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Mechanisms of Resistance

The Comprehensive Antibiotic Resistance Database

Andrew G. McArthur, Nicholas Waglechner, Fazmin Nizam, Austin Yan, Marisa A. Azad, Alison J. Baylay, Kirandeep Bhullar, Marc J. Canova, Gianfranco De Pascale, Linda Ejim, Lindsay Kalan, Andrew M. King, Kalinka Koteva, Mariya Morar, Michael R. Mulvey, Jonathan S. O'Brien, Andrew C. Pawlowski, Laura J. V. Piddock, Peter Spanogiannopoulos, Arlene D. Sutherland, Irene Tang, Patricia L. Taylor, Maulik Thaker, Wenliang Wang, Marie Yan, Tennison Yu, Gerard D. Wright
Andrew G. McArthur
Andrew McArthur Consulting, Hamilton, Ontario, Canadab
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Nicholas Waglechner
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Fazmin Nizam
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Austin Yan
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Marisa A. Azad
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Alison J. Baylay
School of Immunity and Infection and Institute of Microbiology and Infection, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdomc
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Kirandeep Bhullar
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Marc J. Canova
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Gianfranco De Pascale
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Linda Ejim
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Lindsay Kalan
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Andrew M. King
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Kalinka Koteva
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Mariya Morar
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Michael R. Mulvey
National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Manitoba, Canadad
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Jonathan S. O'Brien
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Andrew C. Pawlowski
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Laura J. V. Piddock
School of Immunity and Infection and Institute of Microbiology and Infection, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United Kingdomc
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Peter Spanogiannopoulos
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Arlene D. Sutherland
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Irene Tang
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Patricia L. Taylor
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Maulik Thaker
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Wenliang Wang
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Marie Yan
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Tennison Yu
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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Gerard D. Wright
M.G. DeGroote Institute for Infectious Disease Research, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canadaa
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DOI: 10.1128/AAC.00419-13
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    Fig 1

    Presentation of the Staphylococcus aureus blaZ ß-lactamase gene in the CARD. (A) The gene's Web page in the CARD, providing annotation, accession, source information, ontological classification (SO, ARO, GO), and associated molecular features (mRNA, polypeptide, coding sequence [CDS]). (B) Dynamic browsing and analysis of the blaZ gene using the Web-based genome visualization and analysis tool GBrowse.

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    Fig 2

    Classification of aminocoumarin-resistant gyrase B in the Antibiotic Resistance Ontology (ARO), illustrating the use of ontological relationships to describe knowledge about the gene (see Table 3). The is_a relationships are depicted by solid arrows labeled with “i” and generally denote classification hierarchies within the major branches of the ARO (mechanism, determinant, antibiotic, target), while dashed arrows labeled with “p” reflect part_of relationships between genes and mechanisms. Dashed arrows labeled with “d” depict derived_from relationships between antibiotic-sensitive precursors and antibiotic-resistant forms of the gene, while those labeled with “t” reflect targeted_by relationships between antibiotic-sensitive forms and antibiotic molecules. Dashed arrows labeled with “r” depict confers_resistance relationships between antibiotic resistance genes and antibiotic molecules. Asterisks denote a derived_from relationship between antibiotic-resistant and -sensitive DNA topoisomerase subunits.

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    Fig 3

    Organization of aminoglycoside antibiotics (blue), their target (green), and aminoglycoside resistance genes (red) in the CARD's Antibiotic Resistance Ontology, illustrating the diversity of genes providing resistance to single or multiple aminoglycosides. Nodes represent ontology terms, while edges represent relationships between ontology terms.

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    Fig 4

    An ontology term Web page for tetracycline resistance gene tetX (ARO:3000205) in the CARD, providing descriptive, ontological classification, sequence, protein structure, publication, taxonomic distribution, and bioinformatics data/model information. By providing an ontology-centered interface, the CARD offers a clearinghouse of information on antibiotic resistance genes, mechanisms, drugs, etc. The left column reflects ontological cross-referencing (see Materials and Methods).

