The importance of pathogenicity factors of some Streptococcus spp. and Klebsiella spp. in determining their etiological role in the inflammatory processes of the respiratory tract

Cover Page


Cite item

Full Text

Abstract

Together with the known pathogens of inflammatory processes of the respiratory tract in clinical practice are often found representatives of Streptococcus and Klebsiella, previously considered commensals of the mucous membranes of the upper respiratory tract. The exchange of genetic information facilitates the transfer of virulence factors between strains not only within the species but also within the genus. In such cases, the acquisition of virulence genes by nonpathogenic species from representatives of pathogenic species contributes to the manifestation of previously not typical properties. Therefore, the aim of the research was to study the virulence of opportunistic Streptococcus spp. and Klebsiella spp. in inflammatory processes of the respiratory tract and substantiate their etiological role in the development of the disease. We studied 220 strains of Streptococcus spp. and 97 strains of Klebsiella spp., isolated from patients with inflammatory processes in the respiratory tract and from healthy individuals. Strains of Streptococcus spp. were investigated for the presence of virulence genes: sagA, lmb, fapl, ply, lytA. Strains of Klebsiella spp. were examined for the presence of virulence genes: MrkD, magA, kfu. The phenotypic marker of lmb gene expression in Streptococcus and MrkD gene in Klebsiella was the indicator of adhesion of isolated strains to buccal epithelial cells. Expression of the fapl gene was evaluated in a phenotypic biofilm formation test. In individuals with upper respiratory tract inflammation, the most common types of strepto -cocci were: S. mitis, S. anginosus, and S. oralis. Strains of these species isolated from inflammatory processes in the upper respiratory tract had 2—4 times greater adhesiveness than strains isolated from healthy individuals. Phenotypic determination of the ability to biofilm formation showed that strains of Streptococcus containing the fapl gene formed a dense biofilm in contrast to strains without the fapl gene. K. oxytoca strains isolated from people with sinusitis had mrkd, magA, and kfu virulence genes that are characteristic of K. pneumoniae strains. In phenotypic tests, it was found that the value of the adhesion index in K. oxytoca strains isolated from patients is 4 times higher than in strains of this species isolated from healthy individuals. Thus, to confirm the etiological role of an opportunistic microorganism in the development of the infectious process, it is necessary to be guided by data on the genetic and phenotypic markers of virulence of the isolated strain.

About the authors

L. A. Kraeva

St. Petersburg Pasteur Institute; Military Medical Academy named S.M. Kirov

Author for correspondence.
Email: lykraeva@yandex.ru
ORCID iD: 0000-0002-9115-3250

Lyudmila A. Kraeva - PhD, MD (Medicine), Associate Professor, Head of the Laboratory of Medical Bacteriology, St. Petersburg PI; Professor, Department of Microbiology, S.M. Kirov MMA.

197101, St. Petersburg, Mira str., 14, Phone: +7 (812) 232-94-85. Fax: +7 (812) 498-09-39 Россия

E. S. Kunilova

St. Petersburg Pasteur Institute

Email: fake@neicon.ru

Junior Researcher, Laboratory of Medical Bacteriology.

St. Petersburg

Россия

O. A. Burgasova

RUDN University

Email: fake@neicon.ru

PhD, MD (Medicine), Professor, Department of Infectious Diseases with Courses in Epidemiology and Phthisiology RUDN University.

Moscow Россия

G. N. Hamdulaeva

St. Petersburg Pasteur Institute

Email: fake@neicon.ru

Junior Researcher, Laboratory of Medical Bacteriology.

St. Petersburg

Россия

E. M. Danilova

St. Petersburg Pasteur Institute

Email: fake@neicon.ru

Pediatrician, Head of the Polyclinic Department of the Medical Center.

St. Petersburg Россия

G. I. Bespalova

North-Western State Medical University named after I.I. Mechnikov

Email: fake@neicon.ru

PhD (Biology), Associate Professor, Department of Microbiology.

