Yıl: 2021 Cilt: 47 Sayı: 3 Sayfa Aralığı: 149 - 153 Metin Dili: İngilizce DOI: 10.5152/actavet.2021.21006 İndeks Tarihi: 19-01-2022

Mono- and Mixed-Species Biofilm Formation by Salmonella Infantis, Salmonella Kentucky, Enterococcus faecium, and Enterococcus faecalis

Öz:
It is crucial to understand the interactions between foodborne pathogens, as they are commonly encountered as multi-species biofilms in the food industry. Since Salmonella and Enterococcus are both found in poultry intestinal microbiota, the multi-species biofilms of these strains gain more significance. This study aimed to reveal the synergistic and antagonistic effects of mono- and mixed-species biofilms of Salmonella Infantis, Salmonella Kentucky, Enterococcus faecium, and Enterococcus faecalis on each other. Biofilm formation of mono- and mixed-species at different concentrations (109 , 107 , 105 , and 103cfu/mL) were determined in Tryptic Soy Broth using polystyrene microplates at room temperature (21 ± 1°C) for 48 hours. According to the optical density measured at 590 nm, S. Infantis was determined as a strong biofilm producer, and S. Kentucky and E. faecium were defined as weak biofilm producers under the conditions applied in the study. No biofilm formation was observed in E. faecalis. In addition, while S. Infantis and S. Kentucky exhibited an antagonistic effect on each other when co-incubated, a synergistic effect was seen between the S. Infantis and Enterococcus spp. This study highlights the impact of microbial interactions in mixed-species biofilm formed by foodborne pathogens, and could help in future studies on combating biofilms, especially in poultry-based food processing environments.
Anahtar Kelime:

Belge Türü: Makale Makale Türü: Araştırma Makalesi Erişim Türü: Erişime Açık
  • Açıkalın, H. D. (2017). Salmonella Infantis suşlarının oluşturduğu biyofilm üzerine çevresel ve genetic faktörlerin etkisinin araştırılması. Ankara: Yüksek Lisans Tezi, Ankara Üniversitesi Sağlık Bilimleri Enstitüsü. (Thesis)
  • Agarwal, R. K., Singh, S., Bhilegaonkar, K. N., & Singh, V. P. (2011). Optimization of microtitre plate assay for the testing of biofilm formation ability in different Salmonella serotypes. International Food Research Journal, 18(4), 1493.
  • Antunes, P., Mourão, J., Campos, J., & Peixe, L. (2016). Salmonellosis: The role of poultry meat. Clinical Microbiology and Infection, 22(2), 110–121. [CrossRef]
  • Arias, C. A., & Murray, B. E. (2012). The rise of the Enterococcus: Beyond vancomycin resistance. Nature Reviews. Microbiology, 10(4), 266–278. [CrossRef]
  • Buyukyoruk, S., Ayaz, N. D., Gencay, Y. E., Beyaz, D., & Kocak, P. (2013). Species distribution, molecular characteristics and vancomycin resistance gene profiles of Enterococcus sp. isolates from farmhouse cheeses in western Turkey. International Journal of Dairy Technology, 67(1), 103–109.
  • Ch’ng, J. H., Chong, K. K. L., Lam, L. N., Wong, J. J., & Kline, K. A. (2019). Biofilm-associated infection by enterococci. Nature Reviews. Microbiology, 17(2), 82–94. [CrossRef]
  • Chen, D., Zhao, T., & Doyle, M. P. (2015). Single- and mixed-species biofilm formation by Escherichia coli O157:H7 and Salmonella, and their sensitivity to levulinic acid plus sodium dodecyl sulfate. Food Control, 57, 48–53. [CrossRef]
  • Chen, P., Wang, J. J., Hong, B., Tan, L., Yan, J., Zhang, Z., Liu, H., Pan, Y., & Zhao, Y. (2019). Characterization of mixed-species biofilm formed by Vibrio parahaemolyticus and Listeria monocytogenes. Frontiers in Microbiology, 10, 2543. [CrossRef]
  • Cui, P., Feng, L., Zhang, L., He, J., An, T., Fu, X., Li, C., Zhao, X., Zhai, Y., Li, H., Luo, X., Lei, C., Wang, H., & Yang, X. (2020). Antimicrobial resistance, virulence genes, and biofilm formation capacity Among Enterococcus species From Yaks in Aba Tibetan autonomous prefecture, China. Frontiers in Microbiology, 11, 1250. [CrossRef]
