Exploring antimicrobial resistance to beta-lactams, aminoglycosides and fluoroquinolones in E. coli and K. pneumoniae using proteogenomics

Antimicrobial resistance is mostly studied by means of phenotypic growth inhibition determinations, in combination with PCR confirmations or further characterization by means of whole genome sequencing (WGS). However, the actual proteins that cause resistance such as enzymes and a lack of porins can...

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Vydané v:Scientific reports Ročník 11; číslo 1; s. 12472 - 18
Hlavní autori: Foudraine, Dimard E., Strepis, Nikolaos, Stingl, Christoph, ten Kate, Marian T., Verbon, Annelies, Klaassen, Corné H. W., Goessens, Wil H. F., Luider, Theo M., Dekker, Lennard J. M.
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: London Nature Publishing Group UK 14.06.2021
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Abstract Antimicrobial resistance is mostly studied by means of phenotypic growth inhibition determinations, in combination with PCR confirmations or further characterization by means of whole genome sequencing (WGS). However, the actual proteins that cause resistance such as enzymes and a lack of porins cannot be detected by these methods. Improvements in liquid chromatography (LC) and mass spectrometry (MS) enabled easier and more comprehensive proteome analysis. In the current study, susceptibility testing, WGS and MS are combined into a multi-omics approach to analyze resistance against frequently used antibiotics within the beta-lactam, aminoglycoside and fluoroquinolone group in E. coli and K. pneumoniae . Our aim was to study which currently known mechanisms of resistance can be detected at the protein level using liquid chromatography–mass spectrometry (LC–MS/MS) and to assess whether these could explain beta-lactam, aminoglycoside, and fluoroquinolone resistance in the studied isolates. Furthermore, we aimed to identify significant protein to resistance correlations which have not yet been described before and to correlate the abundance of different porins in relation to resistance to different classes of antibiotics. Whole genome sequencing, high-resolution LC–MS/MS and antimicrobial susceptibility testing by broth microdilution were performed for 187 clinical E. coli and K. pneumoniae isolates. Resistance genes and proteins were identified using the Comprehensive Antibiotic Resistance Database (CARD). All proteins were annotated using the NCBI RefSeq database and Prokka. Proteins of small spectrum beta-lactamases, extended spectrum beta-lactamases, AmpC beta-lactamases, carbapenemases, and proteins of 16S ribosomal RNA methyltransferases and aminoglycoside acetyltransferases can be detected in E. coli and K. pneumoniae by LC–MS/MS. The detected mechanisms matched with the phenotype in the majority of isolates. Differences in the abundance and the primary structure of other proteins such as porins also correlated with resistance. LC–MS/MS is a different and complementary method which can be used to characterize antimicrobial resistance in detail as not only the primary resistance causing mechanisms are detected, but also secondary enhancing resistance mechanisms.
AbstractList Antimicrobial resistance is mostly studied by means of phenotypic growth inhibition determinations, in combination with PCR confirmations or further characterization by means of whole genome sequencing (WGS). However, the actual proteins that cause resistance such as enzymes and a lack of porins cannot be detected by these methods. Improvements in liquid chromatography (LC) and mass spectrometry (MS) enabled easier and more comprehensive proteome analysis. In the current study, susceptibility testing, WGS and MS are combined into a multi-omics approach to analyze resistance against frequently used antibiotics within the beta-lactam, aminoglycoside and fluoroquinolone group in E. coli and K. pneumoniae. Our aim was to study which currently known mechanisms of resistance can be detected at the protein level using liquid chromatography-mass spectrometry (LC-MS/MS) and to assess whether these could explain beta-lactam, aminoglycoside, and fluoroquinolone resistance in the studied isolates. Furthermore, we aimed to identify significant protein to resistance correlations which have not yet been described before and to correlate the abundance of different porins in relation to resistance to different classes of antibiotics. Whole genome sequencing, high-resolution LC-MS/MS and antimicrobial susceptibility testing by broth microdilution were performed for 187 clinical E. coli and K. pneumoniae isolates. Resistance genes and proteins were identified using the Comprehensive Antibiotic Resistance Database (CARD). All proteins were annotated using the NCBI RefSeq database and Prokka. Proteins of small spectrum beta-lactamases, extended spectrum beta-lactamases, AmpC beta-lactamases, carbapenemases, and proteins of 16S ribosomal RNA methyltransferases and aminoglycoside acetyltransferases can be detected in E. coli and K. pneumoniae by LC-MS/MS. The detected mechanisms matched with the phenotype in the majority of isolates. Differences in the abundance and the primary structure of other proteins such as porins also correlated with resistance. LC-MS/MS is a different and complementary method which can be used to characterize antimicrobial resistance in detail as not only the primary resistance causing mechanisms are detected, but also secondary enhancing resistance mechanisms.Antimicrobial resistance is mostly studied by means of phenotypic growth inhibition determinations, in combination with PCR confirmations or further characterization by means of whole genome sequencing (WGS). However, the actual proteins that cause resistance such as enzymes and a lack of porins cannot be detected by these methods. Improvements in liquid chromatography (LC) and mass spectrometry (MS) enabled easier and more comprehensive proteome analysis. In the current study, susceptibility testing, WGS and MS are combined into a multi-omics approach to analyze resistance against frequently used antibiotics within the beta-lactam, aminoglycoside and fluoroquinolone group in E. coli and K. pneumoniae. Our aim was to study which currently known mechanisms of resistance can be detected at the protein level using liquid chromatography-mass spectrometry (LC-MS/MS) and to assess whether these could explain beta-lactam, aminoglycoside, and fluoroquinolone resistance in the studied isolates. Furthermore, we aimed to identify significant protein to resistance correlations which have not yet been described before and to correlate the abundance of different porins in relation to resistance to different classes of antibiotics. Whole genome sequencing, high-resolution LC-MS/MS and antimicrobial susceptibility testing by broth microdilution were performed for 187 clinical E. coli and K. pneumoniae isolates. Resistance genes and proteins were identified using the Comprehensive Antibiotic Resistance Database (CARD). All proteins were annotated using the NCBI RefSeq database and Prokka. Proteins of small spectrum beta-lactamases, extended spectrum beta-lactamases, AmpC beta-lactamases, carbapenemases, and proteins of 16S ribosomal RNA methyltransferases and aminoglycoside acetyltransferases can be detected in E. coli and K. pneumoniae by LC-MS/MS. The detected mechanisms matched with the phenotype in the majority of isolates. Differences in the abundance and the primary structure of other proteins such as porins also correlated with resistance. LC-MS/MS is a different and complementary method which can be used to characterize antimicrobial resistance in detail as not only the primary resistance causing mechanisms are detected, but also secondary enhancing resistance mechanisms.
