Research Article
BibTex RIS Cite

Some virulence genes and biofilm formation capabilities of Listeria monocytogenes isolates from different sources

Year 2025, Volume: 72 Issue: 1, 35 - 45

Ahmet Murat Saytekin , Adem Adıgüzel Khaled Alkilani , Ayfer Güllü Yücetepe , Oktay Keskin

https://doi.org/10.33988/auvfd.1450034

Abstract

In this study, it was aimed to determine the biofilm-forming abilities of both clinical and food-borne isolates of Listeria monocytogenes, to investigate the presence of nine different virulence genes, and to consider the current threat status of this agent. A total of 28 isolates, 21 from food and seven from clinical origin, were used in the study. Two different methods, namely “tube adherence” and “microplate” were used to determine the biofilm formation abilities of isolates. For the determination of nine different virulence genes of Listeria monocytogenes (inlA, inlC, inlJ, hylA, luxS, flaA, prfA, inlB, actA), the method of polymerase chain reaction (PCR) was used. As a result, all isolates were found to be able to form a biofilm to varying degrees by both tube and microplate methods. These two methods were similar in terms of their results. All nine different virulence gene regions were detected at various rates in the isolates. Although the genes directly related to biofilm formation for the isolates weren't detected, to form biofilm was observed. The virulence genes detected in clinical origin isolates were proportionally higher than in food-borne isolates (except for flaA and prfA gene regions). It was concluded that bacteria of Listeria monocytogenes continue to form biofilm and carry virulence genes regardless they are from food or clinical origin. Also, food-borne contaminations continue to be a severe threat to human health. So, to prevent listeriosis, cases of both humans and animals should be taken required precautions and all cases should be considered carefully.

Keywords

Biofilm food Listeria monocytogenes livestock virulence genes

Ethical Statement

The study was reviewed and approved by the Animal Experiments Local Ethic Committee of Harran University, Şanlıurfa, Türkiye (Decision number:01-14 / 2019).

Supporting Institution

This research has been supported within the content of the projects no 20128 and 20021 respectively by Harran University Scientific Research Projects Coordinatorship.

Project Number

20128 ve 20021

Thanks

Some parts of this study were accepted to be master theses belonging to the second and third authors. Furthermore, these parts were presented in XV. National Congress of Veterinary Microbiology (With International Participation), 26-28 October 2022, Nevali Hotel- Şanlıurfa-TÜRKİYE.

