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Mechanisms of Resistance to Clinically Significant Antibiotics of Bacterial Strains of the Genus Bacillus Isolated from Samples from the International Space Station

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Abstract

The Russian Segment of the International Space Station, as a closed habitat, is a favorable environment for the development of microorganisms. There are bacteria and fungi of various systematic groups, some of which can lead to infections. Thus, certain species of spore-forming bacteria of the genus Bacillus are dangerous. Seven strains of bacteria of this genus isolated from samples obtained at the station showed resistance to β-lactam antibiotics, such as penicillin, ampicillin, meropenem, a number of cephalosporin derivatives I (cefazolin), II (cefuroxime), III (ceftriaxone, cefoperazone, ceftazidime), IV (cefepime) generations, and the aminocyclitol antibiotic spectinomycin. It has been found that all these strains are resistant to penicillin and ampicillin with a minimum inhibitory concentration (MIC) from 16 to 2048 μg/mL as well as to cephalosporin antibiotics and meropenem with a MIC value from 2 to 2048 μg/mL. Bacterial resistance to spectinomycin used in patients with an allergy to β-lactams (penicillins and cephalosporins) is in the MIC range from 32 to 2048 μg/mL. The absence of active efflux pumps in B. licheniformis 7-12 with high MIC values for penicillin and ampicillin suggested that this strain has a β-lactamase defense mechanism against these antibiotics. Three more strains resistant to penicillin and ampicillin—B. subtilis 14-12, Bacillus sp. R2HG21, Bacillus sp. HEP3B2—have another defense mechanism: the active transport of antibiotic from the cell, which is mediated by the presence of efflux pumps functioning due to the electrochemical potential of the cell membrane. In six strains of the studied bacilli, it has been shown that the resistance to cephalosporin derivatives of the third to fourth generations—ceftriaxone, ceftazidime, cefepime and the aminocyclitol antibiotic spectinomycin—is also apparently provided by the systems of active outflow of xenobiotics belonging to the group of secondary transporters.

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REFERENCES

  1. Mora, M., Mahnert, A., Koskinen, K., Pausan, M.R., Oberauner-Wappis, L., Krause, R., Perras, A.K., Gorkiewicz, G., Berg, G., and Moissl-Eichinger, C., Microorganisms in confined habitats: Microbial monitoring and control of intensive care units, operating rooms, cleanrooms and the International Space Station, Front Microbiol., 2016, vol. 7, p. 1573.

    Article  Google Scholar 

  2. Mora, M., Perras, A., Alekhova, T., Wink, L., Krause, R., Aleksandrova, A., Novozhilova, T., and Moissl-Eichinger, C., Resilient microorganisms in dust samples of the International Space Station—survival of the adaptation specialists, Microbiome, 2016, vol. 4, no. 1, pp. 65–85.

    Article  Google Scholar 

  3. Alekhova, T.A., Zakharchuk, L.M., Tatarinova, N.Y., Kadnikov, V.V., Mardanov, A.V., Ravin, N.V., and Skryabin, K.G., Diversity of bacteria of the genus Bacillus on board of international space station, Dokl. Biochem. Biophys., 2015, vol. 465, no. 1, pp. 104–107.

    Article  Google Scholar 

  4. Coil, D.A., Neches, R.Y., Lang, J.M., Brown, W.E., Severance, M., Cavalier, D.D., and Eisen, J.A., Growth of 48 built environment bacterial isolates on board the International Space Station (ISS), Peer J., 2016, vol. 4, e1842.

    Article  Google Scholar 

  5. Moissl-Eichinger, C., Cockell, C., and Rettberg, P., Venturing into new realms? Microorganisms in space, FEMS Microbiol. Rev., 2016, vol. 40, no. 5, pp. 722–737.

    Article  CAS  Google Scholar 

  6. Checinska, A., Probst, A.J., Vaishampayan, P., White, J.R., Kumar, D., Stepanov, V.G., Fox, G.E., Nilsson, H.R., Pierson, D.L., Perry, J., and Venkateswaran, K., Microbiomes of the dust particles collected from the International Space Station and Spacecraft Assembly Facilities, Microbiome, 2015, vol. 3, no. 1, pp. 50–68.

    Article  Google Scholar 

  7. Vaishampayan, K.P., Cisneros, J., Pierson, D.L., Rogers, S.O., and Perry, J., International Space Station environmental microbiome-microbial inventories of ISS filter debris, Appl. Microbiol. Biotechnol., 2014, vol. 98, no. 14, pp. 6453–6466.

    Article  Google Scholar 

  8. Farrar, W.E. and Reboli, A.C., The genus Bacillus—Medical, in The Prokaryotes. Handbook on the Biology of Bacteria, vol. 4: Bacteria: Firmicutes, Cyanobacteria, Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H., and Stackebrandt, E., Eds., New York: Springer-Verlag, 2006, pp. 609–630.

  9. Janda, J.M. and Abbot, S.L., 16s rRNA gene sequencing for bacterial identification in the diagnostic laboratory: Pluses, perils, and pitfalls, J. Clin. Microbiol., 2007, vol. 45, no. 9, pp. 2761–2764.

    Article  CAS  Google Scholar 

  10. Elshikh, M., Ahmed, S., Funston, S., Dunlop, P., McGaw, M., Marchant, R., and Banat, I.M., Resazurin-based 96-well plate microdilution method for the determination of minimum inhibitory concentration of biosurfactants, Biotechnol. Lett., 2016, vol. 38, no. 6, pp. 1015–1019.

