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Archives of Microbiology

, Volume 201, Issue 9, pp 1259–1275 | Cite as

Proteomics-based discrimination of differentially expressed proteins in antibiotic-sensitive and antibiotic-resistant Salmonella Typhimurium, Klebsiella pneumoniae, and Staphylococcus aureus

  • Md Jalal Uddin
  • Choong Je Ma
  • Jin-Chul Kim
  • Juhee AhnEmail author
Original Paper
  • 122 Downloads

Abstract

This study was designed to compare the differentially expressed proteins between antibiotic-sensitive and antibiotic-resistant Salmonella Typhimurium, Klebsiella pneumonia, and Staphylococcus aureus. The susceptibilities of wild-type (WT), ciprofloxacin (CIP) and/or oxacillin (OXA)-induced, and clinically isolated resistant (CCARM) S. Typhimurium (STWT, STCIP, and STCCARM), K. pneumoniae (KPWT, KPCIP, and KPCCARM), and S. aureus (SAWT, SACIP, SAOXA, and SACCARM) to antibiotics were determined using broth microdilution assay. STCIP was highly resistant to piperacillin (MIC > 512 μg/ml), KPCIP was resistant to chloramphenicol (128 μg/ml) and norfloxacin (16 μg/ml), SACIP was resistant to fluoroquinolones (32 μg/ml), and SAOXA was resistant to ceftriaxone (32 μg/ml). The protein profiles of antibiotic-sensitive and antibiotic-resistant strains were determined using 2-DE analysis followed by LC–MS/MS. The commonly expressed proteins of STWT–STCIP, STWT–STCCARM, KPWT–KPCIP, KPWT–KPCCARM, SAWT–SACIP, SAWT–SAOXA, and SAWT–SACCARM were 763, 677, 677, 469, 261, 259, and 226, respectively. The unique protein spots were observed 57 (6.5%), 80 (11.5%), and 68 (13.9%), respectively, for STCCARM, KPCCARM, and SACCARM. The highly up-regulated protein, PrsA (10-fold), was observed in STCIP resistant to ciprofloxacin (128-fold), levofloxacin (32-fold), norfloxacin (64-fold), and piperacillin (> 16-fold). The up-regulated proteins (YadC, FimA, and RplB) in KPCIP resistant to chloramphenicol (> 32-fold), ciprofloxacin (32-fold), levofloxacin (6-fold), norfloxacin (128-fold), and sparfloxacin (64-fold). AcrB and RpoB were up-regulated in SACCARM resistant to multiple antibiotics. The differentially expressed proteins were related to the antibiotic resistance of STWT, STCIP, STCCARM, KPWT, KPCIP, KPCCARM, SAWT, SACIP, SAOXA, and SACCARM. The resistance-associated proteins could be useful biomarkers for detecting antibiotic-resistant pathogens.

Keywords

Antibiotic resistance Proteome Salmonella Klebsiella Staphylococcus 

Notes

Acknowledgements

This research was supported by a grant of the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare, Republic of Korea (Grant number: HI15C-1798-000016).

Supplementary material

203_2019_1693_MOESM1_ESM.docx (25 kb)
Supplementary material 1 (DOCX 24 kb)
203_2019_1693_MOESM2_ESM.docx (26 kb)
Supplementary material 2 (DOCX 25 kb)
203_2019_1693_MOESM3_ESM.docx (27 kb)
Supplementary material 3 (DOCX 27 kb)