References

  • Abdollahzade E, Ojagh SM, Hossein H, et al (2016): Prevalence and molecular characterization of Listeria spp. and Listeria monocytogenes isolated from fish, shrimp, and cooked ready-to-eat (RTE) aquatic products in Iran. LWT-Food Sci Technol, 73, 205-211.
  • Angelidis AS, Grammenou AS, Kotzamanidis C, et al (2023): Prevalence, serotypes, antimicrobial resistance and biofilm-forming ability of Listeria monocytogenes isolated from bulk-tank bovine milk in Northern Greece. Pathogens, 12, 837.
  • Angelo C, Pierluigi C, Emanuela Z, et al (2016): A look inside the Listeria monocytogenes biofilms extracellular matrix. Microorganisms, 4, 4-22.
  • Arslan S, Özdemir F (2020): Prevalence and antimicrobial resistance of Listeria species and molecular characterization of Listeria monocytogenes isolated from retail ready-to-eat foods. FEMS Microbiol Lett, 367, 006.
  • Arslan S, Baytur S (2018): Prevalence and antimicrobial resistance of Listeria species and subtyping and virulence factors of Listeria monocytogenes from retail meat. J Food Saf, 39, e12578.
  • Blais BW, Turner G, Sooknanan R, et al (1997): A nucleic acid sequence-based amplification system for detection of Listeria monocytogenes hlya sequences. Appl Environ Microbiol, 63, 310-313.
  • Bonsaglia E, Silva N, Fernades AJ, et al (2014): Production of biofilm by Listeria monocytogenes in different materials and temperatures. Food Control, 35, 386-391.
  • Borucki MK, Call DR (2003): Listeria monocytogenes serotype identification by PCR. J Clin Microbiol, 41, 5537-5540.
  • Cai S, Kabuki DY, Kuaye AY, et al (2002): Rational design of DNA sequence-based strategies for subtyping Listeria monocytogenes. J Clin Microbiol, 40, 3319–3325.
  • Choi MH, Park YJ, Kim M, et al (2018): Increasing incidence of listeriosis and infection-associated clinical outcomes. Ann Lab Med, 38, 102-109.
  • Christensen GD, Simpson WA, Bisno AL, et al (1982): Adherence of slime-producing strains of Staphylococcus epidermidis to smooth surfaces. Infect immun, 37, 318-326.
  • D’Agostino M, Wagner M, Vazquez-Boland JA, et al (2004): A validated PCR-based method to detect Listeria monocytogenes using raw milk as a food model—towards an international standard. J Food Prot, 67, 1646–1655.
  • Den Bakker HC, Cummings CA, Ferreira V, et al (2010): Comparative genomics of the bacterial genus Listeria: Genome evolution is characterized by limited gene acquisition and limited gene loss. BMC Genom, 11, 688.
  • Dhama K, Karthik K, Tiwari R, et al (2015): Listeriosis in animals, its public health significance (food-borne zoonosis) and advances in diagnosis and control: A comprehensive review. Vet Q, 35, 211–235.
  • Di Ciccio P, Rubiola S, Panebianco F, et al (2022): Biofilm formation and genomic features of Listeria monocytogenes strains isolated from meat and dairy industries located in Piedmont (Italy). Int J Food Microbiol, 378, 109784.
  • Doijad SP, Barbuddhe SB, Garg S, et al (2015): Biofilm-forming abilities of Listeria monocytogenes serotypes isolated from different sources. PLoS One, 10, e0137046.
  • Doumith M, Buchrieser C, Glaser P, et al (2004): Differentiation of the major Listeria monocytogenes serovars by multiplex PCR. J Clin Microbiol, 42, 3819-3822.
  • Engelbrecht F, Chun SK, Ochs C, et al (1996): A new prfa regulated gene of Listeria monocytogenes encoding a small, secreted protein which belongs to the family of internalins. Mol Microbiol, 21, 823-837.
  • Ericsson H, Unnerstad H, Mattsson JG, et al (2000): Molecular grouping of Listeria monocytogenes based on the sequence of the inlB gene. J Med Microbiol, 49, 73–80.
  • Gaillard JL, Berche P, Frehel C, et al (1991): Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell, 65, 1127-1141.
  • Haidar-Ahmad N, Kissoyan KAB, Fadlallah SM, et al (2016): Genotypic and virulence characteristics of Listeria monocytogenes recovered from food items in Lebanon. J Infect Dev Ctries, 10, 712-717.
  • İça T, Aydın F, Gümüşsoy KS, et al (2012): Conventional and molecular biotyping of Brucella strains isolated from cattle, sheep, and human. Ankara Univ Vet Fak Derg, 59, 259-264.
  • Jacquet C, Gouin E, Jeannel D, et al (2002): Expression of actA, ami, inlB, and listeriolysin O in Listeria monocytogenes of human and food origin. Appl Environ Microbiol, 68, 616–622.
  • Kotzamanidis C, Papadopoulos T, Vafeas G, et al (2019): Characterization of Listeria monocytogenes from encephalitis cases of small ruminants from different geographical regions, in Greece. J Appl Microbiol, 126, 1373-1382.
  • Lee B, Sophie C, Stéphanie B, et al (2019): Biofilm formation of Listeria monocytogenes strains under food processing environments and pan-genome-wide association study. Front Microbiol, 10, No:2698.
