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Research Article | Clinical Science and Epidemiology

Induction of β-Lactamase Activity and Decreased β-Lactam Susceptibility by CO2 in Clinical Bacterial Isolates

Nathan Mullen, Hugo Raposo, Polyxeni Gudis, Linsey Barker, Romney M. Humphries, Bryan H. Schmitt, Ryan F. Relich, Meghan May
Mariana Castanheira, Editor
Nathan Mullen
a Department of Biomedical Sciences, University of New England College of Osteopathic Medicine, Biddeford, Maine, USA
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Hugo Raposo
a Department of Biomedical Sciences, University of New England College of Osteopathic Medicine, Biddeford, Maine, USA
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Polyxeni Gudis
a Department of Biomedical Sciences, University of New England College of Osteopathic Medicine, Biddeford, Maine, USA
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Linsey Barker
a Department of Biomedical Sciences, University of New England College of Osteopathic Medicine, Biddeford, Maine, USA
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Romney M. Humphries
b Department of Pathology and Laboratory Medicine, David Geffen School of Medicine at UCLA, Los Angeles, California, USA
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Bryan H. Schmitt
c Department of Pathology and Laboratory Medicine, Indiana University School of Medicine, Indianapolis, Indiana, USA
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Ryan F. Relich
c Department of Pathology and Laboratory Medicine, Indiana University School of Medicine, Indianapolis, Indiana, USA
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Meghan May
a Department of Biomedical Sciences, University of New England College of Osteopathic Medicine, Biddeford, Maine, USA
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Mariana Castanheira
JMI Laboratories
Roles: Editor
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DOI: 10.1128/mSphere.00266-17
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  • FIG 1
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    FIG 1

    β-Lactamase activity in F. philomiragia and H. influenzae. Enzymatic units of β-lactamase activity were measured for clinical isolates 14IUHPL0001 and IUH9 and type strains FSC144 and 8143 cultivated in either ambient air (black bars) or 5% CO2 (gray bars). Enzymatic units were normalized to milligrams of total bacterial protein. (A) Both F. philomiragia strains produced significantly (*, P < 0.05; ****, P < 0.0001) higher levels of β-lactamase in 5% CO2 relative to ambient air, and strain 14IUHPL0001 produced significantly more β-lactamase in 5% CO2 relative to FSC144T. (B) Strain IUH9 produced significantly higher levels of β-lactamase in 5% CO2 relative to growth in ambient air and strain 8143T grown in either 5% CO2 or ambient air. There was no significant difference in activities when strain 8143T was grown in 5% CO2 or ambient air.

  • FIG 2
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    FIG 2

    Interrogation of F. philomiragia and H. influenzae for TEM and SHV family β-lactamase genes. blaTEM-specific primers yielded PCR amplicons from both F. philomiragia 14IUHPL0001 and FSC144T, but not from H. influenzae IUH9 or 8143T (top panel). blaSHV-specific primers yielded PCR amplicons from clinical isolates F. philomiragia 14IUHPL0001 and H. influenzae IUH9 but not from either type strain (bottom panel). Negative controls (−) for all reactions were template-free reaction mixtures containing all reagents.

  • FIG 3
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    FIG 3

    Phylogenetic analysis of blaTEM. Phylogenetic analysis performed on the translation of the sequenced amplicon indicated that the 14IUHPL0001 and type strain FSC144T allele clusters with the TEM family β-lactamases. The endogenous chromosomal β-lactamase gene from the type strain FSC144T served as the outgroup.

  • FIG 4
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    FIG 4

    Cultivation of F. philomiragia in 5% CO2 or ambient air generates an alkaline pH shift. Both 14IUHPL0001 and FSC144T significantly shifted the growth medium pH higher in either ambient air (circles) or 5% CO2 (squares) relative to incubated, uninoculated medium.

Tables

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  • TABLE 1

    Antimicrobial susceptibility of Francisella philomiragia under different atmospheric conditions

    Antimicrobial agent(s)MIC (μg/ml) for:
    14IUHPL001FSC144T
    Ambient airCO2Ambient airCO2
    Amikacin≤0.5≤0.5≤0.5≤0.5
    Amoxicillin-clavulanic acid11614
    Ampicillin32>3232>32
    Aztreonam43228
    Cefepime43218
    Ceftazidime≤0.5≤0.5≤0.5≤0.5
    Ceftriaxone≤0.5≤0.5≤0.5≤0.5
    Cefazolin2>3216>32
    Ciprofloxacin≤0.25≤0.25≤0.25≤0.25
    Colistin>8>8>8>8
    Doripenem≤0.251≤0.250.50
    Doxycycline≤1≤1≤1≤1
    Ertapenem≤0.251≤0.25≤0.25
    Gentamicin≤0.5≤0.5≤0.5≤0.5
    Imipenem≤0.250.50≤0.25≤0.25
    Levofloxacin≤2≤2≤2≤2
    Meropenem≤0.250.5≤0.25≤0.25
    Moxifloxacin≤0.25≤0.25≤0.25≤0.25
    Oxacillin≤0.25>16>16>16
    Polymyxin B>4>4>4>4
    Ticarcillin-clavulanic acid≤4≤4≤4≤4
    Tigecycline≤0.25≤0.25≤0.25≤0.25
    Tobramycin≤0.5≤0.5≤0.5≤0.5
    Trimethoprim-sulfamethoxazole>4>4>4>4
  • TABLE 2

    Expression of blaTEM and blaSHV under different atmospheric conditions

    Gene and conditionExpression of gene under condition showna
    F. philomiragiaH. influenzae
    14IUHPL0001FSC144TIUH98143T
    5% CO2
     bla TEM ++−−
     bla SHV +−+−
    Ambient air
     bla TEM −−−−
     bla SHV −−−−
    • ↵a The symbols “+” and “−” indicate the presence or absence, respectively, of RNA/cDNA amplification by reverse transcription-PCR.

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Induction of β-Lactamase Activity and Decreased β-Lactam Susceptibility by CO2 in Clinical Bacterial Isolates
Nathan Mullen, Hugo Raposo, Polyxeni Gudis, Linsey Barker, Romney M. Humphries, Bryan H. Schmitt, Ryan F. Relich, Meghan May
mSphere Jul 2017, 2 (4) e00266-17; DOI: 10.1128/mSphere.00266-17

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Induction of β-Lactamase Activity and Decreased β-Lactam Susceptibility by CO2 in Clinical Bacterial Isolates
Nathan Mullen, Hugo Raposo, Polyxeni Gudis, Linsey Barker, Romney M. Humphries, Bryan H. Schmitt, Ryan F. Relich, Meghan May
mSphere Jul 2017, 2 (4) e00266-17; DOI: 10.1128/mSphere.00266-17
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KEYWORDS

BLA
Francisella
Haemophilus
SHV
TEM
antimicrobial resistance
β-lactamases
carbon dioxide

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