schimmer, C. de Jager, B. Rump, H. Briem, H. Hardardottir, A. Atladottir, E. Gudmundsdottir, and W. van Pelt, “An international outbreak of shiga toxin-producing Escherichia coli O157 infection due to lettuce, September–October 2007” Surveillance and outbreak reports, vol. 13, no. 50, pp. 1–5, 2008.
  • [8] R. B. Slayton, G. Turabelidze, S. D. Bennett, C. A. Schwensohn, A. Q. Yaffee, F. Khan, C. Butler, E. Trees, T. L. Ayers, M. L. Davis, A. S. Laufer, S. Gladbach, I. Williams, and L. B. Gieraltowski, “Outbreak of shiga toxin-producing Escherichia coli (STEC) O157:H7 associated with romaine lettuce consumption, 2011,” PLoS One vol. 8, no.2, e55300, 2013.
  • [9] CDC, “Outbreak of E. coli Infections Linked to Romaine Lettuce Final Update,” Available: https://www.cdc.gov/ecoli/2019/o157h7-11-19/index.html, 2020.
  • [10] CDC, “Multistate outbreak of shiga toxin-producing Escherichia coli O121 infections linked to raw clover sprouts (Final Update),” Available:https://www.cdc.gov/ecoli/2014/o121-05-14/index.html, 2014.
  • [11] K.M. Herman, A.J. Hall, and L. H. Gould, “Outbreaks attributed to fresh leafy vegetables, United States, 1973–2012,” Epidemiology and Infection, vol. 20, pp. 1–11, 2015.
  • [12] CDC, “Outbreak of E. coli Infections Linked to Romaine Lettuce,” Available: https://www.cdc.gov/ecoli/2018/o157h7-11-18/index.html, 2018.
  • [13] E. Giaouris, E. Heir, M. Desvaux, M. Hebraud, T. Moretro, S. Langsrud, A. Doulgeraki, G-J. Nychas, M. Kacaniova, K. Czaczyk, H. Olmez, and M. Simoes, “Intra- and inter-species interactions within biofilms of important foodborne bacterial pathogens,” Frontiers in Microbiology, vol. 6, no. 841, 2015.
  • [14] G. I. Balali, D. Dekugmen, V. G. A. Dela, and P. Adjei-Kusi, “Microbial contamination, an increasing threat to the consumption of fresh fruits and vegetables in Today’s world,” International Journal of Microbiology, Article ID 3029295, 2020.
  • [15] L. L. Nesse, C. Sekse, K. Berg, K.C. Johannesen, H. Solheim, L. K. Vestby, and A. M. Urdahlb, “Potentially pathogenic Escherichia coli can form a biofilm under conditions relevant to the food production chain,” Applied and Environmental Microbiology, vol. 80, no. 7, pp. 2042–9, 2014.
  • [16] U. Romling, W. D. Sierralta, K. Eriksson, and S. Normark, “Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter,” Molecular Microbiology, vol. 28, pp. 249-264, 1998.
  • [17] W. Bokranz, X. Wang, H. Tschape, and U. Römling, “Expression of cellulose and curli fimbriae by Escherichia coli isolated from the gastrointestinal tract,” Journal of Medical Microbiology, vol. 54, pp. 1171–1182, 2005.
  • [18] X. Zogaj, M. Nimtz, M. Rohde,W. Bokranz, and U. Romling, “The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix,” Molecular Microbiology, vol. 39, pp. 1452–1463, 2001.
  • [19] J. Schiebel, A. Bohm, J. Nitschke, M. Burdukiewicz, J. Weinreich, A. Ali, D. Roggenbuck, S. Rödiger, and P. Schieracka, “Genotypic and phenotypic characteristics associated with biofilm formation by human clinical Escherichia coli isolates of different pathotypes,” Applied and Environmental Microbiology, vol. 83, no. 24, e01660-17, 2017.
  • [20] F.M. Ausubel, R.E. Kingston RE, R. Brent, D. D. Moore, J. Seidman , J.A. Smith, K. Struhl, “Current protocols in molecular biology,” Greene Publishing Associates & Wiley Interscience, New York, 1991.
  • [21] J. Chen and M.W. Griffiths, “PCR differentiation of Escherichia coli from other Gram negative bacteria using primers derived from the nucleotide sequences flanking the gene encoding the universal stress protein,” Letters in Applied Microbiology, vol. 27, pp. 369–371, 1998.
  • [22] S. Stepanovic, D. Vukovic, I. Dakic, B. Savic, and M. Svabic-Vlahovic, “A modified microtiter-plate test for quantification of Staphylococcal biofilm formation,” Journal of Microbiological Methods, vol. 40, pp. 175–179, 2000.
  • [23] S. Stepanovic, D. Vukovic, V. Hola, G. D. Bonaventura, S. Djukic, I. Cirkovic, and F. Ruzicka, “Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci,” APMIS, vol. 115, pp. 891–899, 2007.
  • [24] E. Walencka, S. Rozalska, B. Sadowska, and B. Rozalska, “The influence of Lactobacillus acidophilus-derived surfactants on Staphylococcal adhesion and biofilm formation,” Folia Microbiology, vol. 53, pp. 61–66, 2008.
  • [25] Y.T Wu, H. Zhu, M. Willcox, and F. Stapleton, F, “Removal of biofilm from contact lens storage cases,” Investigative Ophthalmology and Visual Science, vol. 51, pp. 6329-6333, 2010.
  • [26] M. Dubravka, P. Bojana, V. Maja, and T. Dalibor, and P. Vladimir, “Investigation of biofilm formation and phylogenetic typing of Escherichia coli strains isolated from milk of cows with mastitis,” Acta Veterinaria-Beograd, vol. 65, no. 2, pp. 202-216, 2015.
  • [27] R. Marti, M. Schmid, S. Kulli, K. Schneeberger, J. Naskova, S. Knochel, C. H. Ahrens, J. Hummerjohanna, “Biofilm formation potential of heat-resistant Escherichia coli dairy isolates and the complete genome of multidrug- resistant, heat-resistant strain fam21845,” Applied and Environmental Microbiology, vol. 83, no. 15, e00628-17, 2017.
There are 27 citations in total.