    Article  CAS  Google Scholar 

  11. Ardebili, A., Lari, A.R., and Talebi, M., Correlation of ciprofloxacin resistance with the AdeABC efflux system in Acinetobacter baumannii clinical isolates, Ann. Lab. Med., 2014, vol. 34, no. 6, pp. 433–438.

    Article  Google Scholar 

  12. Li, X.Z. and Nikaido, H., Efflux-mediated drug resistance in bacteria, Drugs, 2004, vol. 64, no. 2, pp. 159–204.

    Article  CAS  Google Scholar 

  13. Timmery, S., Hu, X., and Mahillon, J., Characterization of Bacilli isolated from the confined environments of the Antarctic Concordia station and the International Space Station, Astrobiology, 2011, vol. 11, no. 4, pp. 323–334.

    Article  CAS  Google Scholar 

  14. 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., and 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, no. 5, pp. 445–456.

    Article  Google Scholar 

  15. Gaci, N., Borrel, G., Tottey, W., O’Toole, P.W., and Brugère, J-F., Archaea and the human gut: New beginning of an old story, World J. Gastroenterol., 2014, vol. 20, no. 43, pp. 16062–16078.

    Article  CAS  Google Scholar 

  16. Nolivos, S., Cayron, J., Dedieu, A., Page, A., Delolme, F., and Lesterlin, C., Role of AcrAB-TolC multidrug efflux pump in drug-resistance acquisition by plasmid transfer, Science, 2019, vol. 364, no. 6442, pp. 778–782.

    Article  CAS  Google Scholar 

  17. Foster, T.J., Antibiotic resistance in Staphylococcus aureus. Current status and future prospects, FEMS Microbiol. Rev., 2017, vol. 41, no. 3, pp. 430–449.

    Article  CAS  Google Scholar 

  18. Piddock, L.J.V., Multidrug-resistance efflux pumps? Not just for resistance, Nat. Rev. Microbiol., 2006, vol. 4, no. 8, pp. 629–636.

    Article  CAS  Google Scholar 

  19. Poole, K., Efflux pumps as antimicrobial resistance mechanisms, Ann. Med., 2007, vol. 39, no. 3, pp. 162–176.

    Article  CAS  Google Scholar 

  20. Blair, J.M.A., Richmond, G.E., and Piddock, L.J.V., Multidrug efflux pumps in gram-negative bacteria and their role in antibiotic resistance, Future Microbiol., 2014, vol. 9, no. 10, pp. 1165–1177.

    Article  CAS  Google Scholar 

  21. Peleg, A.Y., Adams, J., and Paterson, D.L., Tigecycline efflux as a mechanism for nonsusceptibility in Acinetobacter baumannii, Antimicrob. Agents Chemother., 2007, vol. 51, no. 6, pp. 2065–2069.

    Article  CAS  Google Scholar 

  22. Baranova, N. and Elkins, C.A., Antimicrobial drug efflux pumps in other gram-positive bacteria, in Efflux-Mediated Antimicrobial Resistance in Bacteria. Mechanisms, Regulation and Clinical Implications, Li, X., Elkins, C.A., and Zgurskaya, H.I., Eds., Cham: Springer, 2018, pp. 197–218.

    Google Scholar 

  23. Masaoka, Y., Ueno, Y., Morita, Y., Kuroda, T., Mizushima, T., and Tsuchiya, T., A two-component multidrug efflux pump, EbrAB, in Bacillus subtilis, J. Bacteriol., 2000, vol. 182, no. 8, pp. 2307–2310.

    Article  CAS  Google Scholar 

  24. Zhang, Z.C., Pornillos, M.O., Chang, X.G., and Saier, M.H., Functional characterization of the heterooligomeric EbrAB multidrug efflux transporter of Bacillus subtilis, Biochemistry, 2007, vol. 46, no. 17, pp. 5218–5225.

    Article  CAS  Google Scholar 

  25. Van Houdt, R., Mijnendonckx, K., and Leys, N., Microbial contamination monitoring and control during human space missions, Planet. Space Sci., 2012, vol. 60, no. 1, pp. 115–120.

    Article  Google Scholar 

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The research was self-funded.

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Authors and Affiliations

  1. Department of Microbiology, School of Biology, Moscow State University, 119234, Moscow, Russia

    R. R. Yenikeyev, N. Y. Tatarinova & L. M. Zakharchuk

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  1. R. R. Yenikeyev
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  2. N. Y. Tatarinova
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  3. L. M. Zakharchuk
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Correspondence to R. R. Yenikeyev.

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The authors declare that they have no conflict of interests. This article does not contain any studies involving animals or human participants performed by any of the authors.

ADDITIONAL INFORMATION

Yenikeyev ORCID http://orcid.org/0000-0002-8467-9051

Tatarinova ORCID http://orcid.org/0000-0002-9883-5780

Zakharchuck ORCID http://orcid.org/0000-0003-3783-3279

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Translated by E. V. Makeeva

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Yenikeyev, R.R., Tatarinova, N.Y. & Zakharchuk, L.M. Mechanisms of Resistance to Clinically Significant Antibiotics of Bacterial Strains of the Genus Bacillus Isolated from Samples from the International Space Station. Moscow Univ. Biol.Sci. Bull. 75, 224–230 (2020). https://doi.org/10.3103/S0096392520040045

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