Microfluidic chip and mass spectrometry-based detection of bacterial antimicrobial resistance and study of antimicrobial resistance mechanism

ZHANG Dongxue; QIAO Liang

doi:10.11665/j.issn.1000-5048.2023060203

Journal of China Pharmaceutical University > 2023 > 54(6): 695-705. > DOI: 10.11665/j.issn.1000-5048.2023060203

ZHANG Dongxue, QIAO Liang. Microfluidic chip and mass spectrometry-based detection of bacterial antimicrobial resistance and study of antimicrobial resistance mechanism[J]. Journal of China Pharmaceutical University, 2023, 54(6): 695-705. DOI: 10.11665/j.issn.1000-5048.2023060203

Citation:

PDF (937 KB)

Microfluidic chip and mass spectrometry-based detection of bacterial antimicrobial resistance and study of antimicrobial resistance mechanism

Department of Chemistry, and Institutes of Biomedical Sciences, Fudan University, Shanghai 200433, China

Funds: This study was supported by China Postdoctoral Science Foundation (No.2022M720806)

More Information

Received Date: June 01, 2023
Revised Date: December 12, 2023

Graphical Abstract

Abstract

Abstract

Bacterial antimicrobial resistance (AMR) is a globally serious problem that threatens public health security.Misuse and abuse of antibiotics cannot achieve the effect of treating bacterial infectious diseases, but will trigger the SOS response of bacteria, exacerbating the evolution of bacterial AMR and the spread of resistant bacteria.This article focuses on antibiotic-resistant bacteria, briefly introduces the pathogenesis of bacterial AMR and SOS response, and systematically summarizes the determination and mechanism study of bacterial AMR based on microfluidics and mass spectrometry.This article provides theoretical basis for AMR-related drug target mining and new drug development, aiming to develop new methods for rapid detection of bacterial AMR and new methods for bacteria inhibition, and promote the diagnosis and treatment of clinical bacteria infectious diseases.

FullText(HTML)

References (87)