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    Fig 5

    Analysis of the whole genome of Acinetobacter baumannii strain TCDC-AB0715 by the Resistance Gene Identifier (RGI). The A. baumannii strain TCDC-AB0715 is a clinical isolate with resistance to carbapenems, fluoroquinolones, and cephalosporins (26). (A) “Resistance wheel” for A. baumannii strain TCDC-AB0715, predicting resistance to a broad range of antibiotic classes. (B) Details screen of orf0_267, illustrating detection of the aminoglycoside nucleotidyltransferase ANT(3″). (C) Open reading frame (ORF) map of a region of the A. baumannii strain TCDC-AB0715 chromosome, with prediction of β-lactamases TEM-1 and TEM-33 (light blue), aminoglycoside phosphotransferases, nucleotidyltransferases, and acetyltransferases (pink), chloramphenicol acetyltransferase (bright green), sulfonamide-resistant dihydropteroate synthase sul1 (dark green), tetracycline efflux pump tetB (dark pink), and genes implicated in general efflux (dark blue). ORFs unrelated to antibiotic resistance are presented in gray, while non-protein-coding regions are presented in black. The resistance genes identified are consistent with the reported resistance phenotype (26).

Tables

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  • Table 1

    List of antibiotic resistance genes curated in the CARD within which citation, molecular sequence, protein structure, mechanism, and ARO classification details are provideda