Antimicrobial resistance is mostly studied by means of phenotypic growth inhibition determinations, in combination with PCR confirmations or further characterization by means of whole genome sequencing (WGS). However, the actual proteins that cause resistance such as enzymes and a lack of porins cannot be detected by these methods. Improvements in liquid chromatography (LC) and mass spectrometry (MS) enabled easier and more comprehensive proteome analysis. In the current study, susceptibility testing, WGS and MS are combined into a multi-omics approach to analyze resistance against frequently used antibiotics within the beta-lactam, aminoglycoside and fluoroquinolone group in E. coli and K. pneumoniae. Our aim was to study which currently known mechanisms of resistance can be detected at the protein level using liquid chromatography–mass spectrometry (LC–MS/MS) and to assess whether these could explain beta-lactam, aminoglycoside, and fluoroquinolone resistance in the studied isolates. Furthermore, we aimed to identify significant protein to resistance correlations which have not yet been described before and to correlate the abundance of different porins in relation to resistance to different classes of antibiotics. Whole genome sequencing, high-resolution LC–MS/MS and antimicrobial susceptibility testing by broth microdilution were performed for 187 clinical E. coli and K. pneumoniae isolates. Resistance genes and proteins were identified using the Comprehensive Antibiotic Resistance Database (CARD). All proteins were annotated using the NCBI RefSeq database and Prokka. Proteins of small spectrum beta-lactamases, extended spectrum beta-lactamases, AmpC beta-lactamases, carbapenemases, and proteins of 16S ribosomal RNA methyltransferases and aminoglycoside acetyltransferases can be detected in E. coli and K. pneumoniae by LC–MS/MS. The detected mechanisms matched with the phenotype in the majority of isolates. Differences in the abundance and the primary structure of other proteins such as porins also correlated with resistance. LC–MS/MS is a different and complementary method which can be used to characterize antimicrobial resistance in detail as not only the primary resistance causing mechanisms are detected, but also secondary enhancing resistance mechanisms.
Antimicrobial resistance is mostly studied by means of phenotypic growth inhibition determinations, in combination with PCR confirmations or further characterization by means of whole genome sequencing (WGS). However, the actual proteins that cause resistance such as enzymes and a lack of porins cannot be detected by these methods. Improvements in liquid chromatography (LC) and mass spectrometry (MS) enabled easier and more comprehensive proteome analysis. In the current study, susceptibility testing, WGS and MS are combined into a multi-omics approach to analyze resistance against frequently used antibiotics within the beta-lactam, aminoglycoside and fluoroquinolone group in E. coli and K. pneumoniae . Our aim was to study which currently known mechanisms of resistance can be detected at the protein level using liquid chromatography–mass spectrometry (LC–MS/MS) and to assess whether these could explain beta-lactam, aminoglycoside, and fluoroquinolone resistance in the studied isolates. Furthermore, we aimed to identify significant protein to resistance correlations which have not yet been described before and to correlate the abundance of different porins in relation to resistance to different classes of antibiotics. Whole genome sequencing, high-resolution LC–MS/MS and antimicrobial susceptibility testing by broth microdilution were performed for 187 clinical E. coli and K. pneumoniae isolates. Resistance genes and proteins were identified using the Comprehensive Antibiotic Resistance Database (CARD). All proteins were annotated using the NCBI RefSeq database and Prokka. Proteins of small spectrum beta-lactamases, extended spectrum beta-lactamases, AmpC beta-lactamases, carbapenemases, and proteins of 16S ribosomal RNA methyltransferases and aminoglycoside acetyltransferases can be detected in E. coli and K. pneumoniae by LC–MS/MS. The detected mechanisms matched with the phenotype in the majority of isolates. Differences in the abundance and the primary structure of other proteins such as porins also correlated with resistance. LC–MS/MS is a different and complementary method which can be used to characterize antimicrobial resistance in detail as not only the primary resistance causing mechanisms are detected, but also secondary enhancing resistance mechanisms.
