ISIRGAN OTU (URTICA DIOICA) SULU EKSTRAKTININ SALMONELLA ENTERICA SEROVARLARININ BİYOFİLM OLUŞUMU ÜZERİNE ANTİMİKROBİYEL ETKİSİNİN BELİRLENMESİ

Year 2021, Volume: 46 Issue: 2, 324 - 338, 23.03.2021

Aylin Cesur Yeşim Soyer

https://doi.org/10.15237/gida.GD21016

Cited By: 2

Abstract

Salmonella gibi gıda kaynaklı patojenlerde antimikrobiyel direncin artması yol açacağı sağlık problemleri nedeniyle endişelendirmektedir. Bu bağlamda, bitki özleri bilinen antimikrobiyellere önemli doğal alternatifler haline gelmiştir. Suda çözünür ısırgan otu ekstraktlarının 2 mg/mL, 4 mg/mL, 6 mg/mL, 8 mg/mL, 12 mg/mL, 16 mg/mL ve 20 mg/mL konsantrasyonları ile eradikasyon etkisi, Newport, Typhimurium, Enteritidis, Virchow, Othmarschen ve Mikawasima dahil olmak üzere Salmonella enterica alt türü enterica serovarlarının önceden oluşturulmuş biyofilmleri ve yüzme hareketliliği in vitro olarak araştırılmıştır. Her serovar ile bulaştırılan ıspanakta, izolatların oluşturduğu biyofilm oluşumunun engellenmesi için 40 mg/mL konsantre ekstraktın etkin olduğu tespit edilmiştir. Ayrıca, biyofilm oluşumundan sorumlu ana genler (yani rpoS, mlrA, ycfR, fimA, spiA ve csgA) bahsi geçen tüm izolatlarda taranmıştır. Buna ilave olarak, ekstrakt, Mikawasima ve Virchow serovarlarının yüzme hareketlerini önemli ölçüde azalttığı belirlenmiştir. En yüksek azalma sırasıyla in vitro ve ıspanakta 0.88 Log CFU/mL ve 2.00 Log CFU/cm2 olarak bulunmuştur.

Keywords

Salmonella, Isırgan otu, Antimikrobiyel etki, Biyofilm, yüzme hareketliliği

DETERMINATION OF ANTIMICROBIAL EFFECT OF THE AQUEOUS EXTRACT OF STINGING NETTLE (URTICA DIOICA) ON BIOFILM FORMATION OF SALMONELLA ENTERICA SEROVARS

Abstract

Due to health concerns associated with the increase of antimicrobial resistance in foodborne pathogens such as Salmonella, plant extracts have become important natural alternatives to known antimicrobials. The eradication effect of the water-soluble stinging nettle extracts with 2 mg/mL, 4 mg/mL, 6 mg/mL, 8 mg/mL, 12 mg/mL, 16 mg/mL, and 20 mg/mL concentrations, on pre-formed biofilms and swimming motility of Salmonella enterica subspecies enterica serovars, including Newport, Typhimurium, Enteritidis, Virchow, Othmarschen and Mikawasima, was investigated in vitro. Degradation of biofilm formation on spinach inoculated with each serovar was ascertained within different exposure time of 40 mg/mL concentrated extract as well. Moreover, major genes responsible for biofilm formation (i.e., rpoS, mlrA, ycfR, fimA, spiA and csgA) were screened in these isolates. The extract significantly decreased swimming motilities of Mikawasima and Virchow serovars. The highest reductions were found as 0.88 Log CFU/mL and 2.00 Log CFU/cm2 in vitro and on spinach, respectively.