St. Petersburg

Россия

References

  1. Барлетт Д.Д. Инфекции дыхательных путей: пер. с англ. М.: Бином, 2000. 192 с.
  2. Благонравова А.С., Афонин А.Н., Воробьева О.Н., Широкова И.Ю. Сравнительный анализ адгезивности микроорганизмов, выделенных от больных и с объектов внешней среды лечебно-профилактических учреждений // Медицинский альманах. 2011. № 5 (18). С. 215-218.
  3. Бургасова О.А., Краева Л.А., Петрова И.С., Келли Е.И. Случай тяжелого течения смешанной респираторно-вирусной инфекции (грипп А (H1N1) + RS-вирусная), осложненной внебольничной пневмонией, вызванной Streptococcus equi // Инфекционные болезни. 2015. Т. 13, № 1. С. 71—74.
  4. Лабораторная диагностика внебольничных пневмоний: Методические указания. М.: Федеральный центр гигиены и эпидемиологии Роспотребнадзора, 2014. 39 с.
  5. Перцева Т.А., Плеханова О.В., Дмитриченко В.В. Клинически значимые возбудители инфекций дыхательных путей: конспект врача-клинициста и микробиолога. Часть 3: Гемофила. Моракселла // Клиническая иммунология. Аллергология. Инфектология. 2007. № 6 (1). С. 15—20.
  6. Тотолян А.А., Суворов А.Н., Дмитриев А.В. Стрептококки группы В в патологии человека. СПб.: Человек, 2010. 212 с. [Totolyan A.A., Suvorov A.N., Dmitriev A.V. Group B Streptococccus in human pathology. St. Petersburg: Chelovek, 2010. 212p. (In Russ.)]
  7. Beighton D., Carr A.D., Oppenheim B.A. Identification of viridans Streptococci associated with bacteraemia in neutropenic cancer patients. J. Med. Microbiol, 1994, no. 40, pp. 202—204. doi: 10.1099/00222615-40-3-202
  8. Benton A.H., Marquart M.E. The role of pneumococcal virulence factors in ocular infectious diseases. Interdiscip. Perspect. Infect. Dis, 2018:2525173. doi: 10.1155/2018/2525173
  9. Brisse S., Fevre C., Passet V., Issenhuth-Jeanjean S., Tournebize R., Diancourt L., Grimont P. Virulent clones of Klebsiella pneumoniae: identification and evolutionary scenario based on genomic and phenotypic characterization, 2009. PLoS One, no. 4 (3): e4982. doi: 10.1371/journal.pone.0004982
  10. Brisse S., Grimont F., Grimont P.A.D. The genus Klebsiella. Prokaryotes, 2006, no. 6, pp. 159—196. doi: 10.1007/0-387-30746-x_8
  11. Caparon M.G., Stephens D.S., Olsen A., Scott J.R. Role of M protein in adherence of group A streptococci. Infect. Immun., 1991, no. 59, pp. 1811-1817.
  12. Chi F., Nolte O., Bergmann C., Ip M., Hakenbeck R. Crossing the barrier: evolution and spread of a major class of mosaic pbp2xin Streptococcus pneumoniae, S. mitis and S. oralis. Int. J. Med. Microbiol., 2007, no. 297, pp. 503-512. doi: 10.1016/j.ijmm.2007.02.009
  13. Dmitriev A., Shakleina E., Tkacikova L. Genetic heterogeneity of the pathogenic potentials of human and bovine group B Streptococci. Folia Microbiol., 2002, vol. 47, pp. 291-295. doi: 10.1007/bf02817655
  14. Douglas C.W., Heath J., Hampton K.K., Preston F.E. Identity of viridans streptococci isolated from cases of infective endocarditis. J. Med. Microbiol, 1993, no. 39, pp. 179-182. doi: 10.1099/00222615-39-3-179
  15. Facklam R. What happened to the streptococci: overview of taxonomic and nomenclature changes. Clin. Microbiol. Rev., 2002, no. 15, pp. 613-630. doi: 10.1128/CMR.15.4.613-630.2002
  16. Franken C., Haase G., Brandt C. Horizontal gene transfer and host specificity of beta-haemolytic streptococci: the role of a putative composite transposon containing scpB and lmb. Mol. Microbiol., 2001, vol. 41, pp. 925-935. doi: 10.1046/j.1365-2958.2001.02563.x
  17. Havarstein L.S., Gaustad P., Nes I.F., Morrison D.A. Identification of the streptococcal competence-pheromone receptor. Mol. Microbiol., 1996, no. 21, pp. 863-869. doi: 10.1046/j.1365-2958.1996.521416.x
  18. Hirst R.A., Cosai B., Rutman A., Guerin C.J., Nicotera P., Andrew P.W. O’Callaghan C. Streptococcus pneumoniae deficient in pneumolysin or autolysin has reduced virulence in meningitis. J. Infect. Dis., 2008, no. 197, pp. 744-751. doi: 10.1086/527322
  19. Hornick D.B., Allen B.L., Horn M.A., Clegg S. Adherence to respiratory epithelia by recombinant Escherichia coli expressing Klebsiella pneumoniae type 3 fimbrial gene products. Infect Immun., 1992, no. 60, pp. 1577-1588.
  20. Hossain S., De Silva B.C.J., Dahanayake P.S., Heo G.J. Phylogenetic relationships, virulence and antimicrobial resistance properties of Klebsiella sp. isolated from pet turtles in Korea. Lett. Appl. Microbiol., 2020, vol. 70, iss. 2, pp. 71-78. doi: 10.1111/lam.13245