Abstract Antimicrobial resistance is mostly studied by means of phenotypic growth inhibition determinations, in combination with PCR confirmations or further characterization by means of whole genome sequencing (WGS). However, the actual proteins that cause resistance such as enzymes and a lack of porins cannot be detected by these methods. Improvements in liquid chromatography (LC) and mass spectrometry (MS) enabled easier and more comprehensive proteome analysis. In the current study, susceptibility testing, WGS and MS are combined into a multi-omics approach to analyze resistance against frequently used antibiotics within the beta-lactam, aminoglycoside and fluoroquinolone group in E. coli and K. pneumoniae. Our aim was to study which currently known mechanisms of resistance can be detected at the protein level using liquid chromatography–mass spectrometry (LC–MS/MS) and to assess whether these could explain beta-lactam, aminoglycoside, and fluoroquinolone resistance in the studied isolates. Furthermore, we aimed to identify significant protein to resistance correlations which have not yet been described before and to correlate the abundance of different porins in relation to resistance to different classes of antibiotics. Whole genome sequencing, high-resolution LC–MS/MS and antimicrobial susceptibility testing by broth microdilution were performed for 187 clinical E. coli and K. pneumoniae isolates. Resistance genes and proteins were identified using the Comprehensive Antibiotic Resistance Database (CARD). All proteins were annotated using the NCBI RefSeq database and Prokka. Proteins of small spectrum beta-lactamases, extended spectrum beta-lactamases, AmpC beta-lactamases, carbapenemases, and proteins of 16S ribosomal RNA methyltransferases and aminoglycoside acetyltransferases can be detected in E. coli and K. pneumoniae by LC–MS/MS. The detected mechanisms matched with the phenotype in the majority of isolates. Differences in the abundance and the primary structure of other proteins such as porins also correlated with resistance. LC–MS/MS is a different and complementary method which can be used to characterize antimicrobial resistance in detail as not only the primary resistance causing mechanisms are detected, but also secondary enhancing resistance mechanisms.
ArticleNumber 12472
Author Goessens, Wil H. F.
Foudraine, Dimard E.
Stingl, Christoph
Verbon, Annelies
ten Kate, Marian T.
Strepis, Nikolaos
Klaassen, Corné H. W.
Luider, Theo M.
Dekker, Lennard J. M.
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PublicationCentury 2000
PublicationDate 2021-06-14
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PublicationDate_xml – month: 06
  year: 2021
  text: 2021-06-14
  day: 14
PublicationDecade 2020
PublicationPlace London
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PublicationTitle Scientific reports
PublicationTitleAbbrev Sci Rep
PublicationTitleAlternate Sci Rep
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Publisher Nature Publishing Group UK
Nature Publishing Group
Nature Portfolio
Publisher_xml – name: Nature Publishing Group UK
– name: Nature Publishing Group
– name: Nature Portfolio
References van der PuttenBCLQuantifying the contribution of four resistance mechanisms to ciprofloxacin MIC in Escherichia coli: A systematic reviewJ. Antimicrob. Chemother.2019742983103035733910.1093/jac/dky4171:CAS:528:DC%2BC1MXitVans73L
HassingRJDetection of amino acid substitutions in the GyrA protein of fluoroquinolone-resistant typhoidal Salmonella isolates using high-resolution mass spectrometryInt. J. Antimicrob. Agents2016473513561:CAS:528:DC%2BC28XksVWmsbo%3D2713219110.1016/j.ijantimicag.2016.01.018
MasiMRefregiersMPosKMPagesJMMechanisms of envelope permeability and antibiotic influx and efflux in Gram-negative bacteriaNat. Microbiol.20172170011:CAS:528:DC%2BC2sXkvFyqtLs%3D2822498910.1038/nmicrobiol.2017.1
KeaseySLDecreased antibiotic susceptibility driven by global remodeling of the Klebsiella pneumoniae proteomeMol. Cell Proteom.2019186576681:CAS:528:DC%2BC1MXot1Gktrc%3D10.1074/mcp.RA118.000739
R Core TeamA Language and Environment for Statistical Computing2020R Foundation for Statistical Computing
AhmedMAcute cholangitis—An updateWorld J. Gastrointest. Pathophysiol.201891729487761582369810.4291/wjgp.v9.i1.1
WelkerMvan BelkumAOne system for all: Is mass spectrometry a future alternative for conventional antibiotic susceptibility testing?Front. Microbiol.201910271131849870690196510.3389/fmicb.2019.02711
