<italic toggle="yes">Candida albicans</italic> Dispersed Cells Are Developmentally Distinct from Biofilm and Planktonic Cells

ABSTRACT Candida albicans surface-attached biofilms such as those formed on intravenous catheters with direct access to the bloodstream often serve as a nidus for continuous release of cells capable of initiating new infectious foci. We previously reported that cells dispersed from a biofilm are yea...

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Autores principales:	Priya Uppuluri, Maikel Acosta Zaldívar, Matthew Z. Anderson, Matthew J. Dunn, Judith Berman, Jose Luis Lopez Ribot, Julia R. Köhler
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Candida albicans RNA-seq biofilms carbon metabolism dispersal gene expression Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/e43b2715d41848f79094990e8747bd67
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spelling	oai:doaj.org-article:e43b2715d41848f79094990e8747bd672021-11-15T16:00:15Z<italic toggle="yes">Candida albicans</italic> Dispersed Cells Are Developmentally Distinct from Biofilm and Planktonic Cells10.1128/mBio.01338-182150-7511https://doaj.org/article/e43b2715d41848f79094990e8747bd672018-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01338-18https://doaj.org/toc/2150-7511ABSTRACT Candida albicans surface-attached biofilms such as those formed on intravenous catheters with direct access to the bloodstream often serve as a nidus for continuous release of cells capable of initiating new infectious foci. We previously reported that cells dispersed from a biofilm are yeast cells that originate from the top-most hyphal layers of the biofilm. Compared to their planktonic counterparts, these biofilm dispersal yeast cells displayed enhanced virulence-associated characteristics and drug resistance. However, little is known about their molecular properties. To address that issue, in this study we aimed to define the molecular characteristics of these biofilm dispersal cells. We found that the inducer of dispersal, PES1, genetically interacts with the repressor of filamentation, NRG1, in a manner consistent with the definition of dispersed cells as yeast cells. Further, using a flow biofilm model, we performed comprehensive comparative RNA sequencing on freshly dispersed cells in order to identify unique transcriptomic characteristics. Gene expression analysis demonstrated that dispersed cells largely inherit a biofilm-like mRNA profile. Strikingly, however, dispersed cells seemed transcriptionally reprogrammed to acquire nutrients such as zinc and amino acids and to metabolize alternative carbon sources, while their biofilm-associated parent cells did not induce the same high-affinity transporters or express gluconeogenetic genes, despite exposure to the same nutritional signals. Collectively, the findings from this study characterize cell dispersal as an intrinsic step of biofilm development which generates propagules more adept at colonizing distant host sites. This developmental step anticipates the need for virulence-associated gene expression before the cells experience the associated external signals. IMPORTANCE Candida albicans surface-attached biofilms serve as a reservoir of cells to perpetuate and expand an infection; cells released from biofilms on catheters have direct access to the bloodstream. Biofilm dispersal yeast cells exhibit enhanced adhesion, invasion, and biofilm formation compared to their planktonic counterparts. Here, we show using transcriptome sequencing (RNA-seq) that dispersed yeast cells are developmentally distinct from the cells in their parent biofilms as well as from planktonic yeast cells. Dispersal cells possess an anticipatory expression pattern that primes them to infect new sites in the host, to survive in nutrient-starved niches, and to invade new sites. These studies identified dispersal cells as a unique proliferative cell type of the biofilm and showed that they could serve as targets for antibiofilm drug development in the future.Priya UppuluriMaikel Acosta ZaldívarMatthew Z. AndersonMatthew J. DunnJudith BermanJose Luis Lopez RibotJulia R. KöhlerAmerican Society for MicrobiologyarticleCandida albicansRNA-seqbiofilmscarbon metabolismdispersalgene expressionMicrobiologyQR1-502ENmBio, Vol 9, Iss 4 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Candida albicans RNA-seq biofilms carbon metabolism dispersal gene expression Microbiology QR1-502
