Mechanisms of resistance to clinically significant antibiotics in strains of bacteria of the genus Bacillus isolated from samples obtained from a medical institution
Abstract
Isolates of bacterial strains dominating on the surfaces of medical laboratory equipment for the selection of blood tests were obtained. Pure cultures of these bacteria are identified as Bacillus cereus HSA01, Bacillus cereus HSA12, Bacillus cereus HSA03, Bacillus subtilis HSA06, Bacillus amyloliquefaciens HSA09. The resistance of bacteria to a number β-lactam antibiotics and spectinomycin was determined. All strains are resistant to penicillin and ampicillin with a minimum inhibitory concentration (MIC) from 256 to 2048 μg/ml, as well as to cephalosporin antibiotics with a MIC value from 2 to 2048 μg/ml. Bacterial resistance to spectinomycin used in patients with allergy to penicillins and cephalosporins is in the MIC range from 16 to 256 μg/ml.
In B. cereus HSA01, resistance to ampicillin and cefuroxime is due to the operation of efflux pumps, to ceftazidime is provided by the action of metal-β-lactamases (MBL), and to penicillin is explained by the operation of both these systems. High resistance to ampicillin B. cereus HSA12 is provided by the action of MBL, to cefuroxime – by efflux activity, while resistance to ceftazidime is accompanied by the presence of MBL and the action of efflux pumps. In B. cereus HSA03, resistance to penicillin, ampicillin, cefepime, and ceftazidime is explained by efflux activity, to cefazolin and ceftazidime is provided by MBL, and to ampicillin and ceftazidime is due to the presence of both MBL and efflux. The resistance of B. subtilis HSA06 to penicillin and ampicillin is provided only by MBL activity. In B. amyloliquefaciens HSA09, resistance to ampicillin is explained by both the presence of MBL and efflux pumps, and to penicillin is provided only by the action of efflux.
Thus, in the studied group of bacilli, resistance to penicillin, ampicillin and a number of cephalosporin derivatives is provided, depending on the strain and the specific antibiotic, of metal-β-lactamase and/or efflux pumps. Pumps function due to the electrochemical potential of the cell membrane and belong to the group of secondary transporters.
About the Authors
R. R. YenikeyevRussian Federation
1–12 Leninskie gory, Moscow, 119234, Russia
N. Y. Tatarinova
Russian Federation
1–12 Leninskie gory, Moscow, 119234, Russia
L. M. Zakharchuk
Russian Federation
1–12 Leninskie gory, Moscow, 119234, Russia
E. N. Vinogradova
Russian Federation
1–12 Leninskie gory, Moscow, 119234, Russia
References
1. Nikaido H. Multidrug resistance in bacteria // Annu. Rev. Biochem. 2009. Vol. 78. P. 119–146.
2. Farrar W.E., Reboli A.C. The genus Bacillus—Medical // The Prokaryotes. Handbook on the biology of bacteria, vol. 4. Bacteria: Firmicutes, Cyanobacteria / Eds. M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, and E. Stackebrandt. N.Y.: SpringerVerlag, 2006. P. 609–630.
3. Bianco A., Capozzi L., Monno M.R., Del Sambro L., Manzulli V., Pesole G., Loconsole D., Parisi A. Characterization of Bacillus cereus group isolates from human bacteremia by whole-genome sequencing // Front. Microbiol. 2021. Vol. 11: 599524.
4. Ehling-Schulz M., Koehler T.M., Lereclus D. The Bacillus cereus Group: Bacillus species with pathogenic potential // Gram-positive pathogens. 3rd Ed. / Eds. V.A. Fischetti, R.P. Novick, J.J. Ferretti, D.A. Portnoy, M. Braunstein, and J.I. Rood. Washington: ASM Press, 2019. P. 875–902.
5. Yenikeyev R.R., Tatarinova N.Y., Zakharchuk L.M. Mechanisms of resistance to clinically significant antibiotics of strains of bacteria of the genus Bacillus isolated from samples delivered from the International Space Station // Moscow Univ. Biol. Sci. Bull. 2020. Vol. 75. N 4. P. 224–230.
6. Janda J.M., Abbot S.L. 16S rRNA gene sequencing for bacterial identification in the diagnostic laboratory: pluses, perils, and pitfalls // J. Clin. Microbiol. 2007. Vol. 45. N 9. P. 2761–2764.
7. Hrabak J., Chudackova E., Walkova R. Matrixassisted laser desorption ionization time- of flight (MALDI-TOF) mass spectrometry for detection of antibiotic resistance mechanisms: from research to routine diagnosis // Clin. Microbiol. Rev. 2013. Vol. 26. N 1. P. 103–114.
8. Ardebili A., Lari A.R., Talebi M. Correlation of ciprofloxacin resistance with the AdeABC efflux system in Acinetobacter baumannii clinical isolates // Ann. Lab. Med. 2014. Vol. 34. N 6. P. 433–438.
9. Aoki N., Ishii Y. , Tateda K., Saga T., Kimura S., Kikuchi Y., Kobayashi T., Tanabe Y., Tsukada H., Gejyo F., Yamaguchi K. Efficacy of calcium-EDTA as an inhibitor for metallo-β-lactamase in a mouse model of Pseudomonas aeruginosa pneumonia // Antimicrob. Agents Chemother. 2010. Vol. 54. N 11. P. 4582–4588.
