Research Article
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Determination of the activity of the fimF gene and its N-terminal domain disrupted mutant on biofilm formation and its contribution to the oxidative stress response in S. Typhimurium

Year 2025, Volume: 72 Issue: 1, 23 - 33

Tuba Nur Sürkaç , Nefise Akçelik , Mustafa Akçelik

https://doi.org/10.33988/auvfd.1390023

Abstract

Fimbriae is an important virulence factor which plays a key role in cell attachment and colonization of the intestinal mucosa during an infection of Salmonella, a pathogen that causes gastroenteritis and systemic infection in humans. In S. Typhimurium, type 1 fimbriae production strengthens the oxidative stress response. This study aimed to determine the effectiveness of the fimF gene and its N-terminal domain on biofilm formation in S. Typhimurium and their contribution to the oxidative stress response. Before the experiments to prove whether the N-terminal domain of the FimF protein is the region that determines the mechanism and function of the fimF gene; only the N-terminal domain of the fimF gene was cloned behind the pBAD promoter. As a result of biofilm experiments on polystyrene surfaces, it was determined that the biofilm production capacity was reduced significantly in mutant strains in terms of fimF and dam genes (P<0.01). In the oxidative stress response experiment conducted in the presence of hydrogen peroxide (H2O2), it was determined that the mutant strains were more resistant to hydrogen peroxide than the wild-type strain, therefore Salmonella cells perceived the absence of Dam methylase enzyme and FimF protein as a critical internal stress condition and produced strong responses to these stress conditions. As a result of comparative analysis of the N-terminal domain cloned mutant strain with the wild-type, it was proven that the N-terminal domain of the protein in question acts as an adapter protein, due to its close similarities with the wild-type.

Keywords

Biofilm formation fimF gene N-terminal domain Salmonella Typhimurium Type 1 fimbriae

Thanks

This study was derived from the MSc thesis of the first author.