References

  1. Anjum MF (2015) Screening methods for the detection of antimicrobial resistance genes present in bacterial isolates and the microbiota. Future Microbiol 10:317–320CrossRefGoogle Scholar
  2. Anjum MF, Zankari E, Hasman H (2017) Molecular methods for detection of antimicrobial resistance. Microbiol Spectrum.  https://doi.org/10.1128/microbiolspec.ARBA-0011-2017 CrossRefGoogle Scholar
  3. Berkane E, Orlik F, Stegmeier JF, Charbit A, Winterhalter M, Benz R (2006) Interaction of bacteriophage lambda with its cell surface receptor: an in vitro study of binding of the viral tail protein gpJ to LamB (Maltoporin). Biochem 45:2708–2720CrossRefGoogle Scholar
  4. Birošová L, Mikulášová M (2009) Development of triclosan and antibiotic resistance in Salmonella enterica serovar Typhimurium. J Med Microbiol 58:436–441CrossRefGoogle Scholar
  5. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254Google Scholar
  6. Card R, Zhang J, Das P, Cook C, Woodford N, Anjum MF (2013) Evaluation of an expanded microarray for detecting antibiotic resistance genes in a broad range of Gram-negative bacterial pathogens. Antimicrob Agent Chemother 57:458–465CrossRefGoogle Scholar
  7. Chambers HF (1997) Methicillin resistance in staphylococci: molecular and biochemical basis and clinical implications. Clin Microbiol Rev 10:781–791CrossRefGoogle Scholar
  8. Chen B et al (2017) Proteomics progresses in microbial physiology and clinical antimicrobial therapy. Eur J Clin Microbiol Infect Dis 36:403–413CrossRefGoogle Scholar
  9. Cho SY et al (2005) Efficient prefractionation of low-abundance proteins in human plasma and construction of a two-dimensional map. Proteomics 5:3386–3396CrossRefGoogle Scholar
  10. CLSI (2015) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved standard M07-A10Google Scholar
  11. Currie CJ et al (2014) Antibiotic treatment failure in four common infections in UK primary care 1991–2012: longitudinal analysis. Br Med J 349:g5493CrossRefGoogle Scholar
  12. da Costa JP et al (2015) Proteome signatures—How are they obtained and what do they teach us? Appl Microbiol Biotechnol 99:7417–7431CrossRefGoogle Scholar
  13. Dupont M, Dé E, Chollet R, Chevalier J, Pagès J-M (2004) Enterobacter aerogenes OmpX, a cation-selective channel mar- and osmo-regulated. FEBS Lett 569:27–30CrossRefGoogle Scholar
  14. Dupont M, James CE, Chevalier J, Pagès J-M (2007) An early response to environmental stress involves regulation of OmpX and OmpF, two enterobacterial outer membrane pore-forming proteins. Antimicrob Agent Chemother 51:3190–3198CrossRefGoogle Scholar
  15. Enany S, Yoshida Y, Yamamoto T (2014) Exploring extra-cellular proteins in methicillin susceptible and methicillin resistant Staphylococcus aureus by liquid chromatography–tandem mass spectrometry. World J Microbiol Biotechnol 30:1269–1283CrossRefGoogle Scholar
  16. Fehri LF, Sirand-Pugnet P, Gourgues G, Jan G, Wróblewski H, Blanchard A (2005) Resistance to antimicrobial peptides and stress response in Mycoplasma pulmonis. Antimicrob Agent Chemother 49:4154–4165CrossRefGoogle Scholar
  17. Fernández M, Rodríguez-Falcón M, Chiva C, Pachón J, Andreu D, Rivas L (2009) The cost of resistance to colistin in Acinetobacter baumannii: a proteomic perspective. Proteomics 9:1632–1645CrossRefGoogle Scholar
  18. Ferri M, Ranucci E, Romagnoli P, Giaccone V (2017) Antimicrobial resistance: a global emerging threat to public health systems. Crit Rev Food Sci Nutr 57:2857–2876CrossRefGoogle Scholar