  • Lemon K, Nancy F, Roberto K (2010): The virulence regulator PrfA promotes biofilm formation by Listeria monocytogenes. J Bacteriol, 192, 3969-3976.
  • Lianou A, Nychas G-JE, Koutsoumanis KP (2020): Strain variability in biofilm formation: A food safety and quality perspective. Food Res Int, 137, 109424.
  • Liu D, Ainsworth AJ, Austin FW, et al (2003): Characterization of virulent and avirulent Listeria monocytogenes strains by PCR amplification of putative transcriptional regulator and internalin genes. J Med Microbiol, 52, 1066-1070.
  • Liu D, Lawrence ML, Austin FW, et al (2007): A multiplex PCR for species and virulence-specific determination of Listeria monocytogenes. J Microbiol Methods, 71, 133-140.
  • Maggio F, Rossi C, Chiaverini A, et al (2021): Genetic relationships and biofilm formation of Listeria monocytogenes isolated from the smoked salmon industry. Int J Food Microbiol, 356, 109353.
  • Manuel CS, Van Stelten A, Wiedmann M, et al (2015): Prevalence and distribution of Listeria monocytogenes inlA alleles prone to phase variation and inlA alleles with premature stop codon mutations among human, food, animal, and environmental isolates. Appl Environ Microbiol, 81, 8339-8345.
  • Matle I, Mbatha KR, Lentsoane O, et al (2019): Occurrence, serotypes, and characteristics of Listeria monocytogenes in meat and meat products in South Africa between 2014 and 2016. J Food Saf, 39, 12629.
  • Matle I, Mbatha KR, Madoroba E (2020): A review of Listeria monocytogenes from meat and meat products: Epidemiology, virulence factors, antimicrobial resistance and diagnosis. Onderstepoort J Vet Res, 87, a1869.
  • Meghdadi H, Khosravi AD, Sheikh AF, et al (2019): Isolation and characterization of Listeria Monocytogenes from environmental and clinical sources by culture and PCR-RFLP methods. Iran J Microbiol, 11, 7.
  • Nowaka J, Visnovsky SB, Pitmane AR, et al (2021): Biofilm formation by Listeria monocytogenes 15G01, a persistent isolate from a seafood-processing plant, is influenced by inactivation of multiple genes belonging to different functional groups. Food Microbiol, 87, e02349-20.
  • Osman KM, Kappell AD, Fox EM, et al (2020): Prevalence, pathogenicity, virulence, antibiotic resistance, and phylogenetic analysis of biofilm- producing Listeria monocytogenes isolated from different ecological niches in Egypt: Food, Humans, Animals, and Environment. Pathogens, 9, 5.
  • Pangallo D, Kaclíková E, Kuchta T, et al (2001): Detection of Listeria monocytogenes by polymerase chain reaction oriented to inlB gene. New Microbiol, 24, 333-339.
  • Poimenidou V, Dalmasso M, Papadimitriou K, et al (2018): Virulence gene sequencing highlights similarities and differences in sequences in Listeria monocytogenes serotype 1/2a and 4b strains of clinical and food origin from 3 different geographic locations. Front microbiol, 9, 1103.
  • Pyz-Łukasik R, Paszkiewicz W, Kiełbus M, et al (2022): Genetic diversity and potential virulence of Listeria monocytogenes isolates originating from Polish artisanal cheeses. Foods, 11, 2805.
  • Quereda JJ, Leclercq A, Moura A, et al (2020): Listeria valentina sp. nov., isolated from a water trough and the faeces of healthy sheep. Int J Syst Evol Microbiol, 70, 5868-5879.
  • Rantsiou K, Alessandria V, Urso R, et al (2008): Detection, quantification and vitality of Listeria monocytogenes in food as determined by quantitative PCR. Int J Food Microbiol, 121, 99-105.
  • Sela S, Frank S, Belausov E, et al (2006): A mutation in the luxS gene influences Listeria monocytogenes biofilm formation. Appl Environ Microbiol, 72, 5653– 5658.
  • Sharma S, Sharma V, Dahiya DK, et al (2017): Prevalence, virulence potential, and antibiotic susceptibility profile of Listeria monocytogenes isolated from bovine raw milk samples obtained from Rajasthan, India. Foodborne Pathog Dis, 14, 132-140.
  • Soni DK, Singh M, Singh DV, et al (2014): Virulence and genotypic characterization of Listeria monocytogenes isolated from vegetable and soil samples. BMC Microbiol, 14, 241.
  • 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.
  • Takeuchi K, Smith MA, Doyle MP (2003): Pathogenicity of food and clinical Listeria monocytogenes isolates in a mouse bioassay. J Food Prot, 66, 2362–2366.
  • Warke SR, Ingle VC, Kurkure NV, et al (2017): Biofilm formation and associated genes in Listeria monocytogenes. IJVSBT, 12, 7-12.
  • Wu S, Wu Q, Zhang J, et al (2015): Listeria monocytogenes prevalence and characteristics in retail raw foods in China. PLo S One, 10, e0136682.
  • Zhou X, Jiao X (2005): Polymerase chain reaction detection of Listeria monocytogenes using oligonucleotide primers targeting actA gene. Food Control, 16, 125–130.