References

  • Amano A (2010): Bacterial adhesins to host components in periodontitis. Periodontol, 52, 12-37.
  • Aya Castañeda M, Sarnacki SH, Noto Llana M, et al (2015): Dam methylation is required for efficient biofilm production in Salmonella enterica serovar Enteritidis. Int J Food Microbiol, 193, 15-22.
  • Bäumler AJ, Tsolis RM, Heffron F (1997): Fimbrial adhesins of Salmonella typhimurium. Role in bacterial interactions with epithelial cells. Adv Exp Med Biol, 412, 149-158.
  • Beachey EH (1981): Bacterial adherence: adhesin receptor interaction mediating the attachment of bacteria to mucosal surface. J Infect Dis, 143, 325-345.
  • Boddicker JD, Ledeboer NA, Jagnow J, et al (2002): Differential binding to and biofilm formation on, HEp-2 cells by Salmonella enterica serovar Typhimurium is dependent upon allelic variation in the fimH gene of the fim gene cluster. Mol Microbiol, 45, 1255-1265.
  • Bouckaert J, Mackenzie J, de Paz JL, et al (2006): The affinity of the FimH fimbrial adhesin is receptor-driven and quasi-independent of Escherichia coli pathotypes. Mol Microbiol, 61, 1556-1568.
  • Bourgeois JS, Anderson CE, Wang L, et al (2022): Integration of the Salmonella Typhimurium methylome and transcriptome reveals that DNA methylation and transcriptional regulation are largely decoupled under virulence-related conditions. mBio, 13, e0346421.
  • Boyd EF, Hartl DL (1999): Analysis of the type 1 pilin gene cluster fim in Salmonella: its distinct evolutionary histories in the 5' and 3' regions. J Bacteriol, 181, 1301-1308.
  • Campos-Galvão ME, Ribon AO, Araújo EF, et al (2016): Changes in the Salmonella enterica Enteritidis phenotypes in presence of acyl homoserine lactone quorum sensing signals. J Basic Microbiol, 56, 493-501.
  • Castelijn GA, Van der Veen S, Zwietering MH, et al (2012): Diversity in biofilm formation and production of curli fimbriae and cellulose of Salmonella Typhimurium strains of different origin in high and low nutrient medium. Biofouling, 28, 51-63.
  • Chatti A, Messaoudi N, Mihoub M, et al (2012): Effects of hydrogen peroxide on the motility, catalase and superoxide dismutase of dam and/or seqA mutant of Salmonella typhimurium. World J Microbiol Biotechnol, 28, 129-133.
  • Crawford RW, Reeve KE, Gunn JS (2010): Flagellated but not hyperfimbriated Salmonella enterica serovar Typhimurium attaches to and forms biofilms on cholesterol-coated surfaces. J Bacteriol, 192, 2981-2990.
  • Datsenko KA, Wanner BL (2000): One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. PNAS, 97, 6640-6645.
  • Donlan RM (2002): Biofilms: microbial life on surfaces. Emerg Infect Dis, 8, 881-890.
  • Flemming HC, Wingender J, Szewzyk U, et al (2016): Biofilms: an emergent form of bacterial life. Nat Rev Microbiol, 14, 563-575.
  • Gonzalez-Escobedo G, Gunn JS (2013): Identification of Salmonella enterica serovar Typhimurium genes regulated during biofilm formation on cholesterol gallstone surfaces. Infect Immun, 81, 3770-3780.
  • Gossert AD, Bettendorff P, Puorger C, et al (2008): NMR structure of the Escherichia coli type 1 pilus subunit FimF and its interactions with other pilus subunits. J Mol Biol, 375, 752-763.
  • Guo Y, Gu D, Huang T, et al (2020): Essential role of Salmonella Enteritidis DNA adenine methylase in modulating inflammasome activation. BMC Microbiol, 20, 226.
  • Hahn MM, González JF, Gunn JS (2021): Salmonella biofilms tolerate hydrogen peroxide by a combination of extracellular polymeric substance barrier function and catalase enzymes. Front Cell Infect Microbiol, 11, 683081.
  • Hsu CY, Wu YL, Lin HC, et al (2021): A novel dibenzoxazepine attenuates intracellular Salmonella Typhimurium oxidative stress resistance. Microbiol Spectr, 9, e0151921.
  • Jamal M, Ahmad W, Andleeb S, et al (2018): Bacterial biofilm and associated infections. J Chin Med Assoc, 81, 7-11.
  • Keçeli Oğuz S, Has EG, Akçelik N, et al (2023): Phenotypic impacts and genetic regulation characteristics of the DNA adenine methylase gene (dam) in S. Typhimurium biofilm forms. Res Microbiol, 174, 103991.
  • Kim JS, Liu L, Vázquez-Torres A (2021): The DnaK/DnaJ chaperone system enables RNA polymerase-DksA complex formation in Salmonella experiencing oxidative stress. mBio, 12, e03443-20.
  • Kisiela D, Laskowska A, Sapeta A, et al (2006): Functional characterization of the FimH adhesin from Salmonella enterica serovar Enteritidis. Microbiology (Reading, England), 152, 1337-1346.
