Genetic adhesion profiles and adhesive variability of uropathogenic Escherichia coli strains

Cover Page


Cite item

Full Text

Abstract

Our study was aimed at investigating prevalence of adhesion genetic determinants among uropathogenic E. coli strains and assessing their correlation with level of specific and non-specific adhesion. E. coli bacterial cultures (n = 33) isolated from patients with urinary tract infection were examined. A phylogenetic group of strains was detected by using Clermont quadriplex-PCR method. Detection of fimbrial and afimbrial adhesin genes was carried out with end-point PCR. Level of erythrocyte-specific, non-specific hydrophobic and hydrophilic adhesion as well as biofilm formation were estimated by using standard methods. Adhesin genes were detected with the following frequencies: fimH — 75.76%, flu — 66.67%, iha — 39.40%, papC — 33.33%. Each of the genes sfaDE, upaG, afa/draBC and yqi was found with frequency 18.18%, whereas eaeA was not detected. Seven strains (21.21%) carried solely fimbrial adhesin genes, three strains (9.09%) — afimbrial adhesin genes, and twenty-one strains (63.64%) had genes of both adhesin types. Twenty-three individual adhesion genotypes were found among thirty-three UPEC strains. A combination of at least four genes were detected in 45.45% strains, among which 60% belonged to phylogroup B2. Odds ratio for adhesin gene prevalence in B2 group was calculated. It was shown that in B2 group yqi and sfaDE genes were detected by 14-fold more frequently (OR = 14.286) than in other phylogroups, and flu gene was observed at 10-fold higher rate (OR = 10.000). No correlation between such genes and level of adhesion to erythrocytes was found, whereas fimH+, papC+ and upaG+ strains had higher level of non-specific hydrophilic adhesion. It was shown that fimbrial adhesins accounted for bacterial adhesion and biofilm formation stronger than afimbrial ones. Thicker biofilm tended to form on latex catheter surface for strains with positive genetic profile for adhesin gene carriers.

About the authors

M. V. Kuznetsova

Institute of Ecology and Genetics of Microorganisms Ural Branch Russian Academy of Sciences

Author for correspondence.
Email: mar@iegm.ru
ORCID iD: 0000-0001-9625-1151

Marina V. Kuznetsova - PhD, MD (Medicine), Leading Researcher, Laboratory of Molecular Microbiology and Biotechnology, Institute of Ecology and Genetics of Microorganisms Ural Branch Russian Academy of Sciences.

614081, Perm, Goleva str., 13.

Phone: +7 912 983-78-35 (mobile)

Russian Federation

J. S. Gizatullina

Institute of Ecology and Genetics of Microorganisms Ural Branch Russian Academy of Sciences

Email: gizatullina.julia@yandex.ru
ORCID iD: 0000-0001-9625-1151

PhD Student, Laboratory of Molecular Microbiology and Biotechnology, Institute of Ecology and Genetics of Microorganisms Ural Branch Russian Academy of Sciences.

Perm.