Year 2025, Volume: 72 Issue: 1, 35 - 45

Ahmet Murat Saytekin , Adem Adıgüzel Khaled Alkilani , Ayfer Güllü Yücetepe , Oktay Keskin

https://doi.org/10.33988/auvfd.1450034

Abstract

Ethical Statement

Bu çalışmanın Etik Kurul Onayı gerektirmediğini beyan ederim.

Supporting Institution

Harran Üniversitesi Bilimsel Araştırma Projeleri Birimi

Project Number

20128 ve 20021

References

  • Abdollahzade E, Ojagh SM, Hossein H, et al (2016): Prevalence and molecular characterization of Listeria spp. and Listeria monocytogenes isolated from fish, shrimp, and cooked ready-to-eat (RTE) aquatic products in Iran. LWT-Food Sci Technol, 73, 205-211.
  • Angelidis AS, Grammenou AS, Kotzamanidis C, et al (2023): Prevalence, serotypes, antimicrobial resistance and biofilm-forming ability of Listeria monocytogenes isolated from bulk-tank bovine milk in Northern Greece. Pathogens, 12, 837.
  • Angelo C, Pierluigi C, Emanuela Z, et al (2016): A look inside the Listeria monocytogenes biofilms extracellular matrix. Microorganisms, 4, 4-22.
  • Arslan S, Özdemir F (2020): Prevalence and antimicrobial resistance of Listeria species and molecular characterization of Listeria monocytogenes isolated from retail ready-to-eat foods. FEMS Microbiol Lett, 367, 006.
  • Arslan S, Baytur S (2018): Prevalence and antimicrobial resistance of Listeria species and subtyping and virulence factors of Listeria monocytogenes from retail meat. J Food Saf, 39, e12578.
  • Blais BW, Turner G, Sooknanan R, et al (1997): A nucleic acid sequence-based amplification system for detection of Listeria monocytogenes hlya sequences. Appl Environ Microbiol, 63, 310-313.
  • Bonsaglia E, Silva N, Fernades AJ, et al (2014): Production of biofilm by Listeria monocytogenes in different materials and temperatures. Food Control, 35, 386-391.
  • Borucki MK, Call DR (2003): Listeria monocytogenes serotype identification by PCR. J Clin Microbiol, 41, 5537-5540.
  • Cai S, Kabuki DY, Kuaye AY, et al (2002): Rational design of DNA sequence-based strategies for subtyping Listeria monocytogenes. J Clin Microbiol, 40, 3319–3325.
  • Choi MH, Park YJ, Kim M, et al (2018): Increasing incidence of listeriosis and infection-associated clinical outcomes. Ann Lab Med, 38, 102-109.
  • Christensen GD, Simpson WA, Bisno AL, et al (1982): Adherence of slime-producing strains of Staphylococcus epidermidis to smooth surfaces. Infect immun, 37, 318-326.
  • D’Agostino M, Wagner M, Vazquez-Boland JA, et al (2004): A validated PCR-based method to detect Listeria monocytogenes using raw milk as a food model—towards an international standard. J Food Prot, 67, 1646–1655.
  • Den Bakker HC, Cummings CA, Ferreira V, et al (2010): Comparative genomics of the bacterial genus Listeria: Genome evolution is characterized by limited gene acquisition and limited gene loss. BMC Genom, 11, 688.
  • Dhama K, Karthik K, Tiwari R, et al (2015): Listeriosis in animals, its public health significance (food-borne zoonosis) and advances in diagnosis and control: A comprehensive review. Vet Q, 35, 211–235.
  • Di Ciccio P, Rubiola S, Panebianco F, et al (2022): Biofilm formation and genomic features of Listeria monocytogenes strains isolated from meat and dairy industries located in Piedmont (Italy). Int J Food Microbiol, 378, 109784.