  • Kisiela DI, Kramer JJ, Tchesnokova V, et al (2011): Allosteric catch bond properties of the FimH adhesin from Salmonella enterica serovar Typhimurium. J Biol Chem, 286, 38136-38147.
  • Kloppsteck P, Hall M, Hasegawa Y, et al (2016): Structure of the fimbrial protein Mfa4 from Porphyromonas gingivalis in its precursor form: implications for a donor-strand complementation mechanism. Sci Rep, 6, 22945.
  • Kolenda R, Ugorski M, Grzymajlo K (2019): Everything you always wanted to know about salmonella type 1 fimbriae, but were afraid to ask. Front Microbiol, 10, 1017.
  • Lane MC, Mobley HL (2007): Role of P-fimbrial-mediated adherence in pyelonephritis and persistence of uropathogenic Escherichia coli (UPEC) in the mammalian kidney. Kidney Int, 72, 19-25.
  • Leusch HG, Drzeniek Z, Markos-Pusztai Z, et al (1991): Binding of Escherichia coli and Salmonella strains to members of the carcinoembryonic antigen family: differential binding inhibition by aromatic alpha-glycosides of mannose. Infect Immun, 59, 2051-2057.
  • Mannan T, Rafique MW, Bhatti MH, et al (2020): Type 1 fimbriae and motility play a pivotal role during interactions of Salmonella typhimurium with Acanthamoeba castellanii (T4 Genotype). Curr Microbiol, 77, 836-845.
  • Morales EH, Calderón IL, Collao B, et al (2012): Hypochlorous acid and hydrogen peroxide-induced negative regulation of Salmonella enterica serovar Typhimurium ompW by the response regulator ArcA. BMC Microbiology, 12, 63.
  • Nuccio SP, Baumler AJ (2007): Evolution of the chaperone/usher assembly pathway: fimbrial classification goes Greek. Microbiol Mol Biol Rev, 71, 551-575.
  • O'Toole G, Kaplan HB, Kolter R (2000): Biofilm formation as microbial development. Annu Rev Microbiol, 54, 49-79.
  • Percival SL, Malic S, Cruz H, et al (2011): Introduction to Biofilms. In: Biofilms Vet Med, Volume 6. Ed: J. William Costerton. Pp: 41-68.
  • Rehman T, Yin L, Latif MB, et al (2019): Adhesive mechanism of different Salmonella fimbrial adhesins. Microb Pathog, 137, 103748.
  • Römling U, Rohde M (1999): Flagella modulate the multicellular behavior of Salmonella typhimurium on the community level. FEMS Microbiol Lett, 180, 91-102.
  • Römling U, Rohde M, Olsén A, et al (2000): AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol, 36, 10-23.
  • Rosen DA, Pinkner JS, Walker JN, et al (2008): Molecular variations in Klebsiella pneumoniae and Escherichia coli FimH affect function and pathogenesis in the urinary tract. Infect Immun, 76, 3346-3356.
  • Russell PW, Orndorff PE (1992): Lesions in two Escherichia coli type 1 pilus genes alter pilus number and length without affecting receptor binding. J Bacteriol, 174, 5923-5935.
  • Saini S, Pearl JA, Rao CV (2009): Role of FimW, FimY, and FimZ in regulating the expression of type 1 fimbriae in Salmonella enterica serovar Typhimurium. J Bacteriol, 191, 3003-3010.
  • Sambrook J, Russell DW (2001): Mole Molecular Cloning, A Laboratory Manual. 3rd ed. Cold Spring Harbor Laboratory Press, New York.
  • Solano C, García B, Valle J, et al (2002): Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Mol Microbiol, 43, 793-808.
  • Stepanović S, Cirković I, Ranin L, et al (2004): Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Lett Appl Microbiol, 38, 428-432.
  • Tareb R, Bernardeau M, Gueguen M, et al (2013): In vitro characterization of aggregation and adhesion properties of viable and heat-killed forms of two probiotic Lactobacillus strains and interaction with foodborne zoonotic bacteria, especially Campylobacter jejuni. J Med Microbiol, 62, 637-649.
  • Thankavel K, Shah AH, Cohen MS, et al (1999): Molecular basis for the enterocyte tropism exhibited by Salmonella Typhimurium type 1 fimbriae. J Biol Chem, 274, 5797-5809.
  • Vestby LK, Møretrø T, Langsrud S, et al (2009): Biofilm forming abilities of Salmonella are correlated with persistence in fish meal- and feed factories. BMC Vet Res, 5, 20.
  • Wagner C, Hensel M (2011): Adhesive mechanisms of Salmonella enterica. Adv Exp Med Biol, 715, 17-34.
  • Worthington RJ, Richards JJ, Melander C (2012): Small molecule control of bacterial biofilms. OBC, 10, 7457-7474.
  • Yeh KS, Tinker JK, Clegg S (2002): FimZ binds the Salmonella Typhimurium fimA promoter region and may regulate its own expression with FimY. Microbiol Immun, 46, 1-10.
  • Zeiner SA, Dwyer BE, Clegg S (2012): FimA, FimF, and FimH are necessary for assembly of type 1 fimbriae on Salmonella enterica serovar Typhimurium. Infect Immun, 80, 3289-3296.

