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Research Article

Phenotypic Profiling Reveals that Candida albicans Opaque Cells Represent a Metabolically Specialized Cell State Compared to Default White Cells

Iuliana V. Ene, Matthew B. Lohse, Adrian V. Vladu, Joachim Morschhäuser, Alexander D. Johnson, Richard J. Bennett
Malcolm Whiteway, Invited Editor, Judith Berman, Editor
Iuliana V. Ene
aDepartment of Molecular Microbiology and Immunology, Brown University, Providence, Rhode Island, USA
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Matthew B. Lohse
bDepartment of Microbiology, University of California, San Francisco, San Francisco, California, USA
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Adrian V. Vladu
cDepartment of Mathematics, MIT, Cambridge, Massachusetts, USA
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Joachim Morschhäuser
dInstitut für Molekulare Infektionsbiologie, Universität Würzburg, Würzburg, Germany
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Alexander D. Johnson
bDepartment of Microbiology, University of California, San Francisco, San Francisco, California, USA
eDepartment of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, California, USA
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Richard J. Bennett
aDepartment of Molecular Microbiology and Immunology, Brown University, Providence, Rhode Island, USA
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Malcolm Whiteway
Concordia University
Roles: Invited Editor
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Judith Berman
Tel Aviv University
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DOI: 10.1128/mBio.01269-16
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ABSTRACT

The white-opaque switch is a bistable, epigenetic transition affecting multiple traits in Candida albicans including mating, immunogenicity, and niche specificity. To compare how the two cell states respond to external cues, we examined the fitness, phenotypic switching, and filamentation properties of white cells and opaque cells under 1,440 different conditions at 25°C and 37°C. We demonstrate that white and opaque cells display striking differences in their integration of metabolic and thermal cues, so that the two states exhibit optimal fitness under distinct conditions. White cells were fitter than opaque cells under a wide range of environmental conditions, including growth at various pHs and in the presence of chemical stresses or antifungal drugs. This difference was exacerbated at 37°C, consistent with white cells being the default state of C. albicans in the mammalian host. In contrast, opaque cells showed greater fitness than white cells under select nutritional conditions, including growth on diverse peptides at 25°C. We further demonstrate that filamentation is significantly rewired between the two states, with white and opaque cells undergoing filamentous growth in response to distinct external cues. Genetic analysis was used to identify signaling pathways impacting the white-opaque transition both in vitro and in a murine model of commensal colonization, and three sugar sensing pathways are revealed as regulators of the switch. Together, these findings establish that white and opaque cells are programmed for differential integration of metabolic and thermal cues and that opaque cells represent a more metabolically specialized cell state than the default white state.

IMPORTANCE Epigenetic transitions are an important mechanism by which microbes adapt to external stimuli. For Candida albicans, such transitions are crucial for adaptation to complex, fluctuating environments, and therefore contribute to its success as a human pathogen. The white-opaque switch modulates multiple C. albicans attributes, from sexual competency to niche specificity. Here, we demonstrate that metabolic circuits are extensively rewired between white and opaque states, so that the two cell types exhibit optimal fitness under different nutritional conditions and at different temperatures. We thereby establish that epigenetic events can profoundly alter the metabolism of fungal cells. We also demonstrate that epigenetic switching regulates filamentation and biofilm formation, two phenotypes closely associated with pathogenesis. These experiments reveal that white cells, considered the most clinically relevant form of C. albicans, are a “general-purpose” state suited to many environments, whereas opaque cells appear to represent a more metabolically specialized form of the species.

  • Copyright © 2016 Ene 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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Phenotypic Profiling Reveals that Candida albicans Opaque Cells Represent a Metabolically Specialized Cell State Compared to Default White Cells
Iuliana V. Ene, Matthew B. Lohse, Adrian V. Vladu, Joachim Morschhäuser, Alexander D. Johnson, Richard J. Bennett
mBio Nov 2016, 7 (6) e01269-16; DOI: 10.1128/mBio.01269-16

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Phenotypic Profiling Reveals that Candida albicans Opaque Cells Represent a Metabolically Specialized Cell State Compared to Default White Cells
Iuliana V. Ene, Matthew B. Lohse, Adrian V. Vladu, Joachim Morschhäuser, Alexander D. Johnson, Richard J. Bennett
mBio Nov 2016, 7 (6) e01269-16; DOI: 10.1128/mBio.01269-16
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