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Mechanisms of Resistance

Biological Cost of Different Mechanisms of Colistin Resistance and Their Impact on Virulence in Acinetobacter baumannii

Alejandro Beceiro, Antonio Moreno, Nathalie Fernández, Juán A. Vallejo, Jesús Aranda, Ben Adler, Marina Harper, John D. Boyce, Germán Bou
Alejandro Beceiro
Servicio de Microbiología-INIBIC, Complejo Hospitalario Universitario A Coruña (CHUAC), A Coruña, Spain
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Antonio Moreno
Servicio de Microbiología-INIBIC, Complejo Hospitalario Universitario A Coruña (CHUAC), A Coruña, SpainServicio de Microbiología, Complejo Hospitalario Pontevedra, Pontevedra, Spain
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Nathalie Fernández
Servicio de Microbiología-INIBIC, Complejo Hospitalario Universitario A Coruña (CHUAC), A Coruña, Spain
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Juán A. Vallejo
Servicio de Microbiología-INIBIC, Complejo Hospitalario Universitario A Coruña (CHUAC), A Coruña, Spain
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Jesús Aranda
Servicio de Microbiología-INIBIC, Complejo Hospitalario Universitario A Coruña (CHUAC), A Coruña, SpainServicio de Microbiología, Complejo Hospitalario Pontevedra, Pontevedra, SpainDepartament de Genètica i Microbiologia, Facultat de Biociències, Universitat Autònoma de Barcelona (UAB), Cerdanyola del Vallès, Barcelona, Spain
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Ben Adler
Department of Microbiology, Monash University, Melbourne, Victoria, AustraliaAustralian Research Council Centre of Excellence in Structural and Functional Microbial Genomics, Monash University, Melbourne, Victoria, Australia
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Marina Harper
Department of Microbiology, Monash University, Melbourne, Victoria, AustraliaAustralian Research Council Centre of Excellence in Structural and Functional Microbial Genomics, Monash University, Melbourne, Victoria, Australia
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John D. Boyce
Department of Microbiology, Monash University, Melbourne, Victoria, Australia
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Germán Bou
Servicio de Microbiología-INIBIC, Complejo Hospitalario Universitario A Coruña (CHUAC), A Coruña, Spain
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DOI: 10.1128/AAC.01597-13
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  • FIG 1
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    FIG 1

    In vitro growth of ATCC 19606 and the colistin-resistant laboratory derivates. The numbers of CFU per milliliter were determined at 1, 2, 3, 5, 7, and 20 h. The means of four independent replicates (for each growth curve) are shown. The error bars represent the standard deviation (SD).

  • FIG 2
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    FIG 2

    Relative in vitro competition indexes of colistin-resistant mutants. The CI values were calculated as the number of Col-R mutants divided by the number of bacteria of the Col-S parental strain of A. baumannii, and the median CI values are shown in parentheses. Each circle represents the CI obtained in each in vitro replicate. Experiments were performed at 5 and 20 h. In all cases, the differences in bacterial counts were statistically significant (P < 0.01). The error bars represent the standard deviation.

  • FIG 3
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    FIG 3

    Relative in vivo competition indexes determined in a mouse systemic-infection model over 20 h. The CI values were calculated as the number of Col-R mutants divided by the number of bacteria of the Col-S parental strain of A. baumannii, and the median CI values are shown in parentheses. Circles represent the CI obtained in each in vivo replicate. The differences in bacterial counts were statistically significant (P < 0.01). The error bars represent the standard deviation.

  • FIG 4
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    FIG 4

    Abilities of different A. baumannii strains to cause cell death of A549 alveolar cells. (A) Fluorescence microscopy images of human alveolar A549 cells infected with each of the A. baumannii strains and stained with the LIVE/DEAD Cellstain double-staining kit. Healthy cells with intact membranes are stained green, and dead cells with permeabilized membranes are stained red. A549 cells were incubated with the A. baumannii strains ATCC 19606 WT, AL1851 ΔlpxA, Al1852 ΔlpxD, AL1842 ΔlpxC, and ATCC 19606 pmrB for 20 h or left uninfected. (B) Quantification of A549 cell death caused by A. baumannii ATCC 19606 WT and AL1851 ΔlpxA, AL1852 ΔlpxD, and AL1842 ΔlpxC mutants and the pmrB mutant. The results of 6 independent experiments are shown as means and SD. *, P < 0.01 between the parental strain and each of the designated mutants; **, not statistically different.

