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Research Article

Sublethal Exposure to Commercial Formulations of the Herbicides Dicamba, 2,4-Dichlorophenoxyacetic Acid, and Glyphosate Cause Changes in Antibiotic Susceptibility in Escherichia coli and Salmonella enterica serovar Typhimurium

Brigitta Kurenbach, Delphine Marjoshi, Carlos F. Amábile-Cuevas, Gayle C. Ferguson, William Godsoe, Paddy Gibson, Jack A. Heinemann
Stephen J. Giovannoni, Editor
Brigitta Kurenbach
aSchool of Biological Sciences, University of Canterbury, Christchurch, New Zealand
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Delphine Marjoshi
aSchool of Biological Sciences, University of Canterbury, Christchurch, New Zealand
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Carlos F. Amábile-Cuevas
bFundación Lusara, Mexico City, Mexico
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Gayle C. Ferguson
cInstitute of Natural and Mathematical Sciences, Massey University, Palmerston North, New Zealand
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William Godsoe
dBio-Protection Centre, Lincoln University, Lincoln, New Zealand
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Paddy Gibson
aSchool of Biological Sciences, University of Canterbury, Christchurch, New Zealand
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Jack A. Heinemann
aSchool of Biological Sciences, University of Canterbury, Christchurch, New Zealand
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Stephen J. Giovannoni
Oregon State University
Roles: Editor
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DOI: 10.1128/mBio.00009-15
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  • FIG 1 
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    FIG 1 

    Killing curves. On the x axis, antibiotic concentrations (μg/ml) are plotted. Blue bars, no herbicide; orange bars, herbicide present. Herbicide concentrations used were as follows: for Kamba, 1,830 ppm/1,950 ppm (E. coli/S. Typhimurium); for 2,4-D: 1,830 ppm/1,950 ppm; and for Roundup, 1,240 ppm/1,240 ppm. Error bars are standard errors of the means (SEM). Asterisks indicate P values (see Materials and Methods for details). *, P < 0.05; **, P < 0.01; ***, P < 0.001; ns, not significant.

  • FIG 2 
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    FIG 2 

    Dose-response curves. Antibiotic concentrations used (in μg/ml) were as follows: with 2,4-D, Amp at 4/40 (S. Typhimurium/E. coli), Cip at 0.003/0.003, Cam at 4.4/-, Kan at 6/2.5, and Tet at 0.75/-; with Kamba, Amp at 2/0, Cip at 0.03/0.05, Cam at 4/20, Kan at 2/1, and Tet at 0.75/3; and with Roundup, Amp at -/20, Cip at 0.05/0.07, Cam at 2/10, Kan at 12/10, and Tet at 0.45/1. Error bars are SEM, and asterisks indicate P values (see Materials and Methods for details). *, P < 0.05; **, P < 0.01; ***, P < 0.001; ns, not significant; -, not tested.

Tables

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  • TABLE 1 

    MICs of herbicide formulations

    HerbicideMIC (ppm ae):
    E. coli JB578S. Typhimurium SL3770
    Kamba50013,88314,485
    2,4-D46485780
    Roundup74006190
  • TABLE 2 

    Fold changes in antibiotic concentration to cause a 1,000-fold change in the EOP in the presence of a herbicide

    AntibioticHerbicideFold change in antibiotic concn with:
    E. coliaS. Typhimurium
    AmpKamba02.33
    2,4-D1.52
    RoundupNA0
    CamKamba22.2
    2,4-D02.33
    Roundup1.52.5
    CipKamba1.662.66
    2,4-D1.661.66
    Roundup1.85.8
    KanKamba2.52.5
    2,4-D1.51.2
    RoundupNA5
    TetKamba23.33
    2,4-D1.662.5
    Roundup31.66
    • ↵a NA, not applicable (the EOP did not drop below 0.001 at the highest tested concentration).

  • TABLE 3 

    Influence of PAβN exposure on Kamba- and Roundup-induced tolerances in E. colia

    Test conditionEOP without PAβNEOP with PAβN
    LB1.001.093 (0.093)
    Kamba1.42 (0.49)0.292 (7.000 × 10–3)
    Cam2.28 × 10–3 (1.66 × 10–3)<10–7b
    Kamba + Cam1.01 (0.17)<10–7b
    Roundup0.88 (0.44)<10–7b
    Kan8.69 × 10–5 (4.07 × 10–5)0.052 (0.034)
    Roundup + Kan1.44 (0.67)<10–7b
    • ↵a Values are means of results from 3 independent experiments (SEM). Cam was at 10 μg/ml, Kan was at 5 μg/ml, Kamba was at 1,380 ppm, Roundup was at 1,250 ppm, and PAβN was at 25 mM.

    • ↵b Below the detection limit.

  • TABLE 4 

    Strains of E. coli and S. enterica serovar Typhimurium used

    StrainDescriptionSource or reference
    E. coli
        JB578HfrH Su+ thi gal r– m+ RifrLaboratory collection
        TN521DJ901(Δlac-4169) Φ(soxR+ soxS′::lacZ)26
        TN531DJ901(Δlac-4169) Φ(ΔsoxR soxS′::lacZ)26
    S. Typhimurium
        SL3770LT2 pyr+ rfa+55

Supplemental Material

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  • Figure S1 

    Results of blind repeats of the killing curves. On the x axis, antibiotic concentrations (μg/ml) are plotted. Blue bars, no herbicide; orange bars, herbicide present. Herbicide concentrations used were as follows: Kamba, 1,830 ppm/1,950 ppm (E. coli/S. Typhimurium); 2,4-D, 1,830 ppm/1,950 ppm; and Roundup, 1,240 ppm/1,240 ppm. Data are the averages from two independent experiments conducted in duplicate. Download Figure S1, PDF file, 0.5 MB.

    Copyright © 2015 Kurenbach et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

  • Table S1 

    Conversion of ppm to ppm ae of herbicide stock solutions. Table S1, DOCX file, 0.04 MB.

    Copyright © 2015 Kurenbach et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

Additional Files

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  • Tables
  • Supplemental Material
  • Supplementary Data

    Supplementary Data

    Files in this Data Supplement:

    • Figure sf1, PDF - Figure sf1, PDF
    • Table st1, DOCX - Table st1, DOCX
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Sublethal Exposure to Commercial Formulations of the Herbicides Dicamba, 2,4-Dichlorophenoxyacetic Acid, and Glyphosate Cause Changes in Antibiotic Susceptibility in Escherichia coli and Salmonella enterica serovar Typhimurium
Brigitta Kurenbach, Delphine Marjoshi, Carlos F. Amábile-Cuevas, Gayle C. Ferguson, William Godsoe, Paddy Gibson, Jack A. Heinemann
mBio Mar 2015, 6 (2) e00009-15; DOI: 10.1128/mBio.00009-15

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Sublethal Exposure to Commercial Formulations of the Herbicides Dicamba, 2,4-Dichlorophenoxyacetic Acid, and Glyphosate Cause Changes in Antibiotic Susceptibility in Escherichia coli and Salmonella enterica serovar Typhimurium
Brigitta Kurenbach, Delphine Marjoshi, Carlos F. Amábile-Cuevas, Gayle C. Ferguson, William Godsoe, Paddy Gibson, Jack A. Heinemann
mBio Mar 2015, 6 (2) e00009-15; DOI: 10.1128/mBio.00009-15
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