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Mechanisms of Resistance

Novel Aminoglycoside-Tolerant Phoenix Colony Variants of Pseudomonas aeruginosa

Devin Sindeldecker, Kelly Moore, Anthony Li, Daniel J. Wozniak, Matthew Anderson, Devendra H. Dusane, Paul Stoodley
Devin Sindeldecker
aDepartment of Microbial Infection and Immunity, The Ohio State University, Columbus, Ohio, USA
bBiomedical Sciences Graduate Program, The Ohio State University, Columbus, Ohio, USA
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  • ORCID record for Devin Sindeldecker
Kelly Moore
aDepartment of Microbial Infection and Immunity, The Ohio State University, Columbus, Ohio, USA
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Anthony Li
aDepartment of Microbial Infection and Immunity, The Ohio State University, Columbus, Ohio, USA
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Daniel J. Wozniak
aDepartment of Microbial Infection and Immunity, The Ohio State University, Columbus, Ohio, USA
cDepartment of Microbiology, The Ohio State University, Columbus, Ohio, USA
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Matthew Anderson
aDepartment of Microbial Infection and Immunity, The Ohio State University, Columbus, Ohio, USA
cDepartment of Microbiology, The Ohio State University, Columbus, Ohio, USA
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Devendra H. Dusane
aDepartment of Microbial Infection and Immunity, The Ohio State University, Columbus, Ohio, USA
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Paul Stoodley
aDepartment of Microbial Infection and Immunity, The Ohio State University, Columbus, Ohio, USA
dDepartment of Orthopaedics, The Ohio State University, Columbus, Ohio, USA
eNational Center for Advanced Tribology at Southampton (nCATS), Mechanical Engineering, University of Southampton, Southampton, United Kingdom
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DOI: 10.1128/AAC.00623-20
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ABSTRACT

Pseudomonas aeruginosa is an opportunistic bacterial pathogen and is known to produce biofilms. We previously showed the emergence of colony variants in the presence of tobramycin-loaded calcium sulfate beads. In this study, we characterized the variant colonies, which survived the antibiotic treatment, and identified three distinct phenotypes—classically resistant colonies, viable but nonculturable colonies (VBNC), and phoenix colonies. Phoenix colonies, described here for the first time, grow out of the zone of clearance of antibiotic-loaded beads from lawn biofilms while there are still very high concentrations of antibiotic present, suggesting an antibiotic-resistant phenotype. However, upon subculturing of these isolates, phoenix colonies return to wild-type levels of antibiotic susceptibility. Compared with the wild type, phoenix colonies are morphologically similar aside from a deficiency in green pigmentation. Phoenix colonies do not recapitulate the phenotype of any previously described mechanisms of resistance, tolerance, or persistence and, thus, form a novel group with their own phenotype. Growth under anaerobic conditions suggests that an alternative metabolism could lead to the formation of phoenix colonies. These findings suggest that phoenix colonies could emerge in response to antibiotic therapies and lead to recurrent or persistent infections, particularly within biofilms where microaerobic or anaerobic environments are present.

FOOTNOTES

    • Received 2 April 2020.
    • Returned for modification 5 May 2020.
    • Accepted 9 June 2020.
    • Accepted manuscript posted online 15 June 2020.
  • Supplemental material is available online only.

  • Copyright © 2020 American Society for Microbiology.

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Novel Aminoglycoside-Tolerant Phoenix Colony Variants of Pseudomonas aeruginosa
Devin Sindeldecker, Kelly Moore, Anthony Li, Daniel J. Wozniak, Matthew Anderson, Devendra H. Dusane, Paul Stoodley
Antimicrobial Agents and Chemotherapy Aug 2020, 64 (9) e00623-20; DOI: 10.1128/AAC.00623-20

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Novel Aminoglycoside-Tolerant Phoenix Colony Variants of Pseudomonas aeruginosa
Devin Sindeldecker, Kelly Moore, Anthony Li, Daniel J. Wozniak, Matthew Anderson, Devendra H. Dusane, Paul Stoodley
Antimicrobial Agents and Chemotherapy Aug 2020, 64 (9) e00623-20; DOI: 10.1128/AAC.00623-20
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KEYWORDS

Pseudomonas aeruginosa
aminoglycosides
antibiotic tolerance
biofilms

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