DOI QR코드

DOI QR Code

NaCl Concentration-Dependent Aminoglycoside Resistance of Halomonas socia CKY01 and Identification of Related Genes

  • Park, Ye-Lim (Department of Biological Engineering, College of Engineering, Konkuk University) ;
  • Choi, Tae-Rim (Department of Biological Engineering, College of Engineering, Konkuk University) ;
  • Kim, Hyun Joong (Department of Biological Engineering, College of Engineering, Konkuk University) ;
  • Song, Hun-Suk (Department of Biological Engineering, College of Engineering, Konkuk University) ;
  • Lee, Hye Soo (Department of Biological Engineering, College of Engineering, Konkuk University) ;
  • Park, Sol Lee (Department of Biological Engineering, College of Engineering, Konkuk University) ;
  • Lee, Sun Mi (Department of Biological Engineering, College of Engineering, Konkuk University) ;
  • Kim, Sang Hyun (Department of Biological Engineering, College of Engineering, Konkuk University) ;
  • Park, Serom (Department of Biological Engineering, College of Engineering, Konkuk University) ;
  • Bhatia, Shashi Kant (Department of Biological Engineering, College of Engineering, Konkuk University) ;
  • Gurav, Ranjit (Department of Biological Engineering, College of Engineering, Konkuk University) ;
  • Sung, Changmin (Doping Control Center, Korea Institute of Science and Technology) ;
  • Seo, Seung-Oh (Department of Food Science and Nutrition, The Catholic University of Korea) ;
  • Yang, Yung-Hun (Department of Biological Engineering, College of Engineering, Konkuk University)
  • 투고 : 2020.09.11
  • 심사 : 2020.11.02
  • 발행 : 2021.02.28

초록

Among various species of marine bacteria, those belonging to the genus Halomonas have several promising applications and have been studied well. However, not much information has been available on their antibiotic resistance. In our efforts to learn about the antibiotic resistance of strain Halomonas socia CKY01, which showed production of various hydrolases and growth promotion by osmolytes in previous study, we found that it exhibited resistance to multiple antibiotics including kanamycin, ampicillin, oxacillin, carbenicillin, gentamicin, apramycin, tetracycline, and spectinomycin. However, the H. socia CKY01 resistance pattern to kanamycin, gentamicin, apramycin, tetracycline, and spectinomycin differed in the presence of 10% NaCl and 1% NaCl in the culture medium. To determine the mechanism underlying this NaCl concentration-dependent antibiotic resistance, we compared four aminoglycoside resistance genes under different salt conditions while also performing time-dependent reverse transcription PCR. We found that the aph2 gene encoding aminoglycoside phosphotransferase showed increased expression under the 10% rather than 1% NaCl conditions. When these genes were overexpressed in an Escherichia coli strain, pETDuet-1::aph2 showed a smaller inhibition zone in the presence of kanamycin, gentamicin, and apramycin than the respective control, suggesting aph2 was involved in aminoglycoside resistance. Our results demonstrated a more direct link between NaCl and aminoglycoside resistance exhibited by the H. socia CKY01 strain.