    Aminocoumarins
        Aminocoumarin-resistant DNA topoisomerases
            Aminocoumarin-resistant GyrB, ParE, ParY
    Aminoglycosides
        Aminoglycoside acetyltransferases
            AAC(1), AAC(2′), AAC(3), AAC(6′)
        Aminoglycoside nucleotidyltransferases
            ANT(2″), ANT(3″), ANT(4′), ANT(6), ANT(9)
        Aminoglycoside phosphotransferases
            APH(2″), APH(3″), APH(3′), APH(4), APH(6), APH(7″), APH(9)
        16S rRNA methyltransferases
            ArmA, RmtA, RmtB, RmtC, Sgm
    β-Lactams
        Class A β-lactamases
            AER, BLA1, CTX-M, KPC, SHV, TEM, etc.b
        Class B (metallo-)β-lactamases
            BlaB, CcrA, IMP, NDM, VIM, etc.b
        Class C β-lactamases
            ACT, AmpC, CMY, LAT, PDC, etc.b
        Class D β-lactamases
            OXA β-lactamaseb
        mecA (methicillin-resistant PBP2)
        Mutant porin proteins conferring antibiotic resistance
            Antibiotic-resistant Omp36, OmpF, PIB (por)
    Genes modulating β-lactam resistance
        bla (blaI, blaR1) and mec (mecI, mecR1) operons
    Chloramphenicol
        Chloramphenicol acetyltransferase (CAT)
        Chloramphenicol phosphotransferase
    Ethambutol
        Ethambutol-resistant arabinosyltransferase (EmbB)
    Mupirocin
        Mupirocin-resistant isoleucyl-tRNA synthetases
            MupA, MupB
    Peptide antibiotics
        Integral membrane protein MprF
    Phenicol
        Cfr 23S rRNA methyltransferase
    Rifampin
        Rifampin ADP-ribosyltransferase (Arr)
        Rifampin glycosyltransferase
        Rifampin monooxygenase
        Rifampin phosphotransferase
        Rifampin resistance RNA polymerase-binding proteins
            DnaA, RbpA
        Rifampin-resistant beta-subunit of RNA polymerase (RpoB)
    Streptogramins
        Cfr 23S rRNA methyltransferase
        Erm 23S rRNA methyltransferases
            ErmA, ErmB, Erm(31), etc.d
        Streptogramin resistance ATP-binding cassette (ABC) efflux pumps
            Lsa, MsrA, Vga, VgaB
        Streptogramin Vgb lyase
        Vat acetyltransferase
    Fluoroquinolones
        Fluoroquinolone acetyltransferase
        Fluoroquinolone-resistant DNA topoisomerases
            Fluoroquinolone-resistant GyrA, GyrB, ParC
        Quinolone resistance protein (Qnr)
    Fosfomycin
        Fosfomycin phosphotransferases
            FomA, FomB, FosC
        Fosfomycin thiol transferases
            FosA, FosB, FosX
    Glycopeptides
        VanA, VanB, VanD, VanR, VanS, etc.c
    Lincosamides
        Cfr 23S rRNA methyltransferase
        Erm 23S rRNA methyltransferases
            ErmA, ErmB, Erm(31), etc.d
        Lincosamide nucleotidyltransferase (Lin)
    Linezolid
        Cfr 23S rRNA methyltransferase
    Macrolides
        Cfr 23S rRNA methyltransferase
        Erm 23S rRNA methyltransferases
            ErmA, ErmB, Erm(31), etc.d
        Macrolide esterases
            EreA, EreB
        Macrolide glycosyltransferases
            GimA, Mgt, Ole
        Macrolide phosphotransferases (MPH)
            MPH(2′)-I, MPH(2′)-II
        Macrolide resistance efflux pumps
            MefA, MefE, Mel
    Streptothricin
        Streptothricin acetyltransferase (sat)
    Sulfonamides
        Sulfonamide-resistant dihydropteroate synthases
            Sul1, Sul2, Sul3, sulfonamide-resistant FolP
    Tetracyclines
        Mutant porin PIB (por) with reduced permeability
        Tetracycline inactivation enzyme TetX
        Tetracycline resistance major facilitator superfamily (MFS) efflux pumps
            TetA, TetB, TetC, Tet30, Tet31, etc.e
        Tetracycline resistance ribosomal protection proteins
            TetM, TetO, TetQ, Tet32, Tet36, etc.e
    Efflux pumps conferring antibiotic resistance
        ABC antibiotic efflux pump
            MacAB-TolC, MsbA, MsrA,VgaB, etc.f
        MFS antibiotic efflux pump
            EmrD, EmrAB-TolC, NorB, GepA, etc.f
        Multidrug and toxic compound extrusion (MATE) transporter
            MepA
        Resistance-nodulation-cell division (RND) efflux pump
            AdeABC, AcrD, MexAB-OprM, mtrCDE, etc.f
        Small multidrug resistance (SMR) antibiotic efflux pump
            EmrE
    Genes modulating antibiotic efflux
        adeR, acrR, baeSR, mexR, phoPQ, mtrR, etc.g
    • ↵a ARO, Antibiotic Resistance Ontology.

    • ↵b Complete lists of β-lactamase families and individual β-lactamases can be found in the CARD.

    • ↵c Glycopeptide resistance gene clusters include a number of genes encoding proteins with different functions, including sensors, regulators, and enzymes, all of which result in restructuring of the cell wall, providing resistance to glycopeptides. The full list of genes involved can be found in the CARD.

    • ↵d Complete lists of Erm 23S rRNA methyltransferases can be found in the CARD.

    • ↵e Complete lists of tetracycline resistance major facilitator superfamily (MFS) efflux pumps and ribosomal protection proteins can be found in the CARD.

    • ↵f Complete lists of ATP-binding cassette (ABC), MFS, and resistance-nodulation-cell division (RND) antibiotic efflux pumps can be found in the CARD.

    • ↵g Complete lists of efflux regulatory proteins can be found in the CARD, including information on mutations conferring increased rates of antibiotic efflux.