  19. Friedrich T et al (2010) High-throughput microarray technology in diagnostics of enterobacteria based on genome-wide probe selection and regression analysis. BMC Genom 11(1):591CrossRefGoogle Scholar
  20. Glanzmann P, Gustafson J, Komatsuzawa H, Ohta K, Berger-Bächi B (1999) glmM Operon and methicillin-resistant glmM suppressor mutants in Staphylococcus aureus. Antimicrob Agent Chemother 43:240–245CrossRefGoogle Scholar
  21. Halsey TA, Vazquez-Torres A, Gravdahl DJ, Fang FC, Libby SJ (2004) The ferritin-like Dps protein is required for Salmonella enterica serovar Typhimurium oxidative stress resistance and virulence. Infect Immun 72:1155–1158CrossRefGoogle Scholar
  22. Hao H, Dai M, Wang Y, Huang L, Yuan Z (2012) Key genetic elements and regulation systems in methicillin-resistant Staphylococcus aureus. Future Microbiol 7:1315–1329CrossRefGoogle Scholar
  23. Hyyryläinen HL et al (2010) Penicillin-binding protein folding is dependent on the PrsA peptidyl-prolyl cis-trans isomerase in Bacillus subtilis. Mol Microbiol 77:108–127CrossRefGoogle Scholar
  24. Igarashi K, Kashiwagi K (1999) Polyamine transport in bacteria and yeast. Biochem J 344:633–642CrossRefGoogle Scholar
  25. Jones MM et al (2014) Role of the oligopeptide permease ABC transporter of Moraxella catarrhalis in nutrient acquisition and persistence in the respiratory tract. Infect Immun 82:4758–4766CrossRefGoogle Scholar
  26. Jousselin A, Renzoni A, Andrey DO, Monod A, Lew DP, Kelley WL (2012) The posttranslocational chaperone lipoprotein PrsA is involved in both glycopeptide and oxacillin resistance in Staphylococcus aureus. Antimicrob Agent Chemother 56:3629–3640CrossRefGoogle Scholar
  27. Kim S, Kim H, Reuhs BL, Mauer LJ (2006) Differentiation of outer membrane proteins from Salmonella enterica serotypes using fourier transform infrared spectroscopy and chemometrics. Lett Appl Microbiol 42:229–234CrossRefGoogle Scholar
  28. Kim J, Jo A, Ding T, Lee H-Y, Ahn J (2016) Assessment of altered binding specificity of bacteriophage for ciprofloxacin-induced antibiotic-resistant Salmonella typhimurium. Arch Microbiol 198:521–529CrossRefGoogle Scholar
  29. Kumar S, Mukherjee MM, Varela MF (2013) Modulation of bacterial Multidrug resistance efflux pumps of the major facilitator superfamily. Int J Bacteriol 2013:204141CrossRefGoogle Scholar
  30. Laxminarayan R, Chaudhury RR (2016) Antibiotic resistance in India: drivers and opportunities for action. PLOS Med 13:e1001974CrossRefGoogle Scholar
  31. Lee J, Kim K-Y, Lee J, Paik Y-K (2010) Regulation of dauer formation by O-GlcNAcylation in Caenorhabditis elegans. J Biol Chem 285:2930–2939CrossRefGoogle Scholar
  32. Lee C-R, Lee JH, Park KS, Jeong BC, Lee SH (2015) Quantitative proteomic view associated with resistance to clinically important antibiotics in Gram-positive bacteria: a systematic review. Front Microbiol 6:828PubMedPubMedCentralGoogle Scholar
  33. Lima TB et al (2013) Bacterial resistance mechanism: what proteomics can elucidate. FASEB J 27(4):1291–1303CrossRefGoogle Scholar
  34. Lowy FD (2003) Antimicrobial resistance: the example of Staphylococcus aureus. J Clin Investig 111:1265–1273CrossRefGoogle Scholar
  35. Moran RA, Anantham S, Holt KE, Hall RM (2017) Prediction of antibiotic resistance from antibiotic resistance genes detected in antibiotic-resistant commensal Escherichia coli using PCR or WGS. J Antimicrob Chemother 72:700–704PubMedGoogle Scholar