키워드

참고문헌

  1. Dalmaso GZL, Ferreira D, Vermelho AB. 2015. Marine extremophiles: a source of hydrolases for biotechnological applications. Mar. Drugs 13: 1925-1965. https://doi.org/10.3390/md13041925
  2. Hong J-W, Song H-S, Moon Y-M, Hong Y-G, Bhatia SK, Jung H-R, et al. 2019. Polyhydroxybutyrate production in halophilic marine bacteria Vibrio proteolyticus isolated from the Korean peninsula. Bioprocess Biosyst. Eng. 42: 603-610. https://doi.org/10.1007/s00449-018-02066-6
  3. Gurav R, Bhatia SK, Moon Y-M, Choi T-R, Jung H-R, Yang S-Y, et al. 2019. One-pot exploitation of chitin biomass for simultaneous production of electricity, n-acetylglucosamine and polyhydroxyalkanoates in microbial fuel cell using novel marine bacterium Arenibacter palladensis YHY2. J. Clean. Prod. 209: 324-332. https://doi.org/10.1016/j.jclepro.2018.10.252
  4. Diken E, Ozer T, Arikan M, Emrence Z, Oner ET, Ustek D, et al. 2015. Genomic analysis reveals the biotechnological and industrial potential of levan producing halophilic extremophile, Halomonas smyrnensis AAD6T. SpringerPlus 4: 393. https://doi.org/10.1186/s40064-015-1184-3
  5. Dash HR, Mangwani N, Chakraborty J, Kumari S, Das S. 2013. Marine bacteria: potential candidates for enhanced bioremediation. Appl. Microbiol. Biotechnol. 97: 561-571. https://doi.org/10.1007/s00253-012-4584-0
  6. Wang Y, Song Q, Zhang X-H. 2016. Marine microbiological enzymes: studies with multiple strategies and prospects. Mar. Drugs 14: 171. https://doi.org/10.3390/md14100171
  7. Bhatia SK, Kim J, Song H-S, Kim HJ, Jeon J-M, Sathiyanarayanan G, et al. 2017. Microbial biodiesel production from oil palm biomass hydrolysate using marine Rhodococcus sp. YHY01. Bioresour. Technol. 233: 99-109. https://doi.org/10.1016/j.biortech.2017.02.061
  8. Aston JE, Peyton BM. 2007. Response of Halomonas campisalis to saline stress: changes in growth kinetics, compatible solute production and membrane phospholipid fatty acid composition. FEMS Microbiol. Lett. 274: 196-203. https://doi.org/10.1111/j.1574-6968.2007.00851.x
  9. Vargas C, Canovas D, Calderon M, Moron M, Carrasco R, Ventosa A, et al. 2000. Osmoprotection by compatible solutes accumulation in the moderately halophilic bacterium Halomonas elongata DSM 3043. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 126: s151.
  10. Park Y-L, Bhatia SK, Gurav R, Choi T-R, Kim HJ, Song H-S, et al. 2020. Fructose based hyper production of poly-3-hydroxybutyrate from Halomonas sp. YLGW01 and impact of carbon sources on bacteria morphologies. Int. J. Biol. Macromol. 154: 929-936. https://doi.org/10.1016/j.ijbiomac.2020.03.129
  11. Johnson J, Sudheer PD, Yang Y-H, Kim Y-G, Choi K-Y. 2017. Hydrolytic activities of hydrolase enzymes from halophilic microorganisms. Biotechnol. Bioprocess Eng. 22: 450-461. https://doi.org/10.1007/s12257-017-0113-4
  12. Park Y-L, Han Y-H, Song H-S, Park J-Y, Bhatia SK, Gurav R, et al. 2020. Effects of osmolytes on salt resistance of Halomonas socia CKY01 and identification of osmolytes-related genes by genome sequencing. J. Biotechnol. 322: 21-28. https://doi.org/10.1016/j.jbiotec.2020.07.006
  13. von Graevenitz A, Bowman J, Del Notaro C, Ritzler M. 2000. Human infection with Halomonas venusta following fish bite. J. Clin. Microbiol. 38: 3123-3124. https://doi.org/10.1128/JCM.38.8.3123-3124.2000
  14. Stevens DA, Hamilton JR, Johnson N, Kim KK, Lee J-S. 2009. Halomonas, a newly recognized human pathogen causing infections and contamination in a dialysis center: three new species. Medicine 88: 244-249. https://doi.org/10.1097/MD.0b013e3181aede29
  15. Rawat S. 2015. Food Spoilage: Microorganisms and their prevention. Asian J. Plant Sci. Res. 5: 47-56.
  16. Yang J, Zeng ZH, Yang MJ, Cheng ZX, Peng XX, Li H. 2018. NaCl promotes antibiotic resistance by reducing redox states in Vibrio alginolyticus. Environ. Microbiol. 20: 4022-4036. https://doi.org/10.1111/1462-2920.14443
  17. Hood MI, Jacobs AC, Sayood K, Dunman PM, Skaar EP. 2010. Acinetobacter baumannii increases tolerance to antibiotics in response to monovalent cations. Antimicrob. Agents Chemother. 54: 1029-1041. https://doi.org/10.1128/aac.00963-09
  18. Harrison JP, Angel R, Cockell CS. 2017. Astrobiology as a framework for investigating antibiotic susceptibility: a study of Halomonas hydrothermalis. J. R Soc. Interface 14: 20160942. https://doi.org/10.1098/rsif.2016.0942
  19. Zhu M, Dai X. 2018. High salt cross-protects Escherichia coli from antibiotic treatment through increasing efflux pump expression. mSphere. 3: e00095-18.