10. Лазарева А.В., Крыжановская О.А., Бочарова Ю.А., Чеботарь И.В., Маянский Н.А. Распространенность металл-β-лактамаз и эффлюкс-механизмов у карбапенемрезистентных госпитальных штаммов Pseudomonas aeruginosa, выделенных в г. Москве в 2012–2015 гг. // Вестн. РАМН. 2015. Т. 70. № 6. С. 679–683.
11. Li X.Z., Nikaido H. Efflux-mediated drug resistance in bacteria // Drugs. 2004. Vol. 64. N 2. P. 159–204.
12. Bush K. Past and present perspectives on β-lactamases // Antimicrob. Agents Chemother. 2018. Vol. 62. N 10: e01076-18.
13. Timmery S., Hu X., Mahillon J. Characterization of bacilli isolated from the confined environments of the Antarctic Concordia station and the International Space Station // Astrobiology. 2011. Vol. 11. N 4. P. 323–334.
14. Coil D.A., Neches R.Y., Lang J.M., Brown W.E., Severance M., Cavalier D.D., Eisen J.A. Growth of 48 built environment bacterial isolates on board the International Space Station (ISS) // Peer J. 2016. Vol. 4: e1842.
15. Moissl-Eichinger C., Cockell C., Rettberg P. Venturing into new realms? Microorganisms in space // FEMS Microbiol. Rev. 2016. Vol. 40. N 5. P. 722–737.
16. Horneck G., Moeller R., Cadet J., Douki T., Rocco L., Mancinelli R.L., Wayne L., Nicholson W.L., Panitz C., Rabbow E., Rettberg P., Spry A., Stackebrandt E., Vaishampayan P., Venkateswaran K.J. Resistance of bacterial endospores to outer space for planetary protection purposes – Experiment PROTECT of the EXPOSE-E Mission // Astrobiology. 2012. Vol. 12. N 5. P. 445–456.
17. Uchino Y., Iriyama N., Matsumoto K., Hirabayashi Y., Miura K., Kurita D., Kobayashi Y., Yagi M., Kodaira H., Hojo A., Kobayashi S., Hatta Y., Takeuchi J. A case series of Bacillus cereus septicemia in patients with hematological disease // Intern. Med. 2012. Vol. 51. N 19. P. 2733–2738.
18. Schmid P.J., Maitz S., Kittinger C. Bacillus cereus in packaging material: Molecular and phenotypical diversity revealed // Front. Microbiol. 2021. Vol. 12: 698974.
19. Dellinger R.P., Levy M.M., Rhodes A., et al. Surviving sepsis campaign: international guidelines for management of severe sepsis and septic shock, 2012 // Crit. Care Med. 2013. Vol. 41. N 2. P. 580–637.
20. Nolivos S., Cayron J., Dedieu A., Page A., Delolme F., Lesterlin C. Role of AcrAB-TolC multidrug efflux pump in drug-resistance acquisition by plasmid transfer // Science. 2019. Vol. 364. N 6442. P. 778–782.
21. Foster T.J. Antibiotic resistance in Staphylococcus aureus. Current status and future prospects // FEMS Microbiol. Rev. 2017. Vol. 41. N 3. P. 430–449.
22. Baranova N., Elkins C.A. Antimicrobial drug efflux pumps in other gram-positive bacteria // effluxmediated antimicrobial resistance in bacteria. Mechanisms, regulation and clinical implications / Eds. X. Li, C.A. Elkins, and H.I. Zgurskaya. Springer Publ., 2016. P. 197–218.
23. Hassan K.A., Fagerlund A., Elbourne L.D.H., Voros A., Kroeger J.K., Simm R., Tourasse N.J., Finke S., Henderson P.J.F., Okstad J.A., Paulsen I.T., Kolsto A. The putative drug efflux systems of the Bacillus cereus group // PLoS One. 2017. Vol. 12. N 5. P. 35.
24. Stewart N.K., Bhattacharya M., Toth M., Smith C.A., Vakulenko S.B. A surface loop modulates activity of the Bacillus class D β-lactamases // J. Struct. Biol. 2020. Vol. 211. N 2: 107544.
25. Karsisiotis A.I., Damblon C.F. Gordon C.K. Roberts G.C.K. Solution structures of the Bacillus cereus metallo-β-lactamase BcII and its complex with the broad spectrum inhibitor R-thiomandelic acid // Biochem J. 2013. Vol. 456. N 3. P. 397–407.
26. Miyamoto T, Sukimoto K, Sayed A., Kim S., Honjoh K., Hatano S. Detection of penicillin-binding proteins in Bacillus cereus by using biotinylated β-lactams // J. Fac. Agric. Kyushu Univ. 2000. Vol. 44. N 3. P. 299–307.
27. van Duijkeren E., Schink A.K., Roberts M.C., Wang Y., Schwarz S. Mechanisms of bacterial resistance to antimicrobial agents // Microbiol. Spectr. 2017. Vol. 6. N 2. DOI: https://doi.org/10.1128/microbiolspec.ARBA-0019-2017.
Review
For citations:
Yenikeyev R.R., Tatarinova N.Y., Zakharchuk L.M., Vinogradova E.N. Mechanisms of resistance to clinically significant antibiotics in strains of bacteria of the genus Bacillus isolated from samples obtained from a medical institution. Vestnik Moskovskogo universiteta. Seriya 16. Biologiya. 2022;77(2):89–97. (In Russ.)