JacobyGABeta-lactamase nomenclatureAntimicrob. Agents Chemother.200650112311291:CAS:528:DC%2BD28XjvFOktbk%3D16569819142697310.1128/AAC.50.4.1123-1129.2006
HebertASThe one hour yeast proteomeMol. Cell Proteom.2014133393471:CAS:528:DC%2BC2cXitlSksg%3D%3D10.1074/mcp.M113.034769
TripHSimultaneous identification of multiple beta-lactamases in Acinetobacter baumannii in relation to carbapenem and ceftazidime resistance, using liquid chromatography-tandem mass spectrometryJ. Clin. Microbiol.201553192719301:CAS:528:DC%2BC2MXpsFGit7o%3D25788550443207110.1128/JCM.00620-15
LarkinMAClustal W and Clustal X version 2.0Bioinformatics200723294729481:CAS:528:DC%2BD2sXhtlaqsL%2FM10.1093/bioinformatics/btm40417846036
FoudraineDEAccurate detection of the four most prevalent carbapenemases in E. coli and K. pneumoniae by high-resolution mass spectrometryFront. Microbiol.201910276031849899690190710.3389/fmicb.2019.02760
CharretierYSchrenzelJMass spectrometry methods for predicting antibiotic resistanceProteom. Clin. Appl.2016109649811:CAS:528:DC%2BC28Xht1CrtLjK10.1002/prca.201600041
ChangCJDiagnosis of beta-lactam resistance in Acinetobacter baumannii using shotgun proteomics and LC-nano-electrospray ionization ion trap mass spectrometryAnal. Chem.201385280228081:CAS:528:DC%2BC3sXhvVyntb4%3D2337400810.1021/ac303326a
VergalliJPorins and small-molecule translocation across the outer membrane of Gram-negative bacteriaNat. Rev. Microbiol.2020181641761:CAS:528:DC%2BC1MXit1Ors7zL3179236510.1038/s41579-019-0294-2
CorreiaSPoetaPHebraudMCapeloJLIgrejasGMechanisms of quinolone action and resistance: Where do we stand?J. Med. Microbiol.2017665515591:CAS:528:DC%2BC1MXosFCksQ%3D%3D2850492710.1099/jmm.0.000475
DoiYWachinoJIArakawaYAminoglycoside resistance: The emergence of acquired 16S ribosomal RNA methyltransferasesInfect. Dis. Clin. N. Am.20163052353710.1016/j.idc.2016.02.011
CassiniAAttributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: A population-level modelling analysisLancet Infect. Dis.201919566630409683630048110.1016/S1473-3099(18)30605-4
LivermoreDMbeta-Lactamases in laboratory and clinical resistanceClin. Microbiol. Rev.199585575841:CAS:528:DyaK2MXpt12jtLs%3D866547017287610.1128/CMR.8.4.557
WHO. Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. https://www.who.int/medicines/publications/global-priority-list-antibiotic-resistant-bacteria/en/ (2017).
BabiniGSLivermoreDMAre SHV beta-lactamases universal in Klebsiella pneumoniae?Antimicrob. Agents Chemother.20004422301:CAS:528:DC%2BD3cXltlSht70%3D110234449004910.1128/AAC.44.8.2230-2230.2000
WickRRJuddLMGorrieCLHoltKEUnicycler: Resolving bacterial genome assemblies from short and long sequencing readsPLoS Comput. Biol.201713e10055952017PLSCB..13E5595W28594827548114710.1371/journal.pcbi.10055951:CAS:528:DC%2BC2sXhs1agurrF
SoufiBKrugKHarstAMacekBCharacterization of the E. coli proteome and its modifications during growth and ethanol stressFront. Microbiol.2015610325741329433235310.3389/fmicb.2015.00103
StephensCF plasmids are the major carriers of antibiotic resistance genes in human-associated commensal Escherichia colimSphere20205e00709-2032759337740707110.1128/mSphere.00709-20
SeemannTProkka: Rapid prokaryotic genome annotationBioinformatics201430206820691:CAS:528:DC%2BC2cXhtFCrtLjI2464206310.1093/bioinformatics/btu153
Perez-RiverolYThe PRIDE database and related tools and resources in 2019: Improving support for quantification dataNucleic Acids Res.201947D442D4501:CAS:528:DC%2BC1MXhs1GqtrzK3039528910.1093/nar/gky1106
CudicESurmannKPanasiaGHammerEHunkeSThe role of the two-component systems Cpx and Arc in protein alterations upon gentamicin treatment in Escherichia coliBMC Microbiol.20171719728923010560449710.1186/s12866-017-1100-91:CAS:528:DC%2BC1cXitVOgsLjK
StoesserNPredicting antimicrobial susceptibilities for Escherichia coli and Klebsiella pneumoniae isolates using whole genomic sequence dataJ. Antimicrob. Chemother.201368223422441:CAS:528:DC%2BC3sXhvVKns7zI23722448377273910.1093/jac/dkt180
Consortium, C.R.Prediction of Susceptibility to first-line tuberculosis drugs by DNA sequencingN. Engl. J. Med.20183791403141510.1056/NEJMoa1800474
WuSZhuZFuLNiuBLiWWebMGA: A customizable web server for fast metagenomic sequence analysisBMC Genom.20111244410.1186/1471-2164-12-444
WHO. Antimicrobial resistance: Global report on surveillance 2014. https://www.who.int/drugresistance/documents/surveillancereport/en/ (2014).