  20. Benomar S, Evans KC, Unckless RL, Chandler JR. 2019. Efflux pumps in Chromobacterium species increase antibiotic resistance and promote survival in a coculture competition model. Appl. Environ. Microbiol. 85: e00908-19.
  21. Vieira A, Ramesh A, Seddon AM, Karlyshev AV. 2017. CmeABC multidrug efflux pump contributes to antibiotic resistance and promotes Campylobacterjejuni survival and multiplication in Acanthamoeba polyphaga. Appl. Environ. Microbiol. 83: e01600-17.
  22. Bhatia SK, Lee B-R, Sathiyanarayanan G, Song H-S, Kim J, Jeon J-M, et al. 2016. Medium engineering for enhanced production of undecylprodigiosin antibiotic in Streptomyces coelicolor using oil palm biomass hydrolysate as a carbon source. Bioresour. Technol. 217: 141-149. https://doi.org/10.1016/j.biortech.2016.02.055
  23. Phylactides M. 1997. Molecular biology series 3. Tools of molecular biology: gene cloning. Br. J. Hosp. Med. 57: 49-50.
  24. Kim J, Seo H-M, Bhatia SK, Song H-S, Kim J-H, Jeon J-M, et al. 2017. Production of itaconate by whole-cell bioconversion of citrate mediated by expression of multiple cis-aconitate decarboxylase (cadA) genes in Escherichia coli. Sci. Rep. 7: 39768. https://doi.org/10.1038/srep39768
  25. Moon Y-M, Gurav R, Kim J, Hong Y-G, Bhatia SK, Jung H-R, et al. 2018. Whole-cell immobilization of engineered Escherichia coli JY001 with barium-alginate for itaconic acid production. Biotechnol. Bioprocess Eng. 23: 442-447. https://doi.org/10.1007/s12257-018-0170-3
  26. Jorgensen JH, Turnidge JD. 2015. Susceptibility test methods: dilution and disk diffusion methods, pp. 1253-1273. Manual of Clinical Microbiology, 11th Edition, Ed. American Society of Microbiology
  27. Sleator RD, Hill C. 2002. Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol. Rev. 26: 49-71. https://doi.org/10.1016/S0168-6445(01)00071-7
  28. Leon MJ, Hoffmann T, Sanchez-Porro C, Heider J, Ventosa A, Bremer E. 2018. Compatible solute synthesis and import by the moderate halophile Spiribacter salinus: Physiology and genomics. Front. Microbiol. 9: 108. https://doi.org/10.3389/fmicb.2018.00108
  29. Cummings SP, Gilmour DJ. 1995. The effect of NaCl on the growth of a Halomonas species: accumulation and utilization of compatible solutes. Microbiology 141: 1413-1418. https://doi.org/10.1099/13500872-141-6-1413
  30. Robert H, Le Marrec C, Blanco C, Jebbar M. 2000. Glycine betaine, carnitine, and choline enhance salinity tolerance and prevent the accumulation of sodium to a level inhibiting growth of Tetragenococcus halophila. Appl. Environ. Microbiol. 66: 509-517. https://doi.org/10.1128/AEM.66.2.509-517.2000
  31. Kustos T, Kustos I, Kilar F, Rappai G, Kocsis B. 2003. Effect of antibiotics on cell surface hydrophobicity of bacteria causing orthopedic wound infections. Chemotherapy 49: 237-242. https://doi.org/10.1159/000072447
  32. Hart DJ, Vreeland RH. 1988. Changes in the hydrophobic-hydrophilic cell surface character of Halomonas elongata in response to NaCl. J. Bacteriol. 170: 132-135. https://doi.org/10.1128/jb.170.1.132-135.1988
  33. Wilke MS, Lovering AL, Strynadka NC. 2005. β-Lactam antibiotic resistance: a current structural perspective. Curr. Opin. Microbiol. 8: 525-533. https://doi.org/10.1016/j.mib.2005.08.016
  34. Sykes R, Matthew M. 1976. The β-lactamases of gram-negative bacteria and their role in resistance to β-lactam antibiotics. J. Antimicrob. Chemother. 2: 115-157. https://doi.org/10.1093/jac/2.2.115
  35. Davies J, Wright GD. 1997. Bacterial resistance to aminoglycoside antibiotics. Trends Microbiol. 5: 234-240. https://doi.org/10.1016/S0966-842X(97)01033-0
  36. Delcour AH. 2009. Outer membrane permeability and antibiotic resistance. BBA-Proteins Proteom. 1794: 808-816. https://doi.org/10.1016/j.bbapap.2008.11.005
  37. Mingeot-Leclercq M-P, Decout J-L. 2016. Bacterial lipid membranes as promising targets to fight antimicrobial resistance, molecular foundations and illustration through the renewal of aminoglycoside antibiotics and emergence of amphiphilic aminoglycosides. Med. Chem. Commun. 7: 586-611. https://doi.org/10.1039/C5MD00503E
  38. Hong Y-G, Moon Y-M, Hong J-W, No S-Y, Choi T-R, Jung H-R, et al. 2018. Production of glutaric acid from 5-aminovaleric acid using Escherichia coli whole cell bio-catalyst overexpressing GabTD from Bacillus subtilis. Enzyme Microb. Technol. 118: 57-65. https://doi.org/10.1016/j.enzmictec.2018.07.002