Keywords

Antimicrobial effect,, Salmonella, Biofilm, Stinging Nettle, swimming motility

References

• Acar, S., Bulut, E., Durul, B., Uner, I., Kur, M., Avsaroglu, M.D., Kirmaci, H.A., Tel, Y.O., Zeyrek F.Y., Soyer, Y. (2017). Phenotyping and genetic characterization of Salmonella enterica isolates from Turkey revealing arise of different features specific to geography. Int J Food Microbiol, 241: 98-107. https://doi.org/10.1016/j.ijfoodmicro.2016.09.031.
• Amaral, V.C.S., Santos, P.R., da Silva, A.F., dos Santos, A.R., Machinski, J.M., Mikcha, J.M.G. (2015). Effect of carvacrol and thymol on Salmonella spp. biofilms on polypropylene. Int J Food Sci Tech, 50: 2639-2643. https://doi.org/10.1111/ijfs.12934.
• Arnqvist, A., Olsén, A., Normark, S. (1994). Sigma S-dependent growth-phase induction of the csgBA promoter in Escherichia coli can be achieved in vivo by sigma 70 in the absence of the nucleoid-associated protein H-NS. Mol Microbiol, 13: 1021-1032. https://doi.org/10.1111/j.1365-2958.1994.tb00493.x.
• Arteaga, V., Lamas, A., Regal, P., Vázquez, B., Miranda Cepeda, J.M.A., Franco, C.M. (2019). Antimicrobial activity of apitoxin from Apis mellifera in Salmonella enterica strains isolated from poultry and its effects on motility, biofilm formation and gene expression. Microb Pathog, 137: 103771. https://doi.org/10.1016/j.micpath.2019.103771.
• Barnhart, M.M., Chapman, M.R. (2006). Curli Biogenesis and Function. Annu Rev Microbiol, 60: 131–147. https://doi.org/10.1146/annurev.micro.60.080805.142106.
• Brown, P.K., Dozois, C.M., Nickerson, C.A., Zuppardo, A., Terlonge, J., Curtiss, R. (2001). MlrA, a novel regulator of curli (AgF) and extracellular matrix synthesis by Escherichia coli and Salmonella enterica serovar Typhimurium. Mol Microbiol, 41: 349–363. https://doi.org/10.1046/j.1365-2958.2001.02529.x.
• Callejón, R.M., Rodríguez-Naranjo, M.I., Ubeda, C., Hornedo-Ortega, R., Garcia-Parrilla, M.C., Troncoso, A.M. (2015). Reported foodborne outbreaks due to fresh produce in the United States and European Union: trends and causes. Foodborne Pathog Dis, 12: 32-38. https://doi.org/10.1089/fpd.2014.1821.
• Carter, M.Q., Brandl, M.T. (2015). Biofilms in fresh vegetables and fruits. In: Biofilms in the food environment, Pometto III, A. L., Demirci, A. (ed.), WILEY Blackwell, Malaysia, pp. 176-204.
• Chen, C.Y., Eckmann, L., Libby, S.J., Fang, F.C., Okamoto, S., Kagnoff, M.F., Fierer, J., Guiney, V. (1996). Expression of Salmonella typhimurium rpoS and rpoS-dependent genes in the intracellular environment of eukaryotic cells. Infect Immun, 64: 4739-4743.
• Chen, C.Y., Hofmann, C.S., Cottrell, B.J., Strobaugh, T.P.J., Paoli, G.C., Nguyen, L.H., Yan X., Uhlich, G.A. (2013). Phenotypic and genotypic characterization of biofilm forming capabilities in non-O157 Shiga toxin-producing Escherichia coli strains. PLoS One, 8: e84863. https://doi.org/10.1371/journal.pone.0084863.
• Christensen, G.D., Simpson, W.A., Younger, J.J., Baddour, L.M., Barrett, F.F., Melton D.M., Beachey, E.H. (1985). Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol, 22: 996-1006.
• Cohen, H.J., Mechanda S.M., Lin, W. (1996). PCR amplification of the fimA gene sequence of Salmonella typhimurium, a specific method for detection of Salmonella spp. Appl Environ Microbiol, 62: 4303–4308.
• Cui, H., Ma, C., Lin, L. (2016). Synergetic antibacterial efficacy of cold nitrogen plasma and clove oil against Escherichia coli O157: H7 biofilms on lettuce. Food Control, 66: 8–16. https://doi.org/10.1016/j.foodcont.2016.01.035.
• Dar, S.A., Ganai, F.A., Yousuf, A.R., Balkhi, M.U., Bhat, T.M., Sharma, P. (2013). Pharmacological and toxicological evaluation of Urtica dioica. Pharm Biol, 51: 170-180. https://doi.org/10.3109/13880209.2012.715172.
• Deditius, J.A., Felgner, S., Spöring, I., Kühne, C., Frahm, M., Rohde, M., Weiß, S., Erhardt, M. (2015). Characterization of novel factors involved in swimming and swarming motility in Salmonella enterica serovar typhimurium. PLoS One, 10: e0135351. https://doi.org/10.1371/journal.pone.0135351.
• Dong, H., Peng, D., Jiao, X., Zhang, X., Geng, S., Liu, X. (2011). Roles of the spiA gene from Salmonella enteritidis in biofilm formation and virulence. Microbiology, 157: 1798-1805. https://doi.org/10.1099/mic.0.046185-0.