spellingShingle	Candida albicans RNA-seq biofilms carbon metabolism dispersal gene expression Microbiology QR1-502 Priya Uppuluri Maikel Acosta Zaldívar Matthew Z. Anderson Matthew J. Dunn Judith Berman Jose Luis Lopez Ribot Julia R. Köhler <italic toggle="yes">Candida albicans</italic> Dispersed Cells Are Developmentally Distinct from Biofilm and Planktonic Cells
description	ABSTRACT Candida albicans surface-attached biofilms such as those formed on intravenous catheters with direct access to the bloodstream often serve as a nidus for continuous release of cells capable of initiating new infectious foci. We previously reported that cells dispersed from a biofilm are yeast cells that originate from the top-most hyphal layers of the biofilm. Compared to their planktonic counterparts, these biofilm dispersal yeast cells displayed enhanced virulence-associated characteristics and drug resistance. However, little is known about their molecular properties. To address that issue, in this study we aimed to define the molecular characteristics of these biofilm dispersal cells. We found that the inducer of dispersal, PES1, genetically interacts with the repressor of filamentation, NRG1, in a manner consistent with the definition of dispersed cells as yeast cells. Further, using a flow biofilm model, we performed comprehensive comparative RNA sequencing on freshly dispersed cells in order to identify unique transcriptomic characteristics. Gene expression analysis demonstrated that dispersed cells largely inherit a biofilm-like mRNA profile. Strikingly, however, dispersed cells seemed transcriptionally reprogrammed to acquire nutrients such as zinc and amino acids and to metabolize alternative carbon sources, while their biofilm-associated parent cells did not induce the same high-affinity transporters or express gluconeogenetic genes, despite exposure to the same nutritional signals. Collectively, the findings from this study characterize cell dispersal as an intrinsic step of biofilm development which generates propagules more adept at colonizing distant host sites. This developmental step anticipates the need for virulence-associated gene expression before the cells experience the associated external signals. IMPORTANCE Candida albicans surface-attached biofilms serve as a reservoir of cells to perpetuate and expand an infection; cells released from biofilms on catheters have direct access to the bloodstream. Biofilm dispersal yeast cells exhibit enhanced adhesion, invasion, and biofilm formation compared to their planktonic counterparts. Here, we show using transcriptome sequencing (RNA-seq) that dispersed yeast cells are developmentally distinct from the cells in their parent biofilms as well as from planktonic yeast cells. Dispersal cells possess an anticipatory expression pattern that primes them to infect new sites in the host, to survive in nutrient-starved niches, and to invade new sites. These studies identified dispersal cells as a unique proliferative cell type of the biofilm and showed that they could serve as targets for antibiofilm drug development in the future.
format	article
author	Priya Uppuluri Maikel Acosta Zaldívar Matthew Z. Anderson Matthew J. Dunn Judith Berman Jose Luis Lopez Ribot Julia R. Köhler
author_facet	Priya Uppuluri Maikel Acosta Zaldívar Matthew Z. Anderson Matthew J. Dunn Judith Berman Jose Luis Lopez Ribot Julia R. Köhler
author_sort	Priya Uppuluri
title	<italic toggle="yes">Candida albicans</italic> Dispersed Cells Are Developmentally Distinct from Biofilm and Planktonic Cells
title_short	<italic toggle="yes">Candida albicans</italic> Dispersed Cells Are Developmentally Distinct from Biofilm and Planktonic Cells
title_full	<italic toggle="yes">Candida albicans</italic> Dispersed Cells Are Developmentally Distinct from Biofilm and Planktonic Cells
title_fullStr	<italic toggle="yes">Candida albicans</italic> Dispersed Cells Are Developmentally Distinct from Biofilm and Planktonic Cells
title_full_unstemmed	<italic toggle="yes">Candida albicans</italic> Dispersed Cells Are Developmentally Distinct from Biofilm and Planktonic Cells
title_sort	<italic toggle="yes">candida albicans</italic> dispersed cells are developmentally distinct from biofilm and planktonic cells
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/e43b2715d41848f79094990e8747bd67
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<italic toggle="yes">Candida albicans</italic> Dispersed Cells Are Developmentally Distinct from Biofilm and Planktonic Cells

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