Year 2025, Volume: 72 Issue: 1, 23 - 33

Tuba Nur Sürkaç , Nefise Akçelik , Mustafa Akçelik

https://doi.org/10.33988/auvfd.1390023

Abstract

Ethical Statement

Bu çalışmada herhangi bir insan ve/veya hayvan deneği ya da onlardan alınan örnekler kullanılmamıştır. Bu nedenle söz konusu çalışma için herhangi bir etik onaya ihtiyaç yoktur.

References

  • Amano A (2010): Bacterial adhesins to host components in periodontitis. Periodontol, 52, 12-37.
  • Aya Castañeda M, Sarnacki SH, Noto Llana M, et al (2015): Dam methylation is required for efficient biofilm production in Salmonella enterica serovar Enteritidis. Int J Food Microbiol, 193, 15-22.
  • Bäumler AJ, Tsolis RM, Heffron F (1997): Fimbrial adhesins of Salmonella typhimurium. Role in bacterial interactions with epithelial cells. Adv Exp Med Biol, 412, 149-158.
  • Beachey EH (1981): Bacterial adherence: adhesin receptor interaction mediating the attachment of bacteria to mucosal surface. J Infect Dis, 143, 325-345.
  • Boddicker JD, Ledeboer NA, Jagnow J, et al (2002): Differential binding to and biofilm formation on, HEp-2 cells by Salmonella enterica serovar Typhimurium is dependent upon allelic variation in the fimH gene of the fim gene cluster. Mol Microbiol, 45, 1255-1265.
  • Bouckaert J, Mackenzie J, de Paz JL, et al (2006): The affinity of the FimH fimbrial adhesin is receptor-driven and quasi-independent of Escherichia coli pathotypes. Mol Microbiol, 61, 1556-1568.
  • Bourgeois JS, Anderson CE, Wang L, et al (2022): Integration of the Salmonella Typhimurium methylome and transcriptome reveals that DNA methylation and transcriptional regulation are largely decoupled under virulence-related conditions. mBio, 13, e0346421.
  • Boyd EF, Hartl DL (1999): Analysis of the type 1 pilin gene cluster fim in Salmonella: its distinct evolutionary histories in the 5' and 3' regions. J Bacteriol, 181, 1301-1308.
  • Campos-Galvão ME, Ribon AO, Araújo EF, et al (2016): Changes in the Salmonella enterica Enteritidis phenotypes in presence of acyl homoserine lactone quorum sensing signals. J Basic Microbiol, 56, 493-501.
  • Castelijn GA, Van der Veen S, Zwietering MH, et al (2012): Diversity in biofilm formation and production of curli fimbriae and cellulose of Salmonella Typhimurium strains of different origin in high and low nutrient medium. Biofouling, 28, 51-63.
  • Chatti A, Messaoudi N, Mihoub M, et al (2012): Effects of hydrogen peroxide on the motility, catalase and superoxide dismutase of dam and/or seqA mutant of Salmonella typhimurium. World J Microbiol Biotechnol, 28, 129-133.
  • Crawford RW, Reeve KE, Gunn JS (2010): Flagellated but not hyperfimbriated Salmonella enterica serovar Typhimurium attaches to and forms biofilms on cholesterol-coated surfaces. J Bacteriol, 192, 2981-2990.
  • Datsenko KA, Wanner BL (2000): One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. PNAS, 97, 6640-6645.
  • Donlan RM (2002): Biofilms: microbial life on surfaces. Emerg Infect Dis, 8, 881-890.
  • Flemming HC, Wingender J, Szewzyk U, et al (2016): Biofilms: an emergent form of bacterial life. Nat Rev Microbiol, 14, 563-575.
  • Gonzalez-Escobedo G, Gunn JS (2013): Identification of Salmonella enterica serovar Typhimurium genes regulated during biofilm formation on cholesterol gallstone surfaces. Infect Immun, 81, 3770-3780.
  • Gossert AD, Bettendorff P, Puorger C, et al (2008): NMR structure of the Escherichia coli type 1 pilus subunit FimF and its interactions with other pilus subunits. J Mol Biol, 375, 752-763.
  • Guo Y, Gu D, Huang T, et al (2020): Essential role of Salmonella Enteritidis DNA adenine methylase in modulating inflammasome activation. BMC Microbiol, 20, 226.
  • Hahn MM, González JF, Gunn JS (2021): Salmonella biofilms tolerate hydrogen peroxide by a combination of extracellular polymeric substance barrier function and catalase enzymes. Front Cell Infect Microbiol, 11, 683081.
  • Hsu CY, Wu YL, Lin HC, et al (2021): A novel dibenzoxazepine attenuates intracellular Salmonella Typhimurium oxidative stress resistance. Microbiol Spectr, 9, e0151921.
  • Jamal M, Ahmad W, Andleeb S, et al (2018): Bacterial biofilm and associated infections. J Chin Med Assoc, 81, 7-11.
  • Keçeli Oğuz S, Has EG, Akçelik N, et al (2023): Phenotypic impacts and genetic regulation characteristics of the DNA adenine methylase gene (dam) in S. Typhimurium biofilm forms. Res Microbiol, 174, 103991.
  • Kim JS, Liu L, Vázquez-Torres A (2021): The DnaK/DnaJ chaperone system enables RNA polymerase-DksA complex formation in Salmonella experiencing oxidative stress. mBio, 12, e03443-20.