References

[1]	Alanis AJ. Resistance to antibiotics: are we in the post-antibiotic era?[J]. Arch Med Res, 2005, 36(6): 697-705.
[2]	Deresinski S. Methicillin-resistant Staphylococcus aureus: an evolutionary, epidemiologic, and therapeutic odyssey[J]. Clin Infect Dis, 2005, 40(4): 562-573.
[3]	UNEP. Bracing for Superbugs: Strengthening environmental action in the ‘One Health’ response to antimicrobial resistance [R], 2023.
[4]	Ayobami O, Brinkwirth S, Eckmanns T, et al. Antibiotic resistance in hospital-acquired ESKAPE-E infections in low- and lower-middle-income countries: a systematic review and meta-analysis[J]. Emerg Microbes Infect, 2022, 11(1): 443-451.
[5]	Knobler S, Lemon S, Najafi M, et al. WHO global strategy for containment of antimicrobial resistance: executive summary, 2003.
[6]	O''Neill J. Antimicrobial resistance: tackling a crisis for the health and wealth of nations, the review on antimicrobial resistance [R], 2014.
[7]	Antibiotic resisance threats in the United States [R]: CDC Centers for Disease Control and Prevention, Department of Health and Human Services, 2019.
[8]	MacLean RC, San Millan A. The evolution of antibiotic resistance[J]. Science, 2019, 365(6458): 1082-1083.
[9]	Manage PM, Liyanage GY. Antibiotics induced antibacterial resistance[M]//Pharmaceuticals and Personal Care Products: Waste Management and Treatment Technology. Amsterdam: Elsevier, 2019: 429-448.
[10]	Maslowska KH, Makiela-Dzbenska K, Fijalkowska IJ. The SOS system: a complex and tightly regulated response to DNA damage[J]. Environ Mol Mutagen, 2019, 60(4): 368-384.
[11]	Kaushik V, Tiwari M, Tiwari V. Interaction of RecA mediated SOS response with bacterial persistence, biofilm formation, and host response[J]. Int J Biol Macromol, 2022, 217: 931-943.
[12]	Alam MK, Alhhazmi A, DeCoteau JF, et al. RecA inhibitors potentiate antibiotic activity and block evolution of antibiotic resistance[J]. Cell Chem Biol, 2016, 23(3): 381-391.
[13]	Crane JK, Alvarado CL, Sutton MD. Role of the SOS response in the generation of antibiotic resistance in vivo[J]. Antimicrob Agents Chemother, 2021, 65(7): e0001321.
[14]	Mohanraj RS, Mandal J. Azithromycin can induce SOS response and horizontal gene transfer of SXT element in Vibrio cholerae[J]. Mol Biol Rep, 2022, 49(6): 4737-4748.
[15]	Miller C, Thomsen LE, Gaggero C, et al. SOS response induction by beta-lactams and bacterial defense against antibiotic lethality[J]. Science, 2004, 305(5690): 1629-1631.
[16]	Justice SS, Hunstad DA, Cegelski L, et al. Morphological plasticity as a bacterial survival strategy[J]. Nat Rev Microbiol, 2008, 6(2): 162-168.
[17]	Braga PC, Piatti G. Kinetics of filamentation of Escherichia coli induced by different sub-MICs of ceftibuten at different times[J]. Chemotherapy, 1993, 39(4): 272-277.
[18]	Yao ZZ, Kahne D, Kishony R. Distinct single-cell morphological dynamics under beta-lactam antibiotics[J]. Mol Cell, 2012, 48(5): 705-712.
[19]	Bos J, Zhang QC, Vyawahare S, et al. Emergence of antibiotic resistance from multinucleated bacterial filaments[J]. Proc Natl Acad Sci U S A, 2015, 112(1): 178-183.
[20]	Banerjee S, Lo K, Ojkic N, et al. Mechanical feedback promotes bacterial adaptation to antibiotics[J]. Nat Phys, 2021, 17(3): 403-409.
[21]	Patel R. MALDI-TOF MS for the diagnosis of infectious diseases[J]. Clin Chem, 2015, 61(1): 100-111.
[22]	Saffert RT, Cunningham SA, Ihde SM, et al. Comparison of Bruker Biotyper matrix-assisted laser desorption ionization-time of flight mass spectrometer to BD Phoenix automated microbiology system for identification of gram-negative bacilli[J]. J Clin Microbiol, 2011, 49(3): 887-892.
[23]	Zhu YD, Qiao L, Prudent M, et al. Sensitive and fast identification of bacteria in blood samples by immunoaffinity mass spectrometry for quick BSI diagnosis[J]. Chem Sci, 2016, 7(5): 2987-2995.
[24]	Zhu YD, Gasilova N, Jovi? M, et al. Detection of antimicrobial resistance-associated proteins by titanium dioxide-facilitated intact bacteria mass spectrometry[J]. Chem Sci, 2018, 9(8): 2212-2221.
