Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Bacillus subtilis from Soybean Food Shows Antimicrobial Activity for Multidrug-Resistant Acinetobacter baumannii by Affecting the adeS Gene

  • Wang, Tieshan (Clinical Laboratory Center, Beijing Friendship Hospital, Capital Medical University) ;
  • Su, Jianrong (Clinical Laboratory Center, Beijing Friendship Hospital, Capital Medical University)
  • Received : 2016.07.04
  • Accepted : 2016.08.24
  • Published : 2016.12.28
Download PDF
⟨ Previous Next ⟩

Abstract

Exploring novel antibiotics is necessary for multidrug-resistant pathogenic bacteria. Because the probiotics in soybean food have antimicrobial activities, we investigated their effects on multidrug-resistant Acinetobacter baumannii. Nineteen multidrug-resistant A. baumannii strains were clinically isolated as an experimental group and 11 multidrug-sensitive strains as controls. The growth rates of all bacteria were determined by using the analysis for xCELLigence Real-Time Cell. The combination of antibiotics showed synergistic effects on the strains in the control group but no effect on the strains in the experimental group. Efflux pump gene adeS was absent in all the strains from the control group, whereas it exists in all the strains from the experimental group. Furthermore, all the strains lost multidrug resistance when an adeS inhibitor was used. One strain of probiotics isolated from soybean food showed high antimicrobial activity for multidrug-resistant A. baumannii. The isolated strain belongs to Bacillus subtilis according to 16S RNA analysis. Furthermore, E. coli showed multidrug resistance when it was transformed with the adeS gene from A. baumannii whereas the resistant bacteria could be inhibited completely by isolated Bacillus subtilis. Thus, probiotics from soybean food provide potential antibiotics against multidrug-resistant pathogenic bacteria.