  • Kisiela D, Laskowska A, Sapeta A, et al (2006): Functional characterization of the FimH adhesin from Salmonella enterica serovar Enteritidis. Microbiology (Reading, England), 152, 1337-1346.
  • Kisiela DI, Kramer JJ, Tchesnokova V, et al (2011): Allosteric catch bond properties of the FimH adhesin from Salmonella enterica serovar Typhimurium. J Biol Chem, 286, 38136-38147.
  • Kloppsteck P, Hall M, Hasegawa Y, et al (2016): Structure of the fimbrial protein Mfa4 from Porphyromonas gingivalis in its precursor form: implications for a donor-strand complementation mechanism. Sci Rep, 6, 22945.
  • Kolenda R, Ugorski M, Grzymajlo K (2019): Everything you always wanted to know about salmonella type 1 fimbriae, but were afraid to ask. Front Microbiol, 10, 1017.
  • Lane MC, Mobley HL (2007): Role of P-fimbrial-mediated adherence in pyelonephritis and persistence of uropathogenic Escherichia coli (UPEC) in the mammalian kidney. Kidney Int, 72, 19-25.
  • Leusch HG, Drzeniek Z, Markos-Pusztai Z, et al (1991): Binding of Escherichia coli and Salmonella strains to members of the carcinoembryonic antigen family: differential binding inhibition by aromatic alpha-glycosides of mannose. Infect Immun, 59, 2051-2057.
  • Mannan T, Rafique MW, Bhatti MH, et al (2020): Type 1 fimbriae and motility play a pivotal role during interactions of Salmonella typhimurium with Acanthamoeba castellanii (T4 Genotype). Curr Microbiol, 77, 836-845.
  • Morales EH, Calderón IL, Collao B, et al (2012): Hypochlorous acid and hydrogen peroxide-induced negative regulation of Salmonella enterica serovar Typhimurium ompW by the response regulator ArcA. BMC Microbiology, 12, 63.
  • Nuccio SP, Baumler AJ (2007): Evolution of the chaperone/usher assembly pathway: fimbrial classification goes Greek. Microbiol Mol Biol Rev, 71, 551-575.
  • O'Toole G, Kaplan HB, Kolter R (2000): Biofilm formation as microbial development. Annu Rev Microbiol, 54, 49-79.
  • Percival SL, Malic S, Cruz H, et al (2011): Introduction to Biofilms. In: Biofilms Vet Med, Volume 6. Ed: J. William Costerton. Pp: 41-68.
  • Rehman T, Yin L, Latif MB, et al (2019): Adhesive mechanism of different Salmonella fimbrial adhesins. Microb Pathog, 137, 103748.
  • Römling U, Rohde M (1999): Flagella modulate the multicellular behavior of Salmonella typhimurium on the community level. FEMS Microbiol Lett, 180, 91-102.
  • Römling U, Rohde M, Olsén A, et al (2000): AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol, 36, 10-23.
  • Rosen DA, Pinkner JS, Walker JN, et al (2008): Molecular variations in Klebsiella pneumoniae and Escherichia coli FimH affect function and pathogenesis in the urinary tract. Infect Immun, 76, 3346-3356.
  • Russell PW, Orndorff PE (1992): Lesions in two Escherichia coli type 1 pilus genes alter pilus number and length without affecting receptor binding. J Bacteriol, 174, 5923-5935.
  • Saini S, Pearl JA, Rao CV (2009): Role of FimW, FimY, and FimZ in regulating the expression of type 1 fimbriae in Salmonella enterica serovar Typhimurium. J Bacteriol, 191, 3003-3010.
  • Sambrook J, Russell DW (2001): Mole Molecular Cloning, A Laboratory Manual. 3rd ed. Cold Spring Harbor Laboratory Press, New York.
  • Solano C, García B, Valle J, et al (2002): Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Mol Microbiol, 43, 793-808.
  • Stepanović S, Cirković I, Ranin L, et al (2004): Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Lett Appl Microbiol, 38, 428-432.
  • Tareb R, Bernardeau M, Gueguen M, et al (2013): In vitro characterization of aggregation and adhesion properties of viable and heat-killed forms of two probiotic Lactobacillus strains and interaction with foodborne zoonotic bacteria, especially Campylobacter jejuni. J Med Microbiol, 62, 637-649.
  • Thankavel K, Shah AH, Cohen MS, et al (1999): Molecular basis for the enterocyte tropism exhibited by Salmonella Typhimurium type 1 fimbriae. J Biol Chem, 274, 5797-5809.
  • Vestby LK, Møretrø T, Langsrud S, et al (2009): Biofilm forming abilities of Salmonella are correlated with persistence in fish meal- and feed factories. BMC Vet Res, 5, 20.
  • Wagner C, Hensel M (2011): Adhesive mechanisms of Salmonella enterica. Adv Exp Med Biol, 715, 17-34.
  • Worthington RJ, Richards JJ, Melander C (2012): Small molecule control of bacterial biofilms. OBC, 10, 7457-7474.
  • Yeh KS, Tinker JK, Clegg S (2002): FimZ binds the Salmonella Typhimurium fimA promoter region and may regulate its own expression with FimY. Microbiol Immun, 46, 1-10.
  • Zeiner SA, Dwyer BE, Clegg S (2012): FimA, FimF, and FimH are necessary for assembly of type 1 fimbriae on Salmonella enterica serovar Typhimurium. Infect Immun, 80, 3289-3296.
There are 50 citations in total.