[25]	Zhang Y, Tang Y, Tan CR, et al. Toward nanopore electrospray mass spectrometry: nanopore effects in the analysis of bacteria[J]. ACS Cent Sci, 2020, 6(6): 1001-1008.
[26]	Goodacre R, Heald JK, Kell DB. Characterisation of intact microorganisms using electrospray ionisation mass spectrometry[J]. FEMS Microbiol Lett, 1999, 176(1): 17-24.
[27]	Vaidyanathan S, Rowland JJ, Kell DB, et al. Discrimination of aerobic endospore-forming bacteria via electrospray-lonization mass spectrometry of whole cell suspensions[J]. Anal Chem, 2001, 73(17): 4134-4144.
[28]	Dworzanski JP, Snyder AP, Chen R, et al. Identification of bacteria using tandem mass spectrometry combined with a proteome database and statistical scoring[J]. Anal Chem, 2004, 76(8): 2355-2366.
[29]	Kinter M, Sherman NE. Protein Sequencing and Identification Using Tandem Mass Spectrometry: Kinter/Tandem Mass Spectrometry[M]. Hoboken, NJ, USA: John Wiley & Sons, Inc., 2000.
[30]	Chen CY, Clark CG, Langner S, et al. Detection of antimicrobial resistance using proteomics and the comprehensive antibiotic resistance database: a case study[J]. Proteomics Clin Appl, 2020, 14(4): e1800182.
[31]	Blumenscheit C, Pfeifer Y, Werner G, et al. Unbiased antimicrobial resistance detection from clinical bacterial isolates using proteomics[J]. Anal Chem, 2021, 93(44): 14599-14608.
[32]	Bertini I, Hu XY, Luchinat C. Global metabolomics characterization of bacteria: pre-analytical treatments and profiling[J]. Metabolomics, 2014, 10(2): 241-249.
[33]	Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification[J]. Can J Biochem Physiol, 1959, 37(8): 911-917.
[34]	Eugster MR, Loessner MJ. Rapid analysis of Listeria monocytogenes cell wall teichoic acid carbohydrates by ESI-MS/MS[J]. PLoS One, 2011, 6(6): e21500.
[35]	Chingin K, Liang JC, Chen HW. Direct analysis of in vitro grown microorganisms and mammalian cells by ambient mass spectrometry[J]. RSC Adv, 2014, 4(11): 5768-5781.
[36]	Zhu JJ, Hill JE. Detection of Escherichia coli via VOC profiling using secondary electrospray ionization-mass spectrometry (SESI-MS)[J]. Food Microbiol, 2013, 34(2): 412-417.
[37]	Meetani MA, Shin YS, Zhang SF, et al. Desorption electrospray ionization mass spectrometry of intact bacteria[J]. J Mass Spectrom, 2007, 42(9): 1186-1193.
[38]	Zhang JI, Talaty N, Costa AB, et al. Rapid direct lipid profiling of bacteria using desorption electrospray ionization mass spectrometry[J]. Int J Mass Spectrom, 2011, 301(1/2/3): 37-44.
[39]	Li H, Balan P, Vertes A. Molecular imaging of growth, metabolism, and antibiotic inhibition in bacterial colonies by laser ablation electrospray ionization mass spectrometry[J]. Angew Chem Int Ed Engl, 2016, 55(48): 15035-15039.
[40]	Pierce CY, Barr JR, Cody RB, et al. Ambient generation of fatty acid methyl ester ions from bacterial whole cells by direct analysis in real time (DART) mass spectrometry[J]. Chem Commun, 2007(8): 807-809.
[41]	So PK, Yang BC, Li W, et al. Development of tip-desorption electrospray ionization coupled with ion mobility-mass spectrometry for fast screening of carbapenemase-producing bacteria[J]. Talanta, 2019, 201: 237-244.
[42]	Dean SN, Walsh C, Goodman H, et al. Analysis of mixed biofilm (Staphylococcus aureus and Pseudomonas aeruginosa) by laser ablation electrospray ionization mass spectrometry[J]. Biofouling, 2015, 31(2): 151-161.
[43]	Peng B, Li H, Peng XX. Proteomics approach to understand bacterial antibiotic resistance strategies[J]. Expert Rev Proteomics, 2019, 16(10): 829-839.
[44]	Chua SL, Yam JKH, Hao PL, et al. Selective labelling and eradication of antibiotic-tolerant bacterial populations in Pseudomonas aeruginosa biofilms[J]. Nat Commun, 2016, 7: 10750.
[45]	Hao L, Yang X, Chen HL, et al. Molecular characteristics and quantitative proteomic analysis of Klebsiella pneumoniae strains with carbapenem and colistin resistance[J]. Antibiotics, 2022, 11(10): 1341.
[46]	Sharma D, Garg A, Kumar M, et al. Proteome profiling of carbapenem-resistant K. pneumoniae clinical isolate (NDM-4): exploring the mechanism of resistance and potential drug targets[J]. J Proteomics, 2019, 200: 102-110.