Keywords

References

  1. Arbex MA, Bonini EH, Kawakame Pirolla G, D'Ambrosio L, Centis R, Migliori GB. 2016. Effectiveness and safety of imipenem/clavulanate and linezolid to treat multidrug and extensively drug-resistant tuberculosis at a referral hospital in Brazil. Rev Port Pneumol (2006). DOI: 10.1016/j.rppnen. 2016.06.006.
  2. Ardebili A, Lari AR, Beheshti M, Lari ER. 2015. Association between mutations in gyrA and parC genes of Acinetobacter baumannii clinical isolates and ciprofloxacin resistance. Iran J. Basic Med. Sci. 18: 623-626.
  3. Asadollahi K, Taherikalani M, Maleki A, Alizadeh E, Valadbaigi H, Soroush S, et al. 2011. Diversity of aminoglycoside modifying enzyme genes among multidrug resistant Acinetobacter baumannii genotypes isolated from nosocomial infections in Tehran hospitals and their association with class 1 integrons. Acta Microbiol. Immunol. Hung. 58: 359-370. https://doi.org/10.1556/AMicr.58.2011.4.11
  4. Bonnin RA, Poirel L, Nordmann P. 2014. New Delhi metallo-beta-lactamase-producing Acinetobacter baumannii: a novel paradigm for spreading antibiotic resistance genes. Future Microbiol. 9: 33-41. https://doi.org/10.2217/fmb.13.69
  5. Cetin ES, Tekeli A, Ozseven AG, Us E, Aridogan BC. 2013. Determination of in vitro activities of polymyxin B and rifampin in combination with ampicillin/sulbactam or cefoperazone/sulbactam against multidrug-resistant Acinetobacter baumannii by the E-test and checkerboard methods. Jpn. J. Infect. Dis. 66: 463-468. https://doi.org/10.7883/yoken.66.463
  6. Chaari A, Pham T, Mnif B, Chtara K, Medhioub F, Baccouche N, et al. 2015. Colistin-tigecycline versus colistinimipenem-cilastatin combinations for the treatment of Acinetobacter baumannii ventilator-acquired pneumonia: a prognosis study. Intensive Care Med. 41: 2018-2019. https://doi.org/10.1007/s00134-015-4010-z
  7. Chung JH, Bhat A, Kim CJ, Yong D, Ryu CM. 2016. Combination therapy with polymyxin B and netropsin against clinical isolates of multidrug-resistant Acinetobacter baumannii. Sci. Rep. 6: 28168. https://doi.org/10.1038/srep28168
  8. Daniels TL, Deppen S, Arbogast PG, Griffin MR, Schaffner W, Talbot TR. 2008. Mortality rates associated with multidrug-resistant Acinetobacter baumannii infection in surgical intensive care units. Infect. Control Hosp. Epidemiol. 29: 1080-1083. https://doi.org/10.1086/591456
  9. De Bonis P, Lofrese G, Scoppettuolo G, Spanu T, Cultrera R, Labonia M, et al. 2016. Intraventricular versus intravenous colistin for the treatment of extensively drug resistant Acinetobacter baumannii meningitis. Eur. J. Neurol. 23: 68-75. https://doi.org/10.1111/ene.12789
  10. Farnworth E, Mainville I, Desjardins M-P, Gardner N, Fliss I, Champagne C. 2007. Growth of probiotic bacteria and bifidobacteria in a soy yogurt formulation. Int. J. Food Microbiol. 116: 174-181. https://doi.org/10.1016/j.ijfoodmicro.2006.12.015
  11. Garson W, Mc LC, Tetrault PA, Koffler H, Peterson DH, Colingsworth DR. 1949. On the naming of two antibiotics from members of the Bacillus circulans group; circulin and polypeptin. J. Bacteriol. 58: 115-116.
  12. Gholami M, Hashemi A, Hakemi-Vala M, Goudarzi H, Hallajzadeh M. 2015. Efflux pump inhibitor phenylalaninearginine beta-naphthylamide effect on the minimum inhibitory concentration of imipenem in Acinetobacter baumannii strains isolated from hospitalized patients in Shahid Motahari Burn Hospital, Tehran, Iran. Jundishapur J. Microbiol. 8: e19048.
  13. Gulen TA, Guner R, Celikbilek N, Keske S, Tasyaran M. 2015. Clinical importance and cost of bacteremia caused by nosocomial multi drug resistant Acinetobacter baumannii. Int. J. Infect. Dis. 38: 32-35. https://doi.org/10.1016/j.ijid.2015.06.014
  14. Hamdy Mohammed el S, Elsadek Fakhr A, Mohammed El Sayed H, Al Johery SA, Abdel Ghani Hassanein W. 2016. Spread of TEM, VIM, SHV, and CTX-M beta-lactamases in imipenem-resistant gram-negative bacilli isolated from Egyptian Hospitals. Int. J. Microbiol. 2016: 8382605.
  15. Hamidian M, Holt KE, Hall RM. 2015. Genomic resistance island AGI1 carrying a complex class 1 integron in a multiply antibiotic-resistant ST25 Acinetobacter baumannii isolate. J. Antimicrob. Chemother. 70: 2519-2523. https://doi.org/10.1093/jac/dkv137
  16. Howard A, O'Donoghue M, Feeney A, Sleator RD. 2012. Acinetobacter baumannii: an emerging opportunistic pathogen. Virulence 3: 243-250. https://doi.org/10.4161/viru.19700
  17. Huang C, Long Q, Qian K, Fu T, Zhang Z, Liao P, Xie J. 2015. Resistance and integron characterization of Acinetobacter baumannii in a teaching hospital in Chongqing, China. New Microbes New Infect. 8: 103-108. https://doi.org/10.1016/j.nmni.2015.09.015
  18. Jean SS, Hsieh TC, Hsu CW, Lee WS, Bai KJ, Lam C. 2015. Comparison of the clinical efficacy between tigecycline plus extended-infusion imipenem and sulbactam plus imipenem against ventilator-associated pneumonia with pneumonic extensively drug-resistant Acinetobacter baumannii bacteremia, and correlation of clinical efficacy with in vitro synergy tests. J. Microbiol. Immunol. Infect. DOI: 10.1016/j.jmii.2015.06.009.
  19. Kao CY, Chen SS, Hung KH, Wu HM, Hsueh PR, Yan JJ, Wu JJ. 2016. Overproduction of active efflux pump and variations of OprD dominate in imipenem-resistant Pseudomonas aeruginosa isolated from patients with bloodstream infections in Taiwan. BMC Microbiol. 16: 107. https://doi.org/10.1186/s12866-016-0719-2