TatusovRLGalperinMYNataleDAKooninEVThe COG database: A tool for genome-scale analysis of protein functions and evolutionNucleic Acids Res.20002833361:CAS:528:DC%2BD3cXhvVGqu7w%3D1059217510239510.1093/nar/28.1.33
SharmaDGargAKumarMRashidFKhanAUDown-regulation of flagellar, fimbriae, and pili proteins in carbapenem-resistant Klebsiella pneumoniae (NDM-4) clinical isolates: A novel linkage to drug resistanceFront. Microbiol.201910286531921045692805110.3389/fmicb.2019.02865
AlcockBPCARD 2020: Antibiotic resistome surveillance with the comprehensive antibiotic resistance databaseNucleic Acids Res.202048D517D5251:CAS:528:DC%2BB3cXhslWltrnK31665441
JacobyGAAmpC beta-lactamasesClin. Microbiol. Rev.2009221611821:CAS:528:DC%2BD1MXnslKrs7Y%3D19136439262063710.1128/CMR.00036-08
van BelkumAInnovative and rapid antimicrobial susceptibility testing systemsNat. Rev. Microbiol.2020182993113205502610.1038/s41579-020-0327-x1:CAS:528:DC%2BB3cXjtFelsL4%3D
Martinez-MartinezLExtended-spectrum beta-lactamases and the permeability barrierClin. Microbiol. Infect.200814Suppl 182891:CAS:528:DC%2BD1cXhtleiur0%3D1815453110.1111/j.1469-0691.2007.01860.x
ChoiULeeCRDistinct roles of outer membrane porins in antibiotic resistance and membrane integrity in Escherichia coliFront. Microbiol.20191095331114568650374610.3389/fmicb.2019.00953
UddinMJMaCJKimJCAhnJProteomics-based discrimination of differentially expressed proteins in antibiotic-sensitive and antibiotic-resistant Salmonella typhimurium, Klebsiella pneumoniae, and Staphylococcus aureusArch. Microbiol.2019201125912751:CAS:528:DC%2BC1MXht1Git7vP3124034210.1007/s00203-019-01693-1
PaltansingSIncreased expression levels of chromosomal AmpC beta-lactamase in clinical Escherichia coli isolates and their effect on susceptibility to extended-spectrum cephalosporinsMicrob. Drug Resist.2015217161:CAS:528:DC%2BC2MXitFyjt7w%3D2518832910.1089/mdr.2014.0108
LauplandKBIncidence of bloodstream infection: A review of population-based studiesClin. Microbiol. Infect.2013194925001:STN:280:DC%2BC3sznt1KqsQ%3D%3D2339863310.1111/1469-0691.12144
RamirezMSTolmaskyMEAminoglycoside modifying enzymesDrug Resist. Updat.2010131511711:CAS:528:DC%2BC3cXhsV2jtL%2FO20833577299259910.1016/j.drup.2010.08.003
SikoraAEStructural and functional insights into the role of BamD and BamE within the beta-barrel assembly machinery in Neisseria gonorrhoeaeJ. Biol. Chem.2018293110611191:CAS:528:DC%2BC1cXhvVert74%3D2922977810.1074/jbc.RA117.000437
Wan Nur IsmahWAKPrediction of fluoroquinolone susceptibility directly from whole-genome sequence data by using liquid chromatography-tandem mass spectrometry to identify mutant genotypesAntimicrob. Agents Chemother.201862e01814-1729263066582610910.1128/AAC.01814-17
National Center for Biotechnology Information (US). BLAST® Command Line Applications User Manual. https://www.ncbi.nlm.nih.gov/books/NBK279684/ (2018).
CheniaHYPillayBPillayDAnalysis of the mechanisms of fluoroquinolone resistance in urinary tract pathogensJ. Antimicrob. Chemother.200658127412781:CAS:528:DC%2BD28Xht1Ogsr7J1704092310.1093/jac/dkl404
GordonNCPrediction of Staphylococcus aureus antimicrobial resistance by whole-genome sequencingJ. Clin. Microbiol.201452118211911:CAS:528:DC%2BC2cXhsVGksLzO24501024399349110.1128/JCM.03117-13
MoriHKondoAOhshimaAOguraTHiragaSStructure and function of the F plasmid genes essential for partitioningJ. Mol. Biol.19861921151:CAS:528:DyaL2sXivVejuw%3D%3D302939010.1016/0022-2836(86)90459-6
D Sharma (91905_CR36) 2019; 10
GA Jacoby (91905_CR19) 2009; 22
A van Belkum (91905_CR17) 2020; 18
BCL van der Putten (91905_CR24) 2019; 74
BP Alcock (91905_CR43) 2020; 48
91905_CR1
GA Jacoby (91905_CR22) 2006; 50
H Trip (91905_CR14) 2015; 53
KB Laupland (91905_CR3) 2013; 19
91905_CR5
S Paltansing (91905_CR40) 2015; 21
Y Charretier (91905_CR9) 2016; 10
DM Livermore (91905_CR20) 1995; 8
HY Chenia (91905_CR28) 2006; 58
U Choi (91905_CR29) 2019; 10
RJ Hassing (91905_CR26) 2016; 47
H Mori (91905_CR32) 1986; 192
SL Keasey (91905_CR37) 2019; 18
M Ahmed (91905_CR2) 2018; 9
NC Gordon (91905_CR8) 2014; 52
RL Tatusov (91905_CR18) 2000; 28
B Soufi (91905_CR35) 2015; 6
WAK Wan Nur Ismah (91905_CR10) 2018; 62
J Vergalli (91905_CR27) 2020; 18
S Correia (91905_CR31) 2017; 66
Consortium, C.R. (91905_CR7) 2018; 379
MS Ramirez (91905_CR21) 2010; 13
A Cassini (91905_CR4) 2019; 19
CJ Chang (91905_CR13) 2013; 85