[47]	Monteiro R, Hébraud M, Chafsey I, et al. How different is the proteome of the extended spectrum β-lactamase producing Escherichia coli strains from seagulls of the Berlengas natural reserve of Portugal?[J]. J Proteomics, 2016, 145: 167-176.
[48]	Balboa SJ, Hicks LM. Revealing AMP mechanisms of action through resistance evolution and quantitative proteomics[J]. Methods Enzymol, 2022, 663: 259-271.
[49]	Peng JH, Cao J, Ng FM, et al. Pseudomonas aeruginosa develops Ciprofloxacin resistance from low to high level with distinctive proteome changes[J]. J Proteomics, 2017, 152: 75-87.
[50]	Zampieri M, Zimmermann M, Claassen M, et al. Nontargeted metabolomics reveals the multilevel response to antibiotic perturbations[J]. Cell Rep, 2017, 19(6): 1214-1228.
[51]	Liu JJ, Qi MY, Yuan ZC, et al. Nontargeted metabolomics reveals differences in the metabolite profiling among methicillin-resistant and methicillin-susceptible Staphylococcus aureus in response to antibiotics[J]. Mol Omics, 2022, 18(10): 948-956.
[52]	Aros-Calt S, Muller BH, Boudah S, et al. Annotation of the Staphylococcus aureus metabolome using liquid chromatography coupled to high-resolution mass spectrometry and application to the study of methicillin resistance[J]. J Proteome Res, 2015, 14(11): 4863-4875.
[53]	Li H, Xia X, Li XW, et al. Untargeted metabolomic profiling of amphenicol-resistant Campylobacter jejuni by ultra-high-performance liquid chromatography-mass spectrometry[J]. J Proteome Res, 2015, 14(2): 1060-1068.
[54]	Zhang RT, Qin Q, Liu BH, et al. TiO₂-assisted laser desorption/ionization mass spectrometry for rapid profiling of candidate metabolite biomarkers from antimicrobial-resistant bacteria[J]. Anal Chem, 2018, 90(6): 3863-3870.
[55]	Liu SR, Peng XX, Li H. Metabolic mechanism of ceftazidime resistance in Vibrio alginolyticus[J]. Infect Drug Resist, 2019, 12: 417-429.
[56]	Wright MS, Suzuki Y, Jones MB, et al. Genomic and transcriptomic analyses of colistin-resistant clinical isolates of Klebsiella pneumoniae reveal multiple pathways of resistance[J]. Antimicrob Agents Chemother, 2015, 59(1): 536-543.
[57]	Cai SQ, Zhang KX, Wei F, et al. Differential proteomic and genomic comparison of resistance mechanism of Pseudomonas aeruginosa to cefoperazone sodium/sulbactam sodium[J]. An Acad Bras Cienc, 2022, 94(3): e20211160.
[58]	Foudraine DE, Strepis N, Stingl C, et al. Exploring antimicrobial resistance to beta-lactams, aminoglycosides and fluoroquinolones in E. coli and K. pneumoniae using proteogenomics[J]. Sci Rep, 2021, 11(1): 12472.
[59]	Cheng ZX, Yang MJ, Peng B, et al. The depressed central carbon and energy metabolisms is associated to the acquisition of levofloxacin resistance in Vibrio alginolyticus[J]. J Proteomics, 2018, 181: 83-91.
[60]	Yang Y, Lin Y, Qiao L. Direct MALDI-TOF MS identification of bacterial mixtures[J]. Anal Chem, 2018, 90(17): 10400-10408.
[61]	Ducrée J. Special issue: microfluidic lab-on-a-chip platforms for high-performance diagnostics[J]. Diagnostics, 2012, 2(1): 1.
[62]	Liu JF, Yadavali S, Tsourkas A, et al. Microfluidic diafiltration-on-chip using an integrated magnetic peristaltic micropump[J]. Lab Chip, 2017, 17(22): 3796-3803.
[63]	Ohlsson P, Evander M, Petersson K, et al. Integrated acoustic separation, enrichment, and microchip polymerase chain reaction detection of bacteria from blood for rapid sepsis diagnostics[J]. Anal Chem, 2016, 88(19): 9403-9411.
[64]	Hong SC, Kang JS, Lee JE, et al. Continuous aerosol size separator using inertial microfluidics and its application to airborne bacteria and viruses[J]. Lab Chip, 2015, 15(8): 1889-1897.
[65]	Jing WW, Zhao W, Liu SX, et al. Microfluidic device for efficient airborne bacteria capture and enrichment[J]. Anal Chem, 2013, 85(10): 5255-5262.
[66]	Pereiro I, Bendali A, Tabnaoui S, et al. A new microfluidic approach for the one-step capture, amplification and label-free quantification of bacteria from raw samples[J]. Chem Sci, 2017, 8(2): 1329-1336.
[67]	Kang JH, Super M, Yung CW, et al. An extracorporeal blood-cleansing device for sepsis therapy[J]. Nat Med, 2014, 20(10): 1211-1216.