  20. Kim SY, Park SY, Choi SK, Park SH. 2015. Biosynthesis of polymyxins B, E, and P using genetically engineered polymyxin synthetases in the surrogate host Bacillus subtilis. J. Microbiol. Biotechnol. 25: 1015-1025. https://doi.org/10.4014/jmb.1505.05036
  21. Kuo HY, Chang KC, Liu CC, Tang CY, Peng JH, Lu CW, et al. 2014. Insertion sequence transposition determines imipenem resistance in Acinetobacter baumannii. Microb. Drug Resist. 20: 410-415. https://doi.org/10.1089/mdr.2014.0004
  22. Lamers RP, Cavallari JF, Burrows LL. 2013. The efflux inhibitor phenylalanine-arginine beta-naphthylamide (PAbetaN) permeabilizes the outer membrane of gram-negative bacteria. PLoS One 8: e60666. https://doi.org/10.1371/journal.pone.0060666
  23. Lee HY, Huang CW, Chen CL, Wang YH, Chang CJ, Chiu CH. 2015. Emergence in Taiwan of novel imipenem-resistant Acinetobacter baumannii ST455 causing bloodstream infection in critical patients. J. Microbiol. Immunol. Infect. 48: 588-596.
  24. Li S, Zhu D, Li K, Yang Y, Lei Z, Zhang Z. 2013. Soybean curd residue: composition, utilization, and related limiting factors. ISRN Ind. Eng. 2013: 423590.
  25. Lin MF, Lin YY, Tu CC, Lan CY. 2015. Distribution of different efflux pump genes in clinical isolates of multidrugresistant Acinetobacter baumannii and their correlation with antimicrobial resistance. J. Microbiol. Immunol. Infect. DOI: 10.1016/j.jmii.2015.04.004.
  26. Lowings M, Ehlers MM, Dreyer AW, Kock MM. 2015. High prevalence of oxacillinases in clinical multidrug-resistant Acinetobacter baumannii isolates from the Tshwane region, South Africa - an update. BMC Infect. Dis. 15: 521. https://doi.org/10.1186/s12879-015-1246-8
  27. Lucasti C, Vasile L, Sandesc D, Venskutonis D, McLeroth P, Lala M, et al. 2016. Phase 2, dose-ranging study of relebactam with imipenem/cilastatin in subjects with complicated intra-abdominal infection. Antimicrob. Agents Chemother. 60: 6234-6243. https://doi.org/10.1128/AAC.00633-16
  28. Lytvynenko I, Brill S, Oswald C, Pos KM. 2016. Molecular basis of polyspecificity of the small multidrug resistance efflux pump AbeS from Acinetobacter baumannii. J. Mol. Biol. 428: 644-657. https://doi.org/10.1016/j.jmb.2015.12.006
  29. Machairas N, Pistiki A, Droggiti DI, Georgitsi M, Pelekanos N, Damoraki G, et al. 2015. Pre-treatment with probiotics prolongs survival after experimental infection by multidrugresistant Pseudomonas aeruginosa in rodents: an effect on sepsis-induced immunosuppression. Int. J. Antimicrob. Agents 45: 376-384. https://doi.org/10.1016/j.ijantimicag.2014.11.013
  30. Maspi H, Mahmoodzadeh Hosseini H, Amin M, Imani Fooladi AA. 2016. High prevalence of extensively drugresistant and metallo beta-lactamase-producing clinical Acinetobacter baumannii in Iran. Microb. Pathog. 98: 155-159. https://doi.org/10.1016/j.micpath.2016.07.011
  31. McGann P, Courvalin P, Snesrud E, Clifford RJ, Yoon EJ, Onmus-Leone F, et al. 2014. Amplification of aminoglycoside resistance gene aphA1 in Acinetobacter baumannii results in tobramycin therapy failure. MBio 5: e00915.
  32. Meletis G, Oustas E, Botziori C, Kakasi E, Koteli A. 2015. Containment of carbapenem resistance rates of Klebsiella pneumoniae and Acinetobacter baumannii in a Greek hospital with a concomitant increase in colistin, gentamicin and tigecycline resistance. New Microbiol. 38: 417-421.
  33. Munoz-Price LS, Weinstein RA. 2008. Acinetobacter infection. N. Engl. J. Med. 358: 1271-1281. https://doi.org/10.1056/NEJMra070741
  34. Park S, Lee KM, Yoo YS, Yoo JS, Yoo JI, Kim HS, et al. 2011. Alterations of gyrA, gyrB, and parC and activity of efflux pump in fluoroquinolone-resistant Acinetobacter baumannii. Osong Public Health Res. Perspect. 2: 164-170. https://doi.org/10.1016/j.phrp.2011.11.040
  35. Pomba C, Endimiani A, Rossano A, Saial D, Couto N, Perreten V. 2014. First report of OXA-23-mediated carbapenem resistance in sequence type 2 multidrug-resistant Acinetobacter baumannii associated with urinary tract infection in a cat. Antimicrob. Agents Chemother. 58: 1267-1268. https://doi.org/10.1128/AAC.02527-13
  36. Sun C, Hao J, Dou M, Gong Y. 2015. Mutant prevention concentrations of levofloxacin, pazufloxacin and ciprofloxacin for A. baumannii and mutations in gyrA and parC genes. J. Antibiot. (Tokyo) 68: 313-317. https://doi.org/10.1038/ja.2014.150
  37. Wen JT, Zhou Y, Yang L, Xu Y. 2014. Multidrug-resistant genes of aminoglycoside-modifying enzymes and 16S rRNA methylases in Acinetobacter baumannii strains. Genet. Mol. Res. 13: 3842-3849. https://doi.org/10.4238/2014.May.16.9
  38. Xiao SZ, Chu HQ, Han LZ, Zhang ZM, Li B, Zhao L, Xu L. 2016. Resistant mechanisms and molecular epidemiology of imipenem-resistant Acinetobacter baumannii. Mol. Med. Rep. 14: 2483-2488. https://doi.org/10.3892/mmr.2016.5538
  39. Yang YS, Lee Y, Tseng KC, Huang WC, Chuang MF, Kuo SC, et al. 2016. In vivo and in vitro efficacy of minocyclinebased combination therapy for minocycline-resistant Acinetobacter baumannii. Antimicrob. Agents Chemother. 60: 4047-4054. https://doi.org/10.1128/AAC.02994-15

Cited by

  1. 발효 된장의 바이오제닉 아민 함량에 영향을 미치는 바실러스균의 분리 동정 및 프로바이오틱 특성 vol.55, pp.2, 2016, https://doi.org/10.7845/kjm.2019.9017
  2. Peculiarities of Biofilms Formation by Campylobacter Bacteria in Mixed Populations with Other Microbial Contaminants of Food Products vol.168, pp.1, 2016, https://doi.org/10.1007/s10517-019-04647-1