91905_CR46
DE Foudraine (91905_CR16) 2019; 10
E Cudic (91905_CR39) 2017; 17
T Seemann (91905_CR42) 2014; 30
MA Larkin (91905_CR47) 2007; 23
N Stoesser (91905_CR6) 2013; 68
M Masi (91905_CR30) 2017; 2
M Welker (91905_CR15) 2019; 10
GS Babini (91905_CR25) 2000; 44
MJ Uddin (91905_CR38) 2019; 201
S Wu (91905_CR44) 2011; 12
C Stephens (91905_CR33) 2020; 5
RR Wick (91905_CR41) 2017; 13
AE Sikora (91905_CR34) 2018; 293
AS Hebert (91905_CR12) 2014; 13
L Martinez-Martinez (91905_CR11) 2008; 14
Y Doi (91905_CR23) 2016; 30
Y Perez-Riverol (91905_CR48) 2019; 47
R Core Team (91905_CR45) 2020
References_xml – reference: FoudraineDEAccurate detection of the four most prevalent carbapenemases in E. coli and K. pneumoniae by high-resolution mass spectrometryFront. Microbiol.201910276031849899690190710.3389/fmicb.2019.02760
– reference: WickRRJuddLMGorrieCLHoltKEUnicycler: Resolving bacterial genome assemblies from short and long sequencing readsPLoS Comput. Biol.201713e10055952017PLSCB..13E5595W28594827548114710.1371/journal.pcbi.10055951:CAS:528:DC%2BC2sXhs1agurrF
– reference: SharmaDGargAKumarMRashidFKhanAUDown-regulation of flagellar, fimbriae, and pili proteins in carbapenem-resistant Klebsiella pneumoniae (NDM-4) clinical isolates: A novel linkage to drug resistanceFront. Microbiol.201910286531921045692805110.3389/fmicb.2019.02865
– reference: CheniaHYPillayBPillayDAnalysis of the mechanisms of fluoroquinolone resistance in urinary tract pathogensJ. Antimicrob. Chemother.200658127412781:CAS:528:DC%2BD28Xht1Ogsr7J1704092310.1093/jac/dkl404
– reference: CorreiaSPoetaPHebraudMCapeloJLIgrejasGMechanisms of quinolone action and resistance: Where do we stand?J. Med. Microbiol.2017665515591:CAS:528:DC%2BC1MXosFCksQ%3D%3D2850492710.1099/jmm.0.000475
– reference: Consortium, C.R.Prediction of Susceptibility to first-line tuberculosis drugs by DNA sequencingN. Engl. J. Med.20183791403141510.1056/NEJMoa1800474
– reference: LauplandKBIncidence of bloodstream infection: A review of population-based studiesClin. Microbiol. Infect.2013194925001:STN:280:DC%2BC3sznt1KqsQ%3D%3D2339863310.1111/1469-0691.12144
– reference: StoesserNPredicting antimicrobial susceptibilities for Escherichia coli and Klebsiella pneumoniae isolates using whole genomic sequence dataJ. Antimicrob. Chemother.201368223422441:CAS:528:DC%2BC3sXhvVKns7zI23722448377273910.1093/jac/dkt180
– reference: Perez-RiverolYThe PRIDE database and related tools and resources in 2019: Improving support for quantification dataNucleic Acids Res.201947D442D4501:CAS:528:DC%2BC1MXhs1GqtrzK3039528910.1093/nar/gky1106
– reference: AhmedMAcute cholangitis—An updateWorld J. Gastrointest. Pathophysiol.201891729487761582369810.4291/wjgp.v9.i1.1
– reference: CudicESurmannKPanasiaGHammerEHunkeSThe role of the two-component systems Cpx and Arc in protein alterations upon gentamicin treatment in Escherichia coliBMC Microbiol.20171719728923010560449710.1186/s12866-017-1100-91:CAS:528:DC%2BC1cXitVOgsLjK
– reference: LarkinMAClustal W and Clustal X version 2.0Bioinformatics200723294729481:CAS:528:DC%2BD2sXhtlaqsL%2FM10.1093/bioinformatics/btm40417846036
– reference: MasiMRefregiersMPosKMPagesJMMechanisms of envelope permeability and antibiotic influx and efflux in Gram-negative bacteriaNat. Microbiol.20172170011:CAS:528:DC%2BC2sXkvFyqtLs%3D2822498910.1038/nmicrobiol.2017.1
– reference: JacobyGAAmpC beta-lactamasesClin. Microbiol. Rev.2009221611821:CAS:528:DC%2BD1MXnslKrs7Y%3D19136439262063710.1128/CMR.00036-08
– reference: CassiniAAttributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: A population-level modelling analysisLancet Infect. Dis.201919566630409683630048110.1016/S1473-3099(18)30605-4
– reference: RamirezMSTolmaskyMEAminoglycoside modifying enzymesDrug Resist. Updat.2010131511711:CAS:528:DC%2BC3cXhsV2jtL%2FO20833577299259910.1016/j.drup.2010.08.003
– reference: SeemannTProkka: Rapid prokaryotic genome annotationBioinformatics201430206820691:CAS:528:DC%2BC2cXhtFCrtLjI2464206310.1093/bioinformatics/btu153
– reference: AlcockBPCARD 2020: Antibiotic resistome surveillance with the comprehensive antibiotic resistance databaseNucleic Acids Res.202048D517D5251:CAS:528:DC%2BB3cXhslWltrnK31665441
– reference: WHO. Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. https://www.who.int/medicines/publications/global-priority-list-antibiotic-resistant-bacteria/en/ (2017).