Russian Federation

References

  1. Брилис В.И., Брилен Т.А., Ленцнер Х.П. Методика изучения адгезивного процесса микроорганизмов // Лабораторное дело. 1986. № 4. С. 210—212.
  2. Бухарин О.В., Гриценко В.А., Вялкова А.А. Факторы уропатогенности бактерий: роль в патогенезе и значение в диагностике пиелонефрита // Нефрология и диализ. 2001. T. 3, № 4. С. 469—475.
  3. Жабченко И.А. Уропатогенные штаммы Escherichia coli: особенности функционирования, факторы вирулентности, значение в клинической практике // Таврический медико-биологический вестник. 2013. T. 16, № 2. С. 201—206.
  4. Николаев Ю.А. Регуляция адгезии у бактерий Pseudomonas fluorescens под влиянием дистантных межклеточных взаимодействий // Микробиология. 2000. T. 69, № 3. C. 356—361.
  5. Abe C.M., Salvador F.A., Falsetti I.N., Vieira M.A.M., Blanco J., Blanco J.E. Uropathogenic Escherichia coli (UPEC) strains may carry virulence properties of diarrhoeagenic E. coli. FEMS Immunol. Med. Microbiol., 2008, vol. 52, pp. 397—406. doi: 10.1111/j.1574-695X.2008.00388.x
  6. Allsopp L.P., Beloin C., Ulett G.C., Valle J., Totsika M., Sherlock O., Ghigo J.M., Schembri M.A. Molecular characterization of UpaB and UpaC, two new autotransporter proteins of uropathogenic Escherichia coli CFT073. Infect. Immun., 2012, vol. 80, pp. 321-332. doi: 10.1128/IAI.05322-11
  7. Antao E.M., Ewers C., Gurlebeck D., Preisinger R., Homeier T., Li G., Wieler L.H. Signature-tagged mutagenesis in a chicken infection model leads to the identification of a novel avian pathogenic Escherichia coli fimbrial adhesin. PLoS One, 2009, vol. 4, no. 11: e7796. doi: 10.1371/journal.pone.0007796
  8. Asadi S., Kargar M., Solhjoo K., Najafi A., Ghorbani-Dalini S. The association of virulence determinants of uropathogenic Escherichia coli with antibiotic resistance, Jundishapur. J. Microbiol., 2014, vol. 7, no. 5: e9936. doi: 10.5812/jjm.9936
  9. Bahrani-Mougeot F.K., Buckles E.L., Lockatell C.V., Hebel J.R., Johnson D.E., Tang C.M. Type 1 fimbriae and extracellular polysaccharides are preeminent uropathogenic Escherichia coli virulence determinants in the murine urinary tract. Mol. Microbiol., 2002, vol. 45, no. 4, pp. 1079-1093. doi: 10.1046/j.1365-2958.2002.03078.x
  10. Bashir S., Haque A., Sarwar Y., Ali A., Anwar M.I. Virulence profile of different phylogenetic groups of locally isolated community acquired uropathogenic E. coli from Faisalabad region of Pakistan. Ann. Clin. Microbiol. Antimicrob., 2012, vol. 11: 23. doi: 10.1186/1476-0711-11-23
  11. Chakraborty A., Adhikari P., Shenoy S., Saralaya V. Molecular characterization of uropathogenic Escherichia coli isolates at a tertiary care hospital in South India. Ind. J. Med. Microbiol., 2017, vol. 35, pp. 305-310. doi: 10.4103/ijmm.IJMM_14_291
  12. Chapman T.A., Wu X.Y., Barchia I., Bettelheim K.A., Driesen S., Trott D., Wilson M., Chin J.J. Comparison of virulence gene profiles of Escherichia coli strains isolated from healthy and diarrheic swine. Appl. Environ. Microbiol., 2006, vol. 72, no. 7, pp. 4782-4795. doi: 10.1128/AEM.02885-05
  13. Dadi B.R., Abebe T., Zhang L., Mihret A., Abebe W., Amogne W. Distribution of virulence genes and phylogenetics of uropatho-genic Escherichia coli among urinary tract infection patients in Addis Ababa, Ethiopia. BMC Infect. Dis., 2020, vol. 20, no. 108. doi: 10.1186/s12879-020-4844-z
  14. Fattahi S., Kafil H.S., Nahai M.R., Asgharzadeh M., Nori R., Aghazadeh M. Relationship of biofilm formation and different virulence genes in uropathogenic Escherichia coli isolates from Northwest Iran. GMS Hyg. Infect. Control., 2015, vol. 10: doc11. doi: 10.3205/dgkh000254