  • Doijad SP, Barbuddhe SB, Garg S, et al (2015): Biofilm-forming abilities of Listeria monocytogenes serotypes isolated from different sources. PLoS One, 10, e0137046.
  • Doumith M, Buchrieser C, Glaser P, et al (2004): Differentiation of the major Listeria monocytogenes serovars by multiplex PCR. J Clin Microbiol, 42, 3819-3822.
  • Engelbrecht F, Chun SK, Ochs C, et al (1996): A new prfa regulated gene of Listeria monocytogenes encoding a small, secreted protein which belongs to the family of internalins. Mol Microbiol, 21, 823-837.
  • Ericsson H, Unnerstad H, Mattsson JG, et al (2000): Molecular grouping of Listeria monocytogenes based on the sequence of the inlB gene. J Med Microbiol, 49, 73–80.
  • Gaillard JL, Berche P, Frehel C, et al (1991): Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell, 65, 1127-1141.
  • Haidar-Ahmad N, Kissoyan KAB, Fadlallah SM, et al (2016): Genotypic and virulence characteristics of Listeria monocytogenes recovered from food items in Lebanon. J Infect Dev Ctries, 10, 712-717.
  • İça T, Aydın F, Gümüşsoy KS, et al (2012): Conventional and molecular biotyping of Brucella strains isolated from cattle, sheep, and human. Ankara Univ Vet Fak Derg, 59, 259-264.
  • Jacquet C, Gouin E, Jeannel D, et al (2002): Expression of actA, ami, inlB, and listeriolysin O in Listeria monocytogenes of human and food origin. Appl Environ Microbiol, 68, 616–622.
  • Kotzamanidis C, Papadopoulos T, Vafeas G, et al (2019): Characterization of Listeria monocytogenes from encephalitis cases of small ruminants from different geographical regions, in Greece. J Appl Microbiol, 126, 1373-1382.
  • Lee B, Sophie C, Stéphanie B, et al (2019): Biofilm formation of Listeria monocytogenes strains under food processing environments and pan-genome-wide association study. Front Microbiol, 10, No:2698.
  • Lemon K, Nancy F, Roberto K (2010): The virulence regulator PrfA promotes biofilm formation by Listeria monocytogenes. J Bacteriol, 192, 3969-3976.
  • Lianou A, Nychas G-JE, Koutsoumanis KP (2020): Strain variability in biofilm formation: A food safety and quality perspective. Food Res Int, 137, 109424.
  • Liu D, Ainsworth AJ, Austin FW, et al (2003): Characterization of virulent and avirulent Listeria monocytogenes strains by PCR amplification of putative transcriptional regulator and internalin genes. J Med Microbiol, 52, 1066-1070.
  • Liu D, Lawrence ML, Austin FW, et al (2007): A multiplex PCR for species and virulence-specific determination of Listeria monocytogenes. J Microbiol Methods, 71, 133-140.
  • Maggio F, Rossi C, Chiaverini A, et al (2021): Genetic relationships and biofilm formation of Listeria monocytogenes isolated from the smoked salmon industry. Int J Food Microbiol, 356, 109353.
  • Manuel CS, Van Stelten A, Wiedmann M, et al (2015): Prevalence and distribution of Listeria monocytogenes inlA alleles prone to phase variation and inlA alleles with premature stop codon mutations among human, food, animal, and environmental isolates. Appl Environ Microbiol, 81, 8339-8345.
  • Matle I, Mbatha KR, Lentsoane O, et al (2019): Occurrence, serotypes, and characteristics of Listeria monocytogenes in meat and meat products in South Africa between 2014 and 2016. J Food Saf, 39, 12629.