• Doulgeraki, A.I., Papaioannou M., Nychas, G.J.E. (2016). Targeted gene expression study of Salmonella enterica during biofilm formation on rocket leaves. LWT-Food Sci Technol, 65: 254-260. https://doi.org/10.1016/j.lwt.2015.08.017.
• European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC). (2013). Unusual increase of Salmonella Mikawasima infections in humans. EFSA Supporting Publications. 10: 512E. https://doi.org/10.2903/sp.efsa.2013.EN-512.
• Faour-Klingbeil, D., Todd, E.C.D. (2018). A review on the rising prevalence of international standards: threats or opportunities for the agri-food produce sector in developing countries, with a focus on examples from the MENA region. Foods, 7: 33. https://doi.org/10.3390/foods7030033.
• Gülçin, I., Küfrevioǧlu, Ö.I., Oktay, M., Büyükokuroǧlu, M.E. (2004). Antioxidant, antimicrobial, antiulcer and analgesic activities of nettle (Urtica dioica L.). J Ethnopharmacol, 90: 205-215. https://doi.org/10.1016/j.jep.2003.09.028.
• Gunel, E., Polat Kilic, G., Bulut, E., Durul, B., Acar, S., Alpas, H., Soyer, Y. (2015). Salmonella surveillance on fresh produce in retail in Turkey. Int J Food Microbiol, 199: 72-77. https://doi.org/10.1016/j.ijfoodmicro.2015.01.010.
• Gupta, P.D., Birdi, T.J. (2017). Development of botanicals to combat antibiotic resistance. J Ayurveda Integr Med, 8: 266-275. https://doi.org/10.1016/j.jaim.2017.05.004.
• Han, D., Hung, Y.C., Bratcher, C.L., Monu, E.A., Wang, Y., Wang, L. (2018). Formation of sublethally injured Yersinia enterocolitica, Escherichia coli O157:H7, and Salmonella enterica serovar Enteritidis cells after neutral electrolyzed oxidizing water treatments. Appl Environ Microbiol, https://doi.org/10.1128/AEM.01066-18.
• Hattermann, D.R., Ries, S.M. (1989). Motility of Pseudomonas syringae pv. glycinea and its role in infection. Phytopathology, 79: 284-289.
• Heaton, J.C., Jones, K. (2008). Microbial contamination of fruit and vegetables and the behaviour of enteropathogens in the phyllosphere: A review. J Appl Microbiol, 104: 613-626. https://doi.org/10.1111/j.1365-2672.2007.03587.x.
• Kim, S., Choi, Y.G., Eom, J.W., Oh, T.J., Lee, K.S., Kim, S.H., Lee, E.T., Park, M.S., Oh H.B., Lee, B.K. (2007). An outbreak of Salmonella enterica serovar Othmarschen at a funeral service in Guri-si, South Korea. Jpn J Infect Dis, 60: 412-413.
• Koehn, F.E., Carter, G.T. (2005). The evolving role of natural products in drug discovery. Nat Rev Drug Discov, 4: 206-220. https://doi.org/10.1038/nrd1657.
• Ledeboer, N.A., Frye, J.G., McClelland, M., Jones, B.D. (2006). Salmonella enterica serovar Typhimurium requires the Lpf, Pef, and Tafi fimbriae for biofilm formation on HEp-2 tissue culture cells and chicken intestinal epithelium. Infect Immun, 74: 3156-3169. https://doi.org/10.1128/IAI.01428-05.
• Lianou, A., Koutsoumanis, K.P. (2012). Strain variability of the biofilm-forming ability of Salmonella enterica under various environmental conditions. Int J Food Microbiol, 160: 171-178. https://doi.org/10.1016/j.ijfoodmicro.2012.10.002.
• Lu, L., Hu, W., Tian, Z., Yuan, D., Yi, G., Zhou, Y., Cheng, Q., Zhu, J., Li, M. (2019). Developing natural products as potential anti-biofilm agents. Chin Med, 14: 11. https://doi.org/10.1186/s13020-019-0232-2.
• Lu, Y., Dong, H., Chen, S., Chen, Y., Peng, D., Liu, X. (2011). Characterization of biofilm formation by Salmonella enterica serovar Pullorum strains. Afr J Microbiol Res. https://doi.org/10.5897/AJMR11.035.
• Lu, Y., Chen, S., Dong, H., Sun, H., Peng, D., Liu, X. (2012). Identification of genes responsible for biofilm formation or virulence in Salmonella enterica serovar Pullorum. Avian Dis, 56: 134-143. https://doi.org/10.1637/9806-052411-Reg.1.
• Marin, C., Hernandiz, A., Lainez, M. (2009). Biofilm development capacity of Salmonella strains isolated in poultry risk factors and their resistance against disinfectants. Poult Sci, 88: 424-431. https://doi.org/10.3382/ps.2008-00241.
• Mohan, R., Benton, M., Dangelmaier, E., Fu, Z., Sekhar, A.C. (2018). Quorum sensing and biofilm formation in pathogenic and mutualistic plant-bacterial interactions. In: Implication of quorum sensing system in biofilm formation and virulence, Bramhachari, P. V. (ed), Springer, Singapore, pp. 135-137.