– reference: SikoraAEStructural and functional insights into the role of BamD and BamE within the beta-barrel assembly machinery in Neisseria gonorrhoeaeJ. Biol. Chem.2018293110611191:CAS:528:DC%2BC1cXhvVert74%3D2922977810.1074/jbc.RA117.000437
– reference: SoufiBKrugKHarstAMacekBCharacterization of the E. coli proteome and its modifications during growth and ethanol stressFront. Microbiol.2015610325741329433235310.3389/fmicb.2015.00103
– reference: DoiYWachinoJIArakawaYAminoglycoside resistance: The emergence of acquired 16S ribosomal RNA methyltransferasesInfect. Dis. Clin. N. Am.20163052353710.1016/j.idc.2016.02.011
– reference: MoriHKondoAOhshimaAOguraTHiragaSStructure and function of the F plasmid genes essential for partitioningJ. Mol. Biol.19861921151:CAS:528:DyaL2sXivVejuw%3D%3D302939010.1016/0022-2836(86)90459-6
– reference: GordonNCPrediction of Staphylococcus aureus antimicrobial resistance by whole-genome sequencingJ. Clin. Microbiol.201452118211911:CAS:528:DC%2BC2cXhsVGksLzO24501024399349110.1128/JCM.03117-13
– reference: ChangCJDiagnosis of beta-lactam resistance in Acinetobacter baumannii using shotgun proteomics and LC-nano-electrospray ionization ion trap mass spectrometryAnal. Chem.201385280228081:CAS:528:DC%2BC3sXhvVyntb4%3D2337400810.1021/ac303326a
– reference: van der PuttenBCLQuantifying the contribution of four resistance mechanisms to ciprofloxacin MIC in Escherichia coli: A systematic reviewJ. Antimicrob. Chemother.2019742983103035733910.1093/jac/dky4171:CAS:528:DC%2BC1MXitVans73L
– reference: R Core TeamA Language and Environment for Statistical Computing2020R Foundation for Statistical Computing
– reference: Wan Nur IsmahWAKPrediction of fluoroquinolone susceptibility directly from whole-genome sequence data by using liquid chromatography-tandem mass spectrometry to identify mutant genotypesAntimicrob. Agents Chemother.201862e01814-1729263066582610910.1128/AAC.01814-17
– reference: WuSZhuZFuLNiuBLiWWebMGA: A customizable web server for fast metagenomic sequence analysisBMC Genom.20111244410.1186/1471-2164-12-444
– reference: ChoiULeeCRDistinct roles of outer membrane porins in antibiotic resistance and membrane integrity in Escherichia coliFront. Microbiol.20191095331114568650374610.3389/fmicb.2019.00953
– reference: Martinez-MartinezLExtended-spectrum beta-lactamases and the permeability barrierClin. Microbiol. Infect.200814Suppl 182891:CAS:528:DC%2BD1cXhtleiur0%3D1815453110.1111/j.1469-0691.2007.01860.x
– reference: TatusovRLGalperinMYNataleDAKooninEVThe COG database: A tool for genome-scale analysis of protein functions and evolutionNucleic Acids Res.20002833361:CAS:528:DC%2BD3cXhvVGqu7w%3D1059217510239510.1093/nar/28.1.33
– reference: CharretierYSchrenzelJMass spectrometry methods for predicting antibiotic resistanceProteom. Clin. Appl.2016109649811:CAS:528:DC%2BC28Xht1CrtLjK10.1002/prca.201600041
– reference: National Center for Biotechnology Information (US). BLAST® Command Line Applications User Manual. https://www.ncbi.nlm.nih.gov/books/NBK279684/ (2018).
– reference: PaltansingSIncreased expression levels of chromosomal AmpC beta-lactamase in clinical Escherichia coli isolates and their effect on susceptibility to extended-spectrum cephalosporinsMicrob. Drug Resist.2015217161:CAS:528:DC%2BC2MXitFyjt7w%3D2518832910.1089/mdr.2014.0108
– reference: LivermoreDMbeta-Lactamases in laboratory and clinical resistanceClin. Microbiol. Rev.199585575841:CAS:528:DyaK2MXpt12jtLs%3D866547017287610.1128/CMR.8.4.557
– reference: TripHSimultaneous identification of multiple beta-lactamases in Acinetobacter baumannii in relation to carbapenem and ceftazidime resistance, using liquid chromatography-tandem mass spectrometryJ. Clin. Microbiol.201553192719301:CAS:528:DC%2BC2MXpsFGit7o%3D25788550443207110.1128/JCM.00620-15
– reference: WHO. Antimicrobial resistance: Global report on surveillance 2014. https://www.who.int/drugresistance/documents/surveillancereport/en/ (2014).