  • Matle I, Mbatha KR, Madoroba E (2020): A review of Listeria monocytogenes from meat and meat products: Epidemiology, virulence factors, antimicrobial resistance and diagnosis. Onderstepoort J Vet Res, 87, a1869.
  • Meghdadi H, Khosravi AD, Sheikh AF, et al (2019): Isolation and characterization of Listeria Monocytogenes from environmental and clinical sources by culture and PCR-RFLP methods. Iran J Microbiol, 11, 7.
  • Nowaka J, Visnovsky SB, Pitmane AR, et al (2021): Biofilm formation by Listeria monocytogenes 15G01, a persistent isolate from a seafood-processing plant, is influenced by inactivation of multiple genes belonging to different functional groups. Food Microbiol, 87, e02349-20.
  • Osman KM, Kappell AD, Fox EM, et al (2020): Prevalence, pathogenicity, virulence, antibiotic resistance, and phylogenetic analysis of biofilm- producing Listeria monocytogenes isolated from different ecological niches in Egypt: Food, Humans, Animals, and Environment. Pathogens, 9, 5.
  • Pangallo D, Kaclíková E, Kuchta T, et al (2001): Detection of Listeria monocytogenes by polymerase chain reaction oriented to inlB gene. New Microbiol, 24, 333-339.
  • Poimenidou V, Dalmasso M, Papadimitriou K, et al (2018): Virulence gene sequencing highlights similarities and differences in sequences in Listeria monocytogenes serotype 1/2a and 4b strains of clinical and food origin from 3 different geographic locations. Front microbiol, 9, 1103.
  • Pyz-Łukasik R, Paszkiewicz W, Kiełbus M, et al (2022): Genetic diversity and potential virulence of Listeria monocytogenes isolates originating from Polish artisanal cheeses. Foods, 11, 2805.
  • Quereda JJ, Leclercq A, Moura A, et al (2020): Listeria valentina sp. nov., isolated from a water trough and the faeces of healthy sheep. Int J Syst Evol Microbiol, 70, 5868-5879.
  • Rantsiou K, Alessandria V, Urso R, et al (2008): Detection, quantification and vitality of Listeria monocytogenes in food as determined by quantitative PCR. Int J Food Microbiol, 121, 99-105.
  • Sela S, Frank S, Belausov E, et al (2006): A mutation in the luxS gene influences Listeria monocytogenes biofilm formation. Appl Environ Microbiol, 72, 5653– 5658.
  • Sharma S, Sharma V, Dahiya DK, et al (2017): Prevalence, virulence potential, and antibiotic susceptibility profile of Listeria monocytogenes isolated from bovine raw milk samples obtained from Rajasthan, India. Foodborne Pathog Dis, 14, 132-140.
  • Soni DK, Singh M, Singh DV, et al (2014): Virulence and genotypic characterization of Listeria monocytogenes isolated from vegetable and soil samples. BMC Microbiol, 14, 241.
  • 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.
  • Takeuchi K, Smith MA, Doyle MP (2003): Pathogenicity of food and clinical Listeria monocytogenes isolates in a mouse bioassay. J Food Prot, 66, 2362–2366.
  • Warke SR, Ingle VC, Kurkure NV, et al (2017): Biofilm formation and associated genes in Listeria monocytogenes. IJVSBT, 12, 7-12.
  • Wu S, Wu Q, Zhang J, et al (2015): Listeria monocytogenes prevalence and characteristics in retail raw foods in China. PLo S One, 10, e0136682.
  • Zhou X, Jiao X (2005): Polymerase chain reaction detection of Listeria monocytogenes using oligonucleotide primers targeting actA gene. Food Control, 16, 125–130.
There are 49 citations in total.