  • Table 2

    Major branches of the AROa

    Major ARO branchScope
    Determinant of Antibiotic Resistance (ARO:3000000)Antibiotic resistance genes, SNPs, or other molecular entities organized by target (e.g., aminocoumarin, glycopeptides, etc.) and mode of action (e.g., antibiotic inactivation, molecular bypass, etc.)
    Mechanism of Antibiotic Resistance (ARO:1000002)Target alteration, target replacement, antibiotic inactivation, antibiotic efflux, antibiotic target protection, reduced permeability to antibiotic
    Antibiotic Target (ARO:3000708)Targeted cell membrane components, protein or nucleotide synthesis machinery, enzymes, etc.
    Antibiotic Molecule (ARO:1000003)Hierarchical classification of antibiotics (e.g., sulfonamide, β-lactam, glycopeptide antibiotics, etc.)
    Inhibitor of Antibiotic Resistance (ARO:0000076)β-Lactamase and other inhibitors
    Antibiotic Biosynthesis (ARO:3000082)Phosphonoacetaldehyde methyltransfererase, glycopeptide biosynthesis, macrolide biosynthesis, streptogramin biosynthesis, fosfomycin biosynthesis, aminocoumarin biosynthesis, phosphoenolpyruvate (PEP) mutase, phosphonopyruvate decarboxylase
    Antibiotic Resistance Terminology (ARO:3000045)Ontological relationship types, bioinformatic model types, reference molecular sequence types, etc.
    • ↵a ARO, Antibiotic Resistance Ontology. All major branches are part_of ARO:1000001, “process or component of antibiotic biology or chemistry.”

  • Table 3

    Relationship types used within the AROa

    Relationship typeDescriptionSource
    is_aAn axiomatic relationship ontology term in which the subject is placed into a higher order classificationRO
    part_ofA relationship ontology term in which the subject is but part of the objectRO
    derives_fromA relationship ontology term in which the subject has its origins in the objectRO
    regulatesA relationship ontology term in which the subject regulates expression of the objectARO
    confers_resistance_toA relationship ontology term in which the subject confers antibiotic resistance to the objectARO
    confers_resistance_to_drugA relationship ontology term in which the subject (usually a gene) confers clinically relevant resistance to a specific antibioticARO
    targeted_byA relationship ontology term in which the subject is targeted by the object (usually a class of antibiotics)ARO
    targeted_by_drugA relationship ontology term in which the subject is targeted by a specific antibioticARO
    • ↵a ARO, Antibiotic Resistance Ontology; RO, Relation Ontology, a part of the Open Biological and Biomedical Ontologies resource (27). Descriptions are paraphrased.

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The Comprehensive Antibiotic Resistance Database
Andrew G. McArthur, Nicholas Waglechner, Fazmin Nizam, Austin Yan, Marisa A. Azad, Alison J. Baylay, Kirandeep Bhullar, Marc J. Canova, Gianfranco De Pascale, Linda Ejim, Lindsay Kalan, Andrew M. King, Kalinka Koteva, Mariya Morar, Michael R. Mulvey, Jonathan S. O'Brien, Andrew C. Pawlowski, Laura J. V. Piddock, Peter Spanogiannopoulos, Arlene D. Sutherland, Irene Tang, Patricia L. Taylor, Maulik Thaker, Wenliang Wang, Marie Yan, Tennison Yu, Gerard D. Wright
Antimicrobial Agents and Chemotherapy Jun 2013, 57 (7) 3348-3357; DOI: 10.1128/AAC.00419-13

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The Comprehensive Antibiotic Resistance Database
Andrew G. McArthur, Nicholas Waglechner, Fazmin Nizam, Austin Yan, Marisa A. Azad, Alison J. Baylay, Kirandeep Bhullar, Marc J. Canova, Gianfranco De Pascale, Linda Ejim, Lindsay Kalan, Andrew M. King, Kalinka Koteva, Mariya Morar, Michael R. Mulvey, Jonathan S. O'Brien, Andrew C. Pawlowski, Laura J. V. Piddock, Peter Spanogiannopoulos, Arlene D. Sutherland, Irene Tang, Patricia L. Taylor, Maulik Thaker, Wenliang Wang, Marie Yan, Tennison Yu, Gerard D. Wright
Antimicrobial Agents and Chemotherapy Jun 2013, 57 (7) 3348-3357; DOI: 10.1128/AAC.00419-13
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