  • Dale, J. L., Cagnazzo, J., Phan, C. Q., Barnes, A. M., & Dunny, G. M. (2015). Multiple roles for Enterococcus faecalis glycosyltransferases in biofilm-associated antibiotic resistance, cell envelope integrity, and conjugative transfer. Antimicrobial Agents and Chemotherapy, 59(7), 4094–4105. [CrossRef]
  • Da Silva Fernandes, M., Coelho Alvares, A. C., Martins Manoel, J. G., Ramires Esper, L. M., Kabuki, D. Y., & Kuaye, A. Y. (2017). Formation of multi-species biofilms by Enterococcus faecium, Enterococcus faecalis, and Bacillus cereus isolated from ricotta processing and effectiveness of chemical sanitation procedures. International Dairy Journal, 72, 23–28. [CrossRef]
  • Diker, K. S., Göncüoğlu, M., Şahin, G., Akan, M., Gürcan, İ. S., Müştak, H. K., Ayaz, N. D., Sarıçam, S., Salar, M. O., Açıkalın, H. D., Unal, G., Çöven, F., Dakman, A., Gülaçtı, I., Uzunboy, E. N., Yildirim, Ç., Kesler, K., Birinci, S. A., Sökmen, H., & Çiftci, M. M. (2020). Base study for the establishment of national Salmonella control program in hatching farms and table eggs in Turkey. Turkish Journal of Veterinary and Animal Sciences, 44(2), 343–349. [CrossRef]
  • Elexson, N., Afsah-Hejri, L., Rukayadi, Y., Soopna, P., Lee, H. Y., Tuan Zainazor, T. C., Nor Ainy, M., Nakaguchi, Y., Mitsuaki, N., & Son, R. (2014). Effect of detergents as antibacterial agents on biofilm of antibiotics-resistant Vibrio parahaemolyticus isolates. Food Control, 35(1), 378–385. [CrossRef]
  • García-Solache, M., & Rice, L. B. (2019). The Enterococcus: A model of adaptability to its environment. Clinical Microbiology Reviews, 32(2), e00058-18. [CrossRef]
  • Gkana, E. N., Giaouris, E. D., Doulgeraki, A. I., Kathariou, S., & Nychas, G. E. (2016). Biofilm formation by Salmonella Typhimurium and Staphylococcus aureus on stainless steel under either mono- or dualspecies multi-strain conditions and resistance of sessile communities to sub-lethal chemical disinfection. Food Control, 73, 838–846. [CrossRef]
  • Hall-Stoodley, L., Costerton, J. W., & Stoodley, P. (2004). Bacterial biofilms: from the natural environment to infectious diseases. Nature Reviews. Microbiology, 2(2), 95–108. [CrossRef]
  • Jahan, M., & Holley, R. A. (2014). Incidence of virulence factors in enterococci from raw and fermented meat and biofilm forming capacity at 25°C and 37°C. International Journal of Food Microbiology, 170, 65–69. [CrossRef]
  • Kasimoglu-Dogru, A., Gencay, Y. E., & Ayaz, N. D. (2010). Prevalence and antibiotic resistance profiles of Enterococcus species in chicken at slaughter level; Absence of vanA and vanB genes in E. faecalis and E. faecium. Research in Veterinary Science, 89(2), 153–158. [CrossRef]
  • Keklikoglu, N. F., Cufaoglu, G., & Ayaz, N. D. (2019). Effect of bacteriophage application on the formation and removal of Listeria monocytogenes biofilms. Journal of Veterinary Research & Animal Husbandry, 2(1), 110.
  • Kostaki, M., Chorianopoulos, N., Braxou, E., Nychas, G. J., & Giaouris, E. (2012). Differential biofilm formation and chemical disinfection resistance of sessile cells of Listeria monocytogenes strains under monospecies and dual-species (with Salmonella enterica) conditions. Applied and Environmental Microbiology, 78(8), 2586–2595. [CrossRef]
  • Landete, J. M., Peirotén, Á, Medina, M., Arqués, J. L., & RodríguezMínguez, E. (2018). Virulence and antibiotic resistance of Enterococci isolated from healthy breastfed infants. Microbial Drug Resistance, 24(1), 63–69. [CrossRef]
  • La-Rosa, S. L., Montealegre, M. C., Singh, K. V., & Murray, B. E. (2016). Enterococcus faecalis Ebp pili are important for cell-cell aggregation and intraspecies gene transfer. Microbiology, 162(5), 798–802. [CrossRef]
  • Onaran, B., Göncüoğlu, M., & Bilir Ormanci, F. S. (2019). Antibiotic resistance profiles of vancomycin resistant enterococci in chicken meat samples. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 66, 331–336. [CrossRef]
  • Stepanović, S., Ćirković, I., Mijač, V., & Švabić-Vlahović, M. (2003). Influence of the incubation temperature, atmosphere and dynamic conditions on biofilm formation by Salmonella spp. Food Microbiology, 20(3), 339–343. [CrossRef]
