Research Article
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Year 2024, Accepted Papers, 1 - 11

Tuba Nur Sürkaç Mustafa Akçelik Nefise 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. Biofilms Vet Med, 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.

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 2024, Accepted Papers, 1 - 11

Tuba Nur Sürkaç Mustafa Akçelik Nefise 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 < 0.05). 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 Oxidative stress Salmonella Typhimurium Type 1 fimbriae

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. Biofilms Vet Med, 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

Mustafa Akçelik 0000-0002-1227-2324

Nefise Akçelik 0000-0001-5541-1681

Early Pub Date June 28, 2024
Publication Date
Submission Date November 13, 2023
Acceptance Date March 20, 2024
Published in Issue Year 2024Accepted Papers

Cite

APA Sürkaç, T. N., Akçelik, M., & Akçelik, N. (2024). 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 Dergisi1-11. https://doi.org/10.33988/auvfd.1390023
AMA Sürkaç TN, Akçelik M, Akçelik N. 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. Published online June 1, 2024:1-11. doi:10.33988/auvfd.1390023
Chicago Sürkaç, Tuba Nur, Mustafa Akçelik, and Nefise 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, June (June 2024), 1-11. https://doi.org/10.33988/auvfd.1390023.
EndNote Sürkaç TN, Akçelik M, Akçelik N (June 1, 2024) 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 1–11.
IEEE T. N. Sürkaç, M. Akçelik, and N. 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, pp. 1–11, June 2024, 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. June 2024. 1-11. https://doi.org/10.33988/auvfd.1390023.
JAMA Sürkaç TN, Akçelik M, Akçelik N. 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. 2024;:1–11.
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, 2024, pp. 1-11, doi:10.33988/auvfd.1390023.
Vancouver Sürkaç TN, Akçelik M, Akçelik N. 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. 2024:1-11.