– reference: UddinMJMaCJKimJCAhnJProteomics-based discrimination of differentially expressed proteins in antibiotic-sensitive and antibiotic-resistant Salmonella typhimurium, Klebsiella pneumoniae, and Staphylococcus aureusArch. Microbiol.2019201125912751:CAS:528:DC%2BC1MXht1Git7vP3124034210.1007/s00203-019-01693-1
– reference: JacobyGABeta-lactamase nomenclatureAntimicrob. Agents Chemother.200650112311291:CAS:528:DC%2BD28XjvFOktbk%3D16569819142697310.1128/AAC.50.4.1123-1129.2006
– reference: KeaseySLDecreased antibiotic susceptibility driven by global remodeling of the Klebsiella pneumoniae proteomeMol. Cell Proteom.2019186576681:CAS:528:DC%2BC1MXot1Gktrc%3D10.1074/mcp.RA118.000739
– reference: WelkerMvan BelkumAOne system for all: Is mass spectrometry a future alternative for conventional antibiotic susceptibility testing?Front. Microbiol.201910271131849870690196510.3389/fmicb.2019.02711
– reference: VergalliJPorins and small-molecule translocation across the outer membrane of Gram-negative bacteriaNat. Rev. Microbiol.2020181641761:CAS:528:DC%2BC1MXit1Ors7zL3179236510.1038/s41579-019-0294-2
– reference: van BelkumAInnovative and rapid antimicrobial susceptibility testing systemsNat. Rev. Microbiol.2020182993113205502610.1038/s41579-020-0327-x1:CAS:528:DC%2BB3cXjtFelsL4%3D
– reference: BabiniGSLivermoreDMAre SHV beta-lactamases universal in Klebsiella pneumoniae?Antimicrob. Agents Chemother.20004422301:CAS:528:DC%2BD3cXltlSht70%3D110234449004910.1128/AAC.44.8.2230-2230.2000
– reference: StephensCF plasmids are the major carriers of antibiotic resistance genes in human-associated commensal Escherichia colimSphere20205e00709-2032759337740707110.1128/mSphere.00709-20
– reference: HassingRJDetection of amino acid substitutions in the GyrA protein of fluoroquinolone-resistant typhoidal Salmonella isolates using high-resolution mass spectrometryInt. J. Antimicrob. Agents2016473513561:CAS:528:DC%2BC28XksVWmsbo%3D2713219110.1016/j.ijantimicag.2016.01.018
– reference: HebertASThe one hour yeast proteomeMol. Cell Proteom.2014133393471:CAS:528:DC%2BC2cXitlSksg%3D%3D10.1074/mcp.M113.034769
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  ident: 91905_CR16
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– volume: 5
  start-page: e00709-20
  year: 2020
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  publication-title: mSphere
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– ident: 91905_CR1
– volume-title: A Language and Environment for Statistical Computing
  year: 2020
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Snippet Antimicrobial resistance is mostly studied by means of phenotypic growth inhibition determinations, in combination with PCR confirmations or further...
Abstract Antimicrobial resistance is mostly studied by means of phenotypic growth inhibition determinations, in combination with PCR confirmations or further...
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SubjectTerms 631/326/22/1434
631/337/475
Acetyltransferases - analysis
Acetyltransferases - genetics
Acetyltransferases - metabolism
Amino Acid Sequence
Aminoglycoside antibiotics
Aminoglycosides - pharmacology
Aminoglycosides - therapeutic use
Anti-Bacterial Agents - therapeutic use
Antibiotic resistance
Antibiotics
Antimicrobial agents
Antimicrobial resistance
Bacterial Proteins - analysis
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
beta-Lactamases - analysis
beta-Lactamases - genetics
beta-Lactamases - metabolism
beta-Lactams - pharmacology
beta-Lactams - therapeutic use
Chromatography
Chromatography, High Pressure Liquid - methods
DNA, Bacterial - genetics
DNA, Bacterial - isolation & purification
Drug resistance
Drug Resistance, Bacterial - genetics
E coli
Escherichia coli - drug effects
Escherichia coli - enzymology
Escherichia coli - genetics
Escherichia coli - isolation & purification
Fluoroquinolones
Fluoroquinolones - pharmacology
Fluoroquinolones - therapeutic use
Gene Expression Regulation, Bacterial
Genomes
Humanities and Social Sciences
Klebsiella pneumoniae - drug effects
Klebsiella pneumoniae - enzymology
Klebsiella pneumoniae - genetics
Klebsiella pneumoniae - isolation & purification
Liquid chromatography
Mass spectrometry
Mass spectroscopy
Methyltransferases - analysis
Methyltransferases - genetics
Methyltransferases - metabolism
multidisciplinary
Phenotypes
Porins
Proteins
Proteogenomics - methods
Proteomes
RNA, Ribosomal, 16S - metabolism
rRNA 16S
Science
Science (multidisciplinary)
Scientific imaging
Tandem Mass Spectrometry - methods
Whole Genome Sequencing
β-Lactam antibiotics
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Title Exploring antimicrobial resistance to beta-lactams, aminoglycosides and fluoroquinolones in E. coli and K. pneumoniae using proteogenomics
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