Details

Primary Language English
Subjects Structural Biology
Journal Section Research Articles
Authors

Fatma Özdemir 0000-0002-4804-936X

Seza Arslan 0000-0002-2478-6875

Publication Date February 1, 2021
Submission Date September 10, 2020
Acceptance Date October 18, 2020
Published in Issue Year 2021 Volume: 25 Issue: 1

Cite

APA Özdemir, F., & Arslan, S. (2021). Molecular Characterization and Biofilm Formation of Escherichia coli from Vegetables. Sakarya University Journal of Science, 25(1), 12-21. https://doi.org/10.16984/saufenbilder.793400
AMA Özdemir F, Arslan S. Molecular Characterization and Biofilm Formation of Escherichia coli from Vegetables. SAUJS. February 2021;25(1):12-21. doi:10.16984/saufenbilder.793400
Chicago Özdemir, Fatma, and Seza Arslan. “Molecular Characterization and Biofilm Formation of Escherichia Coli from Vegetables”. Sakarya University Journal of Science 25, no. 1 (February 2021): 12-21. https://doi.org/10.16984/saufenbilder.793400.
EndNote Özdemir F, Arslan S (February 1, 2021) Molecular Characterization and Biofilm Formation of Escherichia coli from Vegetables. Sakarya University Journal of Science 25 1 12–21.
IEEE F. Özdemir and S. Arslan, “Molecular Characterization and Biofilm Formation of Escherichia coli from Vegetables”, SAUJS, vol. 25, no. 1, pp. 12–21, 2021, doi: 10.16984/saufenbilder.793400.
ISNAD Özdemir, Fatma - Arslan, Seza. “Molecular Characterization and Biofilm Formation of Escherichia Coli from Vegetables”. Sakarya University Journal of Science 25/1 (February 2021), 12-21. https://doi.org/10.16984/saufenbilder.793400.
JAMA Özdemir F, Arslan S. Molecular Characterization and Biofilm Formation of Escherichia coli from Vegetables. SAUJS. 2021;25:12–21.
MLA Özdemir, Fatma and Seza Arslan. “Molecular Characterization and Biofilm Formation of Escherichia Coli from Vegetables”. Sakarya University Journal of Science, vol. 25, no. 1, 2021, pp. 12-21, doi:10.16984/saufenbilder.793400.
Vancouver Özdemir F, Arslan S. Molecular Characterization and Biofilm Formation of Escherichia coli from Vegetables. SAUJS. 2021;25(1):12-21.