Details

Primary Language English
Subjects Veterinary Bacteriology
Journal Section Research Article
Authors

Ahmet Murat Saytekin 0000-0001-7486-8054

Adem Adıgüzel 0000-0002-7763-0882

Khaled Alkilani 0000-0003-0641-1380

Ayfer Güllü Yücetepe 0000-0002-9842-3305

Oktay Keskin 0000-0002-5977-7872

Project Number 20128 ve 20021
Publication Date
Submission Date March 12, 2024
Acceptance Date July 16, 2024
Published in Issue Year 2025Volume: 72 Issue: 1

Cite

APA Saytekin, A. M., Adıgüzel, A., Alkilani, K., Güllü Yücetepe, A., et al. (n.d.). Some virulence genes and biofilm formation capabilities of Listeria monocytogenes isolates from different sources. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 72(1), 35-45. https://doi.org/10.33988/auvfd.1450034
AMA Saytekin AM, Adıgüzel A, Alkilani K, Güllü Yücetepe A, Keskin O. Some virulence genes and biofilm formation capabilities of Listeria monocytogenes isolates from different sources. Ankara Univ Vet Fak Derg. 72(1):35-45. doi:10.33988/auvfd.1450034
Chicago Saytekin, Ahmet Murat, Adem Adıgüzel, Khaled Alkilani, Ayfer Güllü Yücetepe, and Oktay Keskin. “Some Virulence Genes and Biofilm Formation Capabilities of Listeria Monocytogenes Isolates from Different Sources”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 72, no. 1 n.d.: 35-45. https://doi.org/10.33988/auvfd.1450034.
EndNote Saytekin AM, Adıgüzel A, Alkilani K, Güllü Yücetepe A, Keskin O Some virulence genes and biofilm formation capabilities of Listeria monocytogenes isolates from different sources. Ankara Üniversitesi Veteriner Fakültesi Dergisi 72 1 35–45.
IEEE A. M. Saytekin, A. Adıgüzel, K. Alkilani, A. Güllü Yücetepe, and O. Keskin, “Some virulence genes and biofilm formation capabilities of Listeria monocytogenes isolates from different sources”, Ankara Univ Vet Fak Derg, vol. 72, no. 1, pp. 35–45, doi: 10.33988/auvfd.1450034.
ISNAD Saytekin, Ahmet Murat et al. “Some Virulence Genes and Biofilm Formation Capabilities of Listeria Monocytogenes Isolates from Different Sources”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 72/1 (n.d.), 35-45. https://doi.org/10.33988/auvfd.1450034.
JAMA Saytekin AM, Adıgüzel A, Alkilani K, Güllü Yücetepe A, Keskin O. Some virulence genes and biofilm formation capabilities of Listeria monocytogenes isolates from different sources. Ankara Univ Vet Fak Derg.;72:35–45.
MLA Saytekin, Ahmet Murat et al. “Some Virulence Genes and Biofilm Formation Capabilities of Listeria Monocytogenes Isolates from Different Sources”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 72, no. 1, pp. 35-45, doi:10.33988/auvfd.1450034.
Vancouver Saytekin AM, Adıgüzel A, Alkilani K, Güllü Yücetepe A, Keskin O. Some virulence genes and biofilm formation capabilities of Listeria monocytogenes isolates from different sources. Ankara Univ Vet Fak Derg. 72(1):35-4.
 Download Cover Image