  • FIG 5
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    FIG 5

    Survival of BALB/c (n = 10 per group) mice following intraperitoneal infection with 3 × 108 CFU of the ATCC 19606, AL1842 ΔlpxC, or ATCC 19606 pmrB strain. No difference in survival was found between the mice infected with the pmrB mutant or the parental strain, but survival was significantly higher in mice infected with the AL1842 ΔlpxC mutant (P < 0.01).

  • FIG 6
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    FIG 6

    C. elegans fertility assays. The number of progeny from L4 stage worms was monitored for 5 days in the presence of the nonvirulent control E. coli OP50, the A. baumannii ATCC 19606 WT strain and its colistin-resistant mutants (A), or A. baumannii ABRIM and ABRIM pmrB (B). The error bars represent the standard deviation.

Tables

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  • TABLE 1

    Bacterial strains used in this study

    StrainDescriptionColistin MIC (μg/ml)Source or reference
    ATCC 19606A. baumannii type strain; parent of AL1842 ΔlpxC, AL1851 ΔlpxA, and AL1852 ΔlpxD1American Type Culture Collection
    AL1851 ΔlpxADerivate of ATCC 19606; colistin resistant; 445-bp deletion within lpxA6412
    AL1852 ΔlpxDDerivate of ATCC 19606; colistin resistant; single base deletion at nucleotide [nt] 364 of lpxD and frame shift after K317>12812
    AL1842 ΔlpxCDerivate of ATCC 19606; colistin resistant; 84-bp deletion within lpxC12812
    ATCC 19606 pmrBDerivate of ATCC 19606; colistin resistant; single amino acid substitution (Ala227Val) in PmrB. Ala227Val is adjacent to the conserved histidine at the site of phosphorylation (His228).6415
    ABRIMA. baumannii clinical strain carrying the carbapenemase OXA-24, isolated in a Spanish nosocomial outbreak in 1997121
    ABRIM pmrBDerivate of A. baumannii ABRIM; colistin resistant; single amino acid substitution (Asn353Tyr) in PmrB. This substitution is inside the ATP binding site and may have an effect on the phosphorylation of His228 and thereby on the phosphorylation levels of PmrA.3215
    OP50E. coli strain used for maintenance of C. elegansNAa24
    • ↵a NA, not applicable.

  • TABLE 2

    A. baumannii doubling times and growth rates measured in the exponential phase of growth over the first 300 mina

    StrainDoubling time (g) (min)Growth rate (μ) (h−1)
    ATCC 1960627 ± 31.56 ± 0.27
    AL1851 ΔlpxA49 ± 60.85 ± 0.09
    AL1842 ΔlpxC40 ± 31.03 ± 0.09
    AL1852 ΔlpxD83 ± 80.49 ± 0.03
    ATCC 19606 pmrB32 ± 11.32 ± 0.03
    • ↵a Data were extracted from Fig. 1.

  • TABLE 3

    C. elegans fertility assay

    StrainQuantification (per day) on daya:Total no. of progenyaDifference from controlb (%)
    1234
    A. baumannii
        ATCC 196064599.347.72.33194.2 ± 6.979.5
        AL1851 ΔlpxA70.2158.787.30.7316.9 ± 12129.7
        AL1852 ΔlpxD73.7202.761.30.7338.3 ± 26138.4
        AL1842 ΔlpxC62.5147.272.32.3284.3 ± 50116.3
        ATCC 19606 pmrB46.339237.29.7180.2 ± 2273.7
        ABRIM37.383.776.52.8200.3 ± 1381.9
        ABRIM pmrB38.87575.313.5202.7 ± 30.382.9
    E. coli OP5038.6122.473.210.2244.4 ± 28100
    • ↵a Mean quantification and total no. of progeny by worm.

    • ↵b Percentage of progeny compared to E. coli OP50.

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Biological Cost of Different Mechanisms of Colistin Resistance and Their Impact on Virulence in Acinetobacter baumannii
Alejandro Beceiro, Antonio Moreno, Nathalie Fernández, Juán A. Vallejo, Jesús Aranda, Ben Adler, Marina Harper, John D. Boyce, Germán Bou
Antimicrobial Agents and Chemotherapy Dec 2013, 58 (1) 518-526; DOI: 10.1128/AAC.01597-13

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Biological Cost of Different Mechanisms of Colistin Resistance and Their Impact on Virulence in Acinetobacter baumannii
Alejandro Beceiro, Antonio Moreno, Nathalie Fernández, Juán A. Vallejo, Jesús Aranda, Ben Adler, Marina Harper, John D. Boyce, Germán Bou
Antimicrobial Agents and Chemotherapy Dec 2013, 58 (1) 518-526; DOI: 10.1128/AAC.01597-13
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