• Myšková, P., Karpíšková, R., Dědičová, D. (2013). Salmonellosis outbreaks in the Czech Republic in 2012. Epidemiol Mikrobiol Imunol, 62: 59-63.
• Patel, J., Sharma, M. (2010). Differences in attachment of Salmonella enterica serovars to cabbage and lettuce leaves. Int J Food Microbiol, 139: 41-47. https://doi.org/10.1016/j.ijfoodmicro.2010.02.005.
• Patel, J., Singh, M., Macarisin, D., Sharma, M., Shelton, D. (2013). Differences in biofilm formation of produce and poultry Salmonella enterica isolates and their persistence on spinach plants. Food Microbiol, 36: 388-394. https://doi.org/10.1016/j.fm.2013.06.019.
• Polo, F., Figueras, M.J., Inza, I., Sala, J., Fleisher, J.M., Guarro, J. (1999). Prevalence of Salmonella serotypes in environmental waters and their relationships with indicator organisms. Anton Leeuw Int J G, 75: 285–292.
• Pyatkovskyy, T., Shynkaryk, M., Yousef, A., Sastry, S.K. (2017). Fresh produce sanitization by combination of gaseous ozone and liquid sanitizer. J Food Eng, 75: 285-292. https://doi.org/10.1016/j.jfoodeng.2017.03.031.
• Römling, U., Bian, Z., Hammar, M., Sierralta, W.D., Normark, S. (1998). Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol, 180: 722-731.
• Sadekuzzaman, M., Mizan, M.F.R., Kim, H.S., Yang, S., Ha, S.D. (2018). Activity of thyme and tea tree essential oils against selected foodborne pathogens in biofilms on abiotic surfaces. LWT-Food Sci Technol, 89: 134-139. https://doi.org/10.1016/j.lwt.2017.10.042.
• Salazar, J.K., Deng, K., Tortorello, M.L., Brandl, M.T., Wang, H., Zhang, W. (2013). Genes ycfR, sirA and yigG contribute to the surface attachment of Salmonella enterica Typhimurium and Saintpaul to fresh produce. PLoS ONE, 8: e57272. https://doi.org/10.1371/journal.pone.0057272.
• Sperandio, V., Torres, A.G., Jarvis, B., Nataro, J.P., Kaper, J.B. (2003). Bacteria-host communication: the language of hormones. Proc Natl Acad Sci USA, 100: 8951-8956. https://doi.org/10.1073/pnas.1537100100.
• Steenackers, H., Hermans, K., Vanderleyden, J., De Keersmaecker, S.C.J. (2012). Salmonella biofilms: An overview on occurrence, structure, regulation and eradication. Food Res Int, 45: 502-531. https://doi.org/10.1016/j.foodres.2011.01.038.
• Stepanović, S., Ćirković, I., Ranin, L., Švabić-Vlahović, M. (2004). Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Lett Appl Microbiol, 38: 428–432. https://doi.org/10.1111/j.1472-765X.2004.01513.x.
• Synnott, M., Morse, D.L., Maguire, H., Majid, F., Plummer, M., Leicester, M., Threlfall, E.J., Cowden, J. (1993). An outbreak of Salmonella mikawasima associated with doner kebabs. Epidemiol Infect, 111: 473-481. https://doi.org/10.1017/s0950268800057204.
• Uhlich, G.A., Chen, C.Y., Cottrell, B.J., Hofmann, C.S., Dudley, E.G., Strobaugh, T.P., Nguyen, L.H. (2013). Phage insertion in mlrA and variations in rpoS limit curli expression and biofilm formation in Escherichia coli serotype O157 : H7. Microbiology, 159: 1586-1596. https://doi.org/10.1099/mic.0.066118-0.
• Wang, S., Phillippy, A.M., Deng, K., Rui, X., Li, Z., Lou Tortorello M., Zhang, W. (2010). Transcriptomic responses of Salmonella enterica serovars Enteritidis and Typhimurium to chlorine-based oxidative stress. Appl Environ Microbiol, 76: 5013-5024. https://doi.org/10.1128/AEM.00823-10.
• Wojnicz, D., Kucharska, A.Z., Sokół-Łętowska, A., Kicia M., Tichaczek-Goska, D. (2012). Medicinal plants extracts affect virulence factors expression and biofilm formation by the uropathogenic Escherichia coli. Urol Res, 40: 683–697. https://doi.org/10.1007/s00240-012-0499-6.
• Wolska, J., Janda, K., Szkyrpan, S., Gutowska, I. (2015). The influence of stinging nettle (Urtica dioica L.) extracts on the activity of catalase in THP1 monocytes/macrophages. Pomeranian J Life Sci, 61: 315–318.
• Yaron, S., Römling, U. (2014). Biofilm formation by enteric pathogens and its role in plant colonization and persistence. Microb Biotechnol, 7: 496–516. https://doi.org/10.1111/1751-7915.12186.
• Zeiner, S.A., Dwyer, B.E., 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. https://doi.org/10.1128/IAI.00331-12.