  • Yang, L. A., Liu, Y., Wu, H., Hóiby, N., Molin, S., & Song, Z. J. (2011). Current understanding of multi-species biofilms. International Journal of Oral Science, 3(2), 74–81. [CrossRef]
APA Çufaoğlu G, ONARAN ACAR B, Cengiz G, Ayaz N, GONCUOGLU M (2021). Mono- and Mixed-Species Biofilm Formation by Salmonella Infantis, Salmonella Kentucky, Enterococcus faecium, and Enterococcus faecalis. , 149 - 153. 10.5152/actavet.2021.21006
Chicago Çufaoğlu Gizem,ONARAN ACAR BAHAR,Cengiz Görkem,Ayaz Naim Deniz,GONCUOGLU MUAMMER Mono- and Mixed-Species Biofilm Formation by Salmonella Infantis, Salmonella Kentucky, Enterococcus faecium, and Enterococcus faecalis. (2021): 149 - 153. 10.5152/actavet.2021.21006
MLA Çufaoğlu Gizem,ONARAN ACAR BAHAR,Cengiz Görkem,Ayaz Naim Deniz,GONCUOGLU MUAMMER Mono- and Mixed-Species Biofilm Formation by Salmonella Infantis, Salmonella Kentucky, Enterococcus faecium, and Enterococcus faecalis. , 2021, ss.149 - 153. 10.5152/actavet.2021.21006
AMA Çufaoğlu G,ONARAN ACAR B,Cengiz G,Ayaz N,GONCUOGLU M Mono- and Mixed-Species Biofilm Formation by Salmonella Infantis, Salmonella Kentucky, Enterococcus faecium, and Enterococcus faecalis. . 2021; 149 - 153. 10.5152/actavet.2021.21006
Vancouver Çufaoğlu G,ONARAN ACAR B,Cengiz G,Ayaz N,GONCUOGLU M Mono- and Mixed-Species Biofilm Formation by Salmonella Infantis, Salmonella Kentucky, Enterococcus faecium, and Enterococcus faecalis. . 2021; 149 - 153. 10.5152/actavet.2021.21006
IEEE Çufaoğlu G,ONARAN ACAR B,Cengiz G,Ayaz N,GONCUOGLU M "Mono- and Mixed-Species Biofilm Formation by Salmonella Infantis, Salmonella Kentucky, Enterococcus faecium, and Enterococcus faecalis." , ss.149 - 153, 2021. 10.5152/actavet.2021.21006
ISNAD Çufaoğlu, Gizem vd. "Mono- and Mixed-Species Biofilm Formation by Salmonella Infantis, Salmonella Kentucky, Enterococcus faecium, and Enterococcus faecalis". (2021), 149-153. https://doi.org/10.5152/actavet.2021.21006
APA Çufaoğlu G, ONARAN ACAR B, Cengiz G, Ayaz N, GONCUOGLU M (2021). Mono- and Mixed-Species Biofilm Formation by Salmonella Infantis, Salmonella Kentucky, Enterococcus faecium, and Enterococcus faecalis. Acta Veterinaria Eurasia, 47(3), 149 - 153. 10.5152/actavet.2021.21006
Chicago Çufaoğlu Gizem,ONARAN ACAR BAHAR,Cengiz Görkem,Ayaz Naim Deniz,GONCUOGLU MUAMMER Mono- and Mixed-Species Biofilm Formation by Salmonella Infantis, Salmonella Kentucky, Enterococcus faecium, and Enterococcus faecalis. Acta Veterinaria Eurasia 47, no.3 (2021): 149 - 153. 10.5152/actavet.2021.21006
MLA Çufaoğlu Gizem,ONARAN ACAR BAHAR,Cengiz Görkem,Ayaz Naim Deniz,GONCUOGLU MUAMMER Mono- and Mixed-Species Biofilm Formation by Salmonella Infantis, Salmonella Kentucky, Enterococcus faecium, and Enterococcus faecalis. Acta Veterinaria Eurasia, vol.47, no.3, 2021, ss.149 - 153. 10.5152/actavet.2021.21006
AMA Çufaoğlu G,ONARAN ACAR B,Cengiz G,Ayaz N,GONCUOGLU M Mono- and Mixed-Species Biofilm Formation by Salmonella Infantis, Salmonella Kentucky, Enterococcus faecium, and Enterococcus faecalis. Acta Veterinaria Eurasia. 2021; 47(3): 149 - 153. 10.5152/actavet.2021.21006
Vancouver Çufaoğlu G,ONARAN ACAR B,Cengiz G,Ayaz N,GONCUOGLU M Mono- and Mixed-Species Biofilm Formation by Salmonella Infantis, Salmonella Kentucky, Enterococcus faecium, and Enterococcus faecalis. Acta Veterinaria Eurasia. 2021; 47(3): 149 - 153. 10.5152/actavet.2021.21006
IEEE Çufaoğlu G,ONARAN ACAR B,Cengiz G,Ayaz N,GONCUOGLU M "Mono- and Mixed-Species Biofilm Formation by Salmonella Infantis, Salmonella Kentucky, Enterococcus faecium, and Enterococcus faecalis." Acta Veterinaria Eurasia, 47, ss.149 - 153, 2021. 10.5152/actavet.2021.21006
ISNAD Çufaoğlu, Gizem vd. "Mono- and Mixed-Species Biofilm Formation by Salmonella Infantis, Salmonella Kentucky, Enterococcus faecium, and Enterococcus faecalis". Acta Veterinaria Eurasia 47/3 (2021), 149-153. https://doi.org/10.5152/actavet.2021.21006