  21. Jefferies J., Nieminen L., Kirkham L.A., Johnston C., Smith A., Mitchell T.J. Identification of a secreted cholesterol-dependent cytolysin (mitilysin) from Streptococcus mitis. J. Bacteriol., 2007, no. 189, pp. 627-632. doi: 10.1128/JB.01092-06
  22. Jounblat R., Kadioglu A., Mitchell T.J., Andrew P.W. Pneumococcal behavior and host responses during bronchopneumonia are affected differently by the cytolytic and complement-activating activities of pneumolysin. Infect. Immun., 2003, no. 71, pp. 18131819. doi: 10.1128/IAI.71.4.1813-1819.2003
  23. Khilnani G.C., Dubey D., Hadda V., Sahu S.R., Sood S., Madan K., Tiwari P., Mittal S., Mohan A., Pandey R.M., Guleria R. Predictors and microbiology of ventilator-associated pneumonia among patients with exacerbation of chronic obstructive pulmonary disease. Lung India, 2019, vol. 36, no. 6, pp. 506-511. doi: 10.4103/lungindia.lungindia_13_19
  24. Kilian M., Poulsen K., Blomqvist T., HAvarstein L.S., Bek-Thomsen M., Tettelin H., Sorensen U.B.S. Evolution of Streptococcus pneumoniae and its close commensal relatives. PLoS One, vol. 3, iss. 7: e2683. doi: 10.1371/journal.pone.0002683
  25. King S.J., Whatmore A.M., Dowson C.G. NanA, a neuraminidase from Streptococcus pneumoniae, shows high levels of sequence diversity, at least in part through recombination with Streptococcus oralis. J. Bacteriol, 2005, no. 187, pp. 5376-5386. doi: 10.1128/JB.187.15.5376-5386.2005
  26. Li Z., Sledjeski D.D., Kreikemeyer B., Podbielski A., Boyle M.D. Identification of pel, a Streptococcus pyogenes locus that affects both surface and secreted proteins. J. Bacteriol., 1999, no. 181, pp. 6019-6027.
  27. Lucas, V.S., Beighton D., Roberts G.J., Challacombe S.J. Changes in the oral streptococcal flora of children undergoing allogeneic bone marrow transplantation. J. Infect., 1997, no. 35, pp. 135-141. doi: 10.1016/S0163-4453(97)91545-0
  28. Marrie T.J., Peeling R.W., Fine M J. Ambulatory patients with community-aquired pneumonia: the frequency of atypical agents and clinical course. Am. J. Med,, 1996, vol. 101, pp. 508-515. doi: 10.1016/S0002-9343(96)00255-0
  29. Marrie T.J., Tirrel G.J., Majumbar S.R., Eurich D. Risk factors for pneumococcal endocarditi. Eur. J. Clin. Microbiol., 2018, vol. 37, no. 2,pp. 277-280. doi: 10.1007/s10096-017-3128-z
  30. Morrison, D.A. Streptococcal competence for genetic transformation: regulation by peptide pheromones. Microb. Drug Resist., 1997, no. 3, pp. 27-37. doi: 10.1089/mdr.1997.3.27
  31. Nakagawa I., Kurokawa K., Yamashita A. Genome sequence of an M3 strain of Streptococcus pyogenes reveals a large-scale genomic rearrangement in invasive strains and new insights into phage evolution. Genome Res., 2003, vol. 13, no. 6А, pp. 10421055.
  32. Neeleman C., Klaassen C.H., Klomberg D.M., de Valk H.A., Mouton J.W. Pneumolysin is a key factor in misidentification of macrolide-resistant Streptococcus pneumoniae and is a putative virulence factor of S. mitis and other streptococci. J. Clin. Microbiol,, 2004, no. 42, pp. 4355-4357. doi: 10.1128/JCM.42.9.4355-4357.2004
  33. Nobbs A.H., Lamont R.J., Jenkinson H.F. Streptococcus adherence and colonization. Microbiol. Mol. Biol. Rev., 2009, vol. 73, no. 3,pp. 407-450. doi: 10.1128/MMBR.00014-09.
  34. Potera C. Foraging a link between biofilms and disease. Science, 1999, no. 283, pp. 1837-1839. doi: 10.1126/science.283.5409.1837
  35. Struve C., Bojer M., Nielsen E.M., Hansen D.S., Krogfelt K.A. Investigation of the putative virulence gene magA in a worldwide collection of 495 Klebsiella isolates: magA is restricted to the gene cluster of Klebsiella pneumoniae capsule serotype K1. J. Med. Microbiol., 2005, no. 54,pp. 1111-1113. doi: 10.1099/jmm.0.46165-0
  36. Whatmore A.M., Efstratiou A., Pickerill A.P., Broughton K., Woodard G., Sturgeon D., George R., Dowson C.G. Genetic relationships between clinical isolates of Streptococcus pneumoniae, Streptococcus oralis, and Streptococcus mitis: characterization of “atypical” pneumococci and organisms allied to S. mitis harboring S. pneumoniae virulence factor-encoding genes. Infect. Immun, 2000, no. 68,pp. 1374-1382. doi: 10.1128/iai.68.3.1374-1382.2000
  37. Wu H., Mintz K.P., Ladha M., Fives-Taylor P.M. Isolation and characterization of Fap1, a fimbriae-associated adhesin of Streptococcus parasanguis FW213. Mol. Microbiol., 1998, no. 28(3), pp. 487-500. doi: 10.1046/j.1365-2958.1998.00805.x

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2020 Kraeva L.A., Kunilova E.S., Burgasova O.A., Hamdulaeva G.N., Danilova E.M., Bespalova G.I.

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