  15. Flores-Mireles A.L., Walker J.N., Caparon M., Hultgren S.J. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat. Rev. Microbiol., 2015, vol. 13, no. 5, pp. 269-284. doi: 10.1038/nrmicro3432
  16. Guiral E., Bosch J., Vila J., Soto S.M. Prevalence of Escherichia coli among samples collected from the genital tract in pregnant and non-pregnant women: relationship with virulence. FEMS Microbiol. Lett., 2011, vol. 314, pp. 170-173. doi: 10.1111/j.1574-6968.2010.02160.x
  17. Johnson J.R. Virulence factors in Escherichia coli urinary tract infection. Clin. Microbiol. Rev., 1991, vol. 4, no. 1, pp. 80-128. doi: 10.1128/cmr.4.1.80
  18. Johnson J.R., Russo T.A. Extraintestinal pathogenic Escherichia coli (ExPEC): the “other bad E. coli”. J. Lab. Clin. Med., 2002, vol. 139, pp. 155-162. doi: 10.1067/mlc.2002.121550
  19. Johnson J.R., Stell A.L. Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J. Infect. Dis., 2000, vol. 181, no. 1, pp. 261-272. doi: 10.1086/315217
  20. Jones B.W. Glial cells missing: a genetic switch that controls glial versus neuronal fate. Cell, 1995, vol. 82, no. 6, pp. 1013-1023. doi: 10.1016/0092-8674(95)90280-5
  21. Khairy R.M., Mohamed E.S., Abdel Ghany H.M., Abdelrahim S.S. Phylogenic classification and virulence genes profiles of uropathogenic E. coli and diarrhegenic E. coli strains isolated from community acquired infections. PLoS One, 2019, vol. 14, no. 9: e0222441. doi: 10.1371/journal.pone.0222441
  22. Le Bouguenec C. Adhesins and invasins of pathogenic Escherichia coli. Int. J. Med. Microbiol., 2005, vol. 295, no. 6-7, pp. 471478. doi: 10.1016/j.ijmm.2005.07.001
  23. Le Bouguenec C., Archambaud M., Labigne A. Rapid and specific detection of the pap, afa, and sfa adhesin-encoding operons in uropathogenic Escherichia coli strains by polymerase chain reaction. J. Clin. Microbiol., 1992, vol. 30, pp. 1189 -1193.
  24. Melican K., Sandoval R.M., Kader A., Josefsson L., Tanner G.A., Molitoris B.A., Richter-Dahlfors A. Uropathogenic Escherichia coli P and Type 1 fimbriae act in synergy in a living host to facilitate renal colonization leading to nephron obstruction. PLoS Pathog., 2011, vol. 7, no. 2: e1001298. doi: 10.1371/journal.ppat.1001298
  25. Merritt J.H., Kadouri D.E., O'Toole G.A. Growing and analyzing static biofilm. Curr. Protoc. Microbiol., 2005, chapter 1, unit 1: 1B.1. doi: 10.1002/9780471729259.mc01b01s00
  26. Morales-Espinosa R., Hernandez-Castro R., Delgado G., Mendez J.L., Navarro A., Manjarrez A., Cravioto A. UPEC strain characterization isolated from Mexican patients with recurrent urinary infections. J. Infect. Develop. Count., 2016, vol. 10, no. 4, pp. 317-328. doi: 10.3855/jidc.6652
  27. Mulvey M.A. Adhesion and entry of uropathogenic Escherichia coli. Cell Microbiol., 2002, vol. 4, no. 5, pp. 257-271. doi: 10.1046/j.1462-5822.2002.00193.x
  28. Najafi A., Hasanpour M., Askary A., Aziemzadeh M., Hashemi N. Distribution of pathogenicity island markers and virulence factors in new phylogenetic groups of uropathogenic Escherichia coli isolates. Folia Microbiol., 2017, vol. 63, no. 3, pp. 335-343. doi: 10.1007/s12223-017-0570-3
  29. Naves P., del Prado G., Huelves L., Gracia M., Ruiz V., Blanco J., Dahbi G., Blanco M., del Carmen Ponte M., Soriano F. Correlation between virulence factors and in vitro biofilm formation by Escherichia coli strains. Microb. Pathog., 2008, vol. 45, no. 2, pp. 86-91. doi: 10.1016/j.micpath.2008.03.003
  30. O'Hara R.W., Jenks P.J., Emery M., Upton M. Rapid detection of extra-intestinal pathogenic Escherichia coli multi-locus sequence type 127 using a specific PCR assay. J. Med. Microbiol., 2018, vol. 68, no. 2, pp. 188-196. doi: 10.1099/jmm.0.000902