  36. Morita Y, Tomida J, Kawamura Y (2014) Response of Pseudomonas aeroginosa to antimicrobials. Front Microbiol 8:e442Google Scholar
  37. Moussatova A, Kandt C, O’Mara ML, Tieleman DP (2008) ATP-binding cassette transporters in Escherichia coli. Biochim Biophys Acta Biomembr 1778:1757–1771CrossRefGoogle Scholar
  38. Muroi M, Shima K, Igarashi M, Nakagawa Y, Tanamoto K-i (2012) Application of matrix-assisted laser desorption ionization-time of flight mass spectrometry for discrimination of laboratory-derived antibiotic-resistant bacteria. Biol Pharmaceut Bull 35:1841–1845CrossRefGoogle Scholar
  39. Nikaido H (2009) Multidrug resistance in bacteria. Ann Rev Biochem 78:119–146CrossRefGoogle Scholar
  40. Park AJ, Krieger JR, Khursigara CM (2016) Survival proteomes: the emerging proteotype of antimicrobial resistance. FEMS Microbiol Rev 40:323–342CrossRefGoogle Scholar
  41. Peng B et al (2017) Outer membrane proteins form specific patterns in antibiotic-resistant Edwadsiella tarda. Front Microbiol 8:e69Google Scholar
  42. Pieper R et al (2006) Comparative proteomic analysis of Staphylococcus aureus strains with differences in resistance to the cell wall-targeting antibiotic vancomycin. Proteomics 6:4246–4258CrossRefGoogle Scholar
  43. Pinho MG, de Lencastre H, Tomasz A (2001) An acquired and a native penicillin-binding protein cooperate in building the cell wall of drug-resistant staphylococci. Proc Nat Acad Sci 98:10886–10891CrossRefGoogle Scholar
  44. Rakhuba DV, Kolomiets EI, Dey ES, Novik GI (2010) Bacteriophage receptors, mechanisms of phage adsorption and penetration into host cell. Polish J Microbiol 59:145–155Google Scholar
  45. Rumbo C et al (2013) Contribution of efflux pumps, porins, and β-lactamases to multidrug resistance in clinical isolates of Acinetobacter baumannii. Antimicrob Agent Chemother 57:5247–5257CrossRefGoogle Scholar
  46. Strauss C, Endimiani A, Perreten V (2015) A novel universal DNA labeling and amplification system for rapid microarray-based detection of 117 antibiotic resistance genes in Gram-positive bacteria. J Microbiol Method 108:25–30CrossRefGoogle Scholar
  47. Susin MF, Baldini RL, Gueiros-Filho F, Gomes SL (2006) GroES/GroEL and DnaK/DnaJ have distinct roles in stress responses and during cell cycle progression in Caulobacter crescentus. J Bacteriol 188:8044–8053CrossRefGoogle Scholar
  48. van Duin D, Paterson D (2016) Multidrug resistant bacteria in the community: trends and lessons learned. Infect Dis Clin North Am 30:377–390CrossRefGoogle Scholar
  49. Vranakis I et al (2014) Proteome studies of bacterial antibiotic resistance mechanisms. J Proteom 97:88–99CrossRefGoogle Scholar
  50. Webber MA et al (2009) The global consequence of disruption of the AcrAB-TolC efflux pump in Salmonella enterica includes reduced expression of SPI-1 and other attributes required to infect the host. J Bacteriol 191:4276–4285CrossRefGoogle Scholar
  51. Webber MA et al (2013) Clinically relevant mutant DNA gyrase alters supercoiling, changes the transcriptome, and confers multidrug resistance. mBio 4:e00273-13CrossRefGoogle Scholar
  52. Weiller GF, Caraux G, Sylvester N (2004) The modal distribution of protein isoelectric points reflects amino acid properties rather than sequence evolution. Proteomics 4:943–949CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Medical Biomaterials Engineering and Institute of Bioscience and BiotechnologyKangwon National UniversityChuncheonRepublic of Korea

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