[68]	Homann AR, Niebling L, Zehnle S, et al. A microfluidic cartridge for fast and accurate diagnosis of Mycobacterium tuberculosis infections on standard laboratory equipment[J]. Lab Chip, 2021, 21(8): 1540-1548.
[69]	Jin JL, Duan LJ, Fu JL, et al. A real-time LAMP-based dual-sample microfluidic chip for rapid and simultaneous detection of multiple waterborne pathogenic bacteria from coastal waters[J]. Anal Methods, 2021, 13(24): 2710-2721.
[70]	Krafft B, Tycova A, Urban RD, et al. Microfluidic device for concentration and SERS-based detection of bacteria in drinking water[J]. Electrophoresis, 2021, 42(1/2): 86-94.
[71]	Li YX, Wang T, Wu JM. Capture and detection of urine bacteria using a microchannel silicon nanowire microfluidic chip coupled with MALDI-TOF MS[J]. Analyst, 2021, 146(4): 1151-1156.
[72]	Bian XJ, Lan Y, Wang B, et al. Microfluidic air sampler for highly efficient bacterial aerosol collection and identification[J]. Anal Chem, 2016, 88(23): 11504-11512.
[73]	Srikanth S, Jayapiriya US, Dubey SK, et al. A lab-on-chip platform for simultaneous culture and electrochemical detection of bacteria[J]. iScience, 2022, 25(11): 105388.
[74]	Xu BL, Du Y, Lin JQ, et al. Simultaneous identification and antimicrobial susceptibility testing of multiple uropathogens on a microfluidic chip with paper-supported cell culture arrays[J]. Anal Chem, 2016, 88(23): 11593-11600.
[75]	Lee WB, Fu CY, Chang WH, et al. A microfluidic device for antimicrobial susceptibility testing based on a broth dilution method[J]. Biosens Bioelectron, 2017, 87: 669-678.
[76]	Ma LY, Petersen M, Lu XN. Identification and antimicrobial susceptibility testing of Campylobacter using a microfluidic lab-on-a-chip device[J]. Appl Environ Microbiol, 2020, 86(9): e00096-e00020.
[77]	Ma LY, He WD, Petersen M, et al. Next-generation antimicrobial resistance surveillance system based on the internet-of-things and microfluidic technique[J]. ACS Sens, 2021, 6(9): 3477-3484.
[78]	Choi J, Yoo J, Lee M, et al. A rapid antimicrobial susceptibility test based on single-cell morphological analysis[J]. Sci Transl Med, 2014, 6(267): 267ra174.
[79]	Song KN, Yu ZQ, Zu XY, et al. Microfluidic chip for detection of drug resistance at the single-cell level[J]. Micromachines, 2022, 14(1): 46.
[80]	Kandavalli V, Karempudi P, Larsson J, et al. Rapid antibiotic susceptibility testing and species identification for mixed samples[J]. Nat Commun, 2022, 13(1): 6215.
[81]	Feng XJ, Liu BF, Li JJ, et al. Advances in coupling microfluidic chips to mass spectrometry[J]. Mass Spectrom Rev, 2015, 34(5): 535-557.
[82]	Jiang Y, Wang PC, Locascio LE, et al. Integrated plastic microfluidic devices with ESI-MS for drug screening and residue analysis[J]. Anal Chem, 2001, 73(9): 2048-2053.
[83]	Lee J, Musyimi HK, Soper SA, et al. Development of an automated digestion and droplet deposition microfluidic chip for MALDI-TOF MS[J]. J Am Soc Mass Spectrom, 2008, 19(7): 964-972.
[84]	Dai YC, Li CY, Yi J, et al. Plasmonic colloidosome-coupled MALDI-TOF MS for bacterial heteroresistance study at single-cell level[J]. Anal Chem, 2020, 92(12): 8051-8057.
[85]	Zhang DX, Zhang YJ, Yin F, et al. Microfluidic filter device coupled mass spectrometry for rapid bacterial antimicrobial resistance analysis[J]. Analyst, 2021, 146(2): 515-520.
[86]	Zhang DX, Yang Y, Qin Q, et al. MALDI-TOF characterization of protein expression mutation during morphological changes of bacteria under the impact of antibiotics[J]. Anal Chem, 2019, 91(3): 2352-2359.
[87]	Zhang DX, Yin F, Qin Q, et al. Molecular responses during bacterial filamentation reveal inhibition methods of drug-resistant bacteria[J]. Proc Natl Acad Sci U S A, 2023, 120(27): e2301170120.

Cited By

Get Citation

PDF

XML

Article views (466) PDF downloads (291)

Turn off MathJax

Article Contents

Abstract

References

Microfluidic chip and mass spectrometry-based detection of bacterial antimicrobial resistance and study of antimicrobial resistance mechanism

Abstract

References

Catalog

Export File

Citation

Format

Content