Details

Primary Language English
Subjects Veterinary Bacteriology, Veterinary Microbiology
Journal Section Research Article
Authors

Tuba Nur Sürkaç 0000-0001-6828-2663

Nefise Akçelik 0000-0001-5541-1681

Mustafa Akçelik 0000-0002-1227-2324

Early Pub Date June 28, 2024
Publication Date
Submission Date November 13, 2023
Acceptance Date March 20, 2024
Published in Issue Year 2025Volume: 72 Issue: 1

Cite

APA Sürkaç, T. N., Akçelik, N., & Akçelik, M. (n.d.). Determination of the activity of the fimF gene and its N-terminal domain disrupted mutant on biofilm formation and its contribution to the oxidative stress response in S. Typhimurium. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 72(1), 23-33. https://doi.org/10.33988/auvfd.1390023
AMA Sürkaç TN, Akçelik N, Akçelik M. Determination of the activity of the fimF gene and its N-terminal domain disrupted mutant on biofilm formation and its contribution to the oxidative stress response in S. Typhimurium. Ankara Univ Vet Fak Derg. 72(1):23-33. doi:10.33988/auvfd.1390023
Chicago Sürkaç, Tuba Nur, Nefise Akçelik, and Mustafa Akçelik. “Determination of the Activity of the FimF Gene and Its N-Terminal Domain Disrupted Mutant on Biofilm Formation and Its Contribution to the Oxidative Stress Response in S. Typhimurium”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 72, no. 1 n.d.: 23-33. https://doi.org/10.33988/auvfd.1390023.
EndNote Sürkaç TN, Akçelik N, Akçelik M Determination of the activity of the fimF gene and its N-terminal domain disrupted mutant on biofilm formation and its contribution to the oxidative stress response in S. Typhimurium. Ankara Üniversitesi Veteriner Fakültesi Dergisi 72 1 23–33.
IEEE T. N. Sürkaç, N. Akçelik, and M. Akçelik, “Determination of the activity of the fimF gene and its N-terminal domain disrupted mutant on biofilm formation and its contribution to the oxidative stress response in S. Typhimurium”, Ankara Univ Vet Fak Derg, vol. 72, no. 1, pp. 23–33, doi: 10.33988/auvfd.1390023.
ISNAD Sürkaç, Tuba Nur et al. “Determination of the Activity of the FimF Gene and Its N-Terminal Domain Disrupted Mutant on Biofilm Formation and Its Contribution to the Oxidative Stress Response in S. Typhimurium”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 72/1 (n.d.), 23-33. https://doi.org/10.33988/auvfd.1390023.
JAMA Sürkaç TN, Akçelik N, Akçelik M. Determination of the activity of the fimF gene and its N-terminal domain disrupted mutant on biofilm formation and its contribution to the oxidative stress response in S. Typhimurium. Ankara Univ Vet Fak Derg.;72:23–33.
MLA Sürkaç, Tuba Nur et al. “Determination of the Activity of the FimF Gene and Its N-Terminal Domain Disrupted Mutant on Biofilm Formation and Its Contribution to the Oxidative Stress Response in S. Typhimurium”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 72, no. 1, pp. 23-33, doi:10.33988/auvfd.1390023.
Vancouver Sürkaç TN, Akçelik N, Akçelik M. Determination of the activity of the fimF gene and its N-terminal domain disrupted mutant on biofilm formation and its contribution to the oxidative stress response in S. Typhimurium. Ankara Univ Vet Fak Derg. 72(1):23-3.
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