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Research Article

Commensal Protection of Staphylococcus aureus against Antimicrobials by Candida albicans Biofilm Matrix

Eric F. Kong, Christina Tsui, Sona Kucharíková, David Andes, Patrick Van Dijck, Mary Ann Jabra-Rizk
Joseph Heitman, Editor
Eric F. Kong
aGraduate Program in Life Sciences, Molecular Microbiology and Immunology Program, University of Maryland, Baltimore, Maryland, USA
bDepartment of Microbiology and Immunology, School of Medicine, University of Maryland, Baltimore, Maryland, USA
cDepartment of Oncology and Diagnostic Sciences, Dental School, University of Maryland, Baltimore, Maryland, USA
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Christina Tsui
cDepartment of Oncology and Diagnostic Sciences, Dental School, University of Maryland, Baltimore, Maryland, USA
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Sona Kucharíková
dLaboratory of Molecular Cell Biology, KU Leuven, Leuven-Heverlee, Flanders, Belgium
eDepartment of Molecular Microbiology, VIB, Leuven-Heverlee, Flanders, Belgium
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David Andes
fDepartment of Medicine, Microbiology and Immunology, University of Wisconsin, Madison, Wisconsin, USA
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Patrick Van Dijck
dLaboratory of Molecular Cell Biology, KU Leuven, Leuven-Heverlee, Flanders, Belgium
eDepartment of Molecular Microbiology, VIB, Leuven-Heverlee, Flanders, Belgium
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Mary Ann Jabra-Rizk
bDepartment of Microbiology and Immunology, School of Medicine, University of Maryland, Baltimore, Maryland, USA
cDepartment of Oncology and Diagnostic Sciences, Dental School, University of Maryland, Baltimore, Maryland, USA
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Joseph Heitman
Duke University
Roles: Editor
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DOI: 10.1128/mBio.01365-16
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ABSTRACT

Biofilm-associated polymicrobial infections, particularly those involving fungi and bacteria, are responsible for significant morbidity and mortality and tend to be challenging to treat. Candida albicans and Staphylococcus aureus specifically are considered leading opportunistic fungal and bacterial pathogens, respectively, mainly due to their ability to form biofilms on catheters and indwelling medical devices. However, the impact of mixed-species biofilm growth on therapy remains largely understudied. In this study, we investigated the influence of C. albicans secreted cell wall polysaccharides on the response of S. aureus to antibacterial agents in biofilm. Results demonstrated significantly enhanced tolerance for S. aureus to drugs in the presence of C. albicans or its secreted cell wall polysaccharide material. Fluorescence confocal time-lapse microscopy revealed impairment of drug diffusion through the mixed biofilm matrix. Using C. albicans mutant strains with modulated cell wall polysaccharide expression, exogenous supplementation, and enzymatic degradation, the C. albicans-secreted β-1,3-glucan cell wall component was identified as the key matrix constituent providing the bacteria with enhanced drug tolerance. Further, antibody labeling demonstrated rapid coating of the bacteria by the C. albicans matrix material. Importantly, via its effect on the fungal biofilm matrix, the antifungal caspofungin sensitized the bacteria to the drugs. Understanding such symbiotic interactions with clinical relevance between microbial species in biofilms will greatly aid in overcoming the limitations of current therapies and in defining potential new targets for treating polymicrobial infections.

IMPORTANCE The fungus Candida albicans and the bacterium Staphylococcus aureus are important microbial pathogens responsible for the majority of infections in hospitalized patients and are often coisolated from a host. In this study, we demonstrated that when grown together, the fungus provides the bacterium with enhanced tolerance to antimicrobial drugs. This process was mediated by polysaccharides secreted by the fungal cell into the environment. The biofilm matrix formed by these polysaccharides prevented penetration by the drugs and provided the bacteria with protection. Importantly, we show that by inhibiting the production of the fungal polysaccharides, a specific antifungal agent indirectly sensitized the bacteria to antimicrobials. Understanding the therapeutic implications of the interactions between these two diverse microbial species will aid in overcoming the limitations of current therapies and in defining new targets for treating complex polymicrobial infections.

  • Copyright © 2016 Kong et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Commensal Protection of Staphylococcus aureus against Antimicrobials by Candida albicans Biofilm Matrix
Eric F. Kong, Christina Tsui, Sona Kucharíková, David Andes, Patrick Van Dijck, Mary Ann Jabra-Rizk
mBio Oct 2016, 7 (5) e01365-16; DOI: 10.1128/mBio.01365-16

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Commensal Protection of Staphylococcus aureus against Antimicrobials by Candida albicans Biofilm Matrix
Eric F. Kong, Christina Tsui, Sona Kucharíková, David Andes, Patrick Van Dijck, Mary Ann Jabra-Rizk
mBio Oct 2016, 7 (5) e01365-16; DOI: 10.1128/mBio.01365-16
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