Commensal Protection of <named-content content-type="genus-species">Staphylococcus aureus</named-content> against Antimicrobials by <named-content content-type="genus-species">Candida albicans</named-content> Biofilm Matrix

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...

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Autores principales: Eric F. Kong, Christina Tsui, Sona Kucharíková, David Andes, Patrick Van Dijck, Mary Ann Jabra-Rizk
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Publicado: American Society for Microbiology 2016
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spelling oai:doaj.org-article:00eff668d2994f409d164eb2c4aa38b62021-11-15T15:50:15ZCommensal Protection of <named-content content-type="genus-species">Staphylococcus aureus</named-content> against Antimicrobials by <named-content content-type="genus-species">Candida albicans</named-content> Biofilm Matrix10.1128/mBio.01365-162150-7511https://doaj.org/article/00eff668d2994f409d164eb2c4aa38b62016-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01365-16https://doaj.org/toc/2150-7511ABSTRACT 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.Eric F. KongChristina TsuiSona KucharíkováDavid AndesPatrick Van DijckMary Ann Jabra-RizkAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 5 (2016)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Eric F. Kong
Christina Tsui
Sona Kucharíková
David Andes
Patrick Van Dijck
Mary Ann Jabra-Rizk
Commensal Protection of <named-content content-type="genus-species">Staphylococcus aureus</named-content> against Antimicrobials by <named-content content-type="genus-species">Candida albicans</named-content> Biofilm Matrix
description 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.
format article
author Eric F. Kong
Christina Tsui
Sona Kucharíková
David Andes
Patrick Van Dijck
Mary Ann Jabra-Rizk
author_facet Eric F. Kong
Christina Tsui
Sona Kucharíková
David Andes
Patrick Van Dijck
Mary Ann Jabra-Rizk
author_sort Eric F. Kong
title Commensal Protection of <named-content content-type="genus-species">Staphylococcus aureus</named-content> against Antimicrobials by <named-content content-type="genus-species">Candida albicans</named-content> Biofilm Matrix
title_short Commensal Protection of <named-content content-type="genus-species">Staphylococcus aureus</named-content> against Antimicrobials by <named-content content-type="genus-species">Candida albicans</named-content> Biofilm Matrix
title_full Commensal Protection of <named-content content-type="genus-species">Staphylococcus aureus</named-content> against Antimicrobials by <named-content content-type="genus-species">Candida albicans</named-content> Biofilm Matrix
title_fullStr Commensal Protection of <named-content content-type="genus-species">Staphylococcus aureus</named-content> against Antimicrobials by <named-content content-type="genus-species">Candida albicans</named-content> Biofilm Matrix
title_full_unstemmed Commensal Protection of <named-content content-type="genus-species">Staphylococcus aureus</named-content> against Antimicrobials by <named-content content-type="genus-species">Candida albicans</named-content> Biofilm Matrix
title_sort commensal protection of <named-content content-type="genus-species">staphylococcus aureus</named-content> against antimicrobials by <named-content content-type="genus-species">candida albicans</named-content> biofilm matrix
publisher American Society for Microbiology
publishDate 2016
url https://doaj.org/article/00eff668d2994f409d164eb2c4aa38b6
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