  31. Rasha M.K., Ebtisam S.M., Hend M.A.G., Soha S.A. Phylogenic classification and virulence genes profiles of uropathogenic E. coli and diarrhegenic E. coli strains isolated from community acquired infections. PLoS One, 2019, vol. 14, no. 9: e0222441. doi: 10.1371/journal.pone.0222441
  32. Sheikh A.F., Goodarzi H., Yadyad M.J., Amin S.A.M., Jomehzadeh N., Ranjbar R., Moradzadeh M., Azarpira S., Akhond M.R., Hashemzadeh M. Virulence-associated genes and drug susceptibility patterns of uropathogenic Escherichia coli isolated from patients with urinary tract infection. Infect. Drug Resist., 2019, vol. 12, pp. 2039-2047. doi: 10.2147/IDR.S199764
  33. Spindola M.G., Cunha M.P.V., Moreno L.Z., Amigo C.R., Silva A.P.S., Parra B.M., Poor A.P., de Oliveira C.H., Perez B.P., Knobl T., Moreno A.M. Genetic diversity, virulence genotype and antimicrobial resistance of uropathogenic Escherichia coli (UPEC) isolated from sows. Veter. Quart., 2018, vol. 38, no. 1, pp. 79-87. doi: 10.1080/01652176.2018.1519321
  34. Szemiako K., Krawczyk B., Samet A., Sledzinska A., Nowicki B., Nowicki S., Kur J. A subset of two adherence systems, acute pro-inflammatory pap genes and invasion coding dra, fim or sfa, increases the risk of Escherichia coli translocation to the bloodstream. Eur. J. Clin. Microbiol. Infect. Dis., 2013, vol. 32, pp. 1579-1582. doi: 10.1007/s10096-013-1913-x
  35. Terlizzi M.E., Gribaudo G., Maffei M.E. Uropathogenic Escherichia coli (UPEC) infections: virulence factors, bladder responses, antibiotic, and non-antibiotic antimicrobial strategies. Front. Microbiol., 2017, vol. 8: 1566. doi: 10.3389/fmicb.2017.01566
  36. Tiba M.R., Yano T., Leite Dda S. Genotypic characterization of virulence factors in Escherichia coli strains from patients with cystitis. Rev. Inst. Med. Trop. Sao Paulo, 2008, vol. 50, no. 5, pp. 255-260. doi: 10.1590/s0036-46652008000500001
  37. Ulett G.C., Valle J., Beloin C., Sherlock O., Ghigo J.M., Schembri M.A. Functional analysis of antigen 43 in uropathogenic Escherichia coli reveals a role in long-term persistence in the urinary tract. Infect. Immun., 2007, vol. 75, no. 7, pp. 3233-3244. doi: 10.1128/IAI.01952-06
  38. Valle J., Mabbett A.N., Ulett G.C., Toledo-Arana A., Wecker K., Totsika M., Schembri M.A., Ghigo J.M., Beloin C. UpaG, a new member of the trimeric autotransporter family of adhesins in uropathogenic Escherichia coli. J. Bacteriol., 2008, vol. 190, pp. 4147-4161. doi: 10.1128/JB.00122-08
  39. Wiles T.J., Kulesus R.R., Mulvey M.A. Origins and virulence mechanisms of uropathogenic Escherichia coli. Exp. Mol. Pathol., 2008, vol. 85, no. 1, pp. 11-19. doi: 10.1016/j.yexmp.2008.03.007
  40. Yahiaoui M., Robin F., Bakour R., Hamidi M., Bonnet R., Messai Y. Antibiotic resistance, virulence, and genetic background of community-acquired uropathogenic Escherichia coli from Algeria. Microb. Drug. Resist., 2015, vol. 21, pp. 516-526. doi: 10.1089/mdr.2015.0045
  41. Yun K.W., Kim H.Y., Park H.K., Kim W., Lim I.S. Virulence factors of uropathogenic Escherichia coli of urinary tract infections and asymptomatic bacteriuria in children. J. Microbiol. Immunol. Infect., 2014, vol. 47, no. 6, pp. 455-461. doi: 10.1016/j.jmii.2013.07.010
  42. Zhao L., Gao S., Huan H., Xu X., Zhu X., Yang W., Gao Q., Lui X. Comparison of virulence factors and expression of specific genes between uropathogenic Escherichia coli and avian pathogenic E. coli in a murine urinary tract infection model and a chicken challenge model. Microbiol., 2009, vol. 155, pp. 1634-1644. doi: 10.1099/mic.0.024869-0

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2020 Kuznetsova M.V., Gizatullina J.S.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 64788 от 02.02.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies