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Transcriptional Profiling of a Yeast Colony Provides New Insight into the Heterogeneity of Multicellular Fungal Communities

Understanding multicellular fungal structures is important for designing better strategies against human fungal pathogens. For example, the ability to form multicellular biofilms is a key virulence property of the yeast Candida albicans. C. albicans biofilms form on indwelling medical devices and ar...

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Autores principales: Traven, Ana, Jänicke, Amrei, Harrison, Paul, Swaminathan, Angavai, Seemann, Torsten, Beilharz, Traude H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3460911/
https://www.ncbi.nlm.nih.gov/pubmed/23029448
http://dx.doi.org/10.1371/journal.pone.0046243
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author Traven, Ana
Jänicke, Amrei
Harrison, Paul
Swaminathan, Angavai
Seemann, Torsten
Beilharz, Traude H.
author_facet Traven, Ana
Jänicke, Amrei
Harrison, Paul
Swaminathan, Angavai
Seemann, Torsten
Beilharz, Traude H.
author_sort Traven, Ana
collection PubMed
description Understanding multicellular fungal structures is important for designing better strategies against human fungal pathogens. For example, the ability to form multicellular biofilms is a key virulence property of the yeast Candida albicans. C. albicans biofilms form on indwelling medical devices and are drug resistant, causing serious infections in hospital settings. Multicellular fungal communities are heterogeneous, consisting of cells experiencing different environments. Heterogeneity is likely important for the phenotypic characteristics of communities, yet it is poorly understood. Here we used colonies of the yeast Saccharomyces cerevisiae as a model fungal multicellular structure. We fractionated the outside colony layers from the cells in the center by FACS, using a Cit1-GFP marker expressed exclusively on the outside. Transcriptomics analysis of the two subpopulations revealed that the outside colony layers are actively growing by fermentative metabolism, while the cells residing on the inside are in a resting state and experience changes to mitochondrial activity. Our data shows several parallels with C. albicans biofilms providing insight into the contributions of heterogeneity to biofilm phenotypes. Hallmarks of C. albicans biofilms – the expression of ribosome and translation functions and activation of glycolysis and ergosterol biosynthesis occur on the outside of colonies, while expression of genes associates with sulfur assimilation is observed in the colony center. Cell wall restructuring occurs in biofilms, and cell wall functions are enriched in both fractions: the outside cells display enrichment of cell wall biosynthesis enzymes and cell wall proteins, while the inside cells express cell wall degrading enzymes. Our study also suggests that noncoding transcription and posttranscriptional mRNA regulation play important roles during growth of yeast in colonies, setting the scene for investigating these pathways in the development of multicellular fungal communities.
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spelling pubmed-34609112012-10-01 Transcriptional Profiling of a Yeast Colony Provides New Insight into the Heterogeneity of Multicellular Fungal Communities Traven, Ana Jänicke, Amrei Harrison, Paul Swaminathan, Angavai Seemann, Torsten Beilharz, Traude H. PLoS One Research Article Understanding multicellular fungal structures is important for designing better strategies against human fungal pathogens. For example, the ability to form multicellular biofilms is a key virulence property of the yeast Candida albicans. C. albicans biofilms form on indwelling medical devices and are drug resistant, causing serious infections in hospital settings. Multicellular fungal communities are heterogeneous, consisting of cells experiencing different environments. Heterogeneity is likely important for the phenotypic characteristics of communities, yet it is poorly understood. Here we used colonies of the yeast Saccharomyces cerevisiae as a model fungal multicellular structure. We fractionated the outside colony layers from the cells in the center by FACS, using a Cit1-GFP marker expressed exclusively on the outside. Transcriptomics analysis of the two subpopulations revealed that the outside colony layers are actively growing by fermentative metabolism, while the cells residing on the inside are in a resting state and experience changes to mitochondrial activity. Our data shows several parallels with C. albicans biofilms providing insight into the contributions of heterogeneity to biofilm phenotypes. Hallmarks of C. albicans biofilms – the expression of ribosome and translation functions and activation of glycolysis and ergosterol biosynthesis occur on the outside of colonies, while expression of genes associates with sulfur assimilation is observed in the colony center. Cell wall restructuring occurs in biofilms, and cell wall functions are enriched in both fractions: the outside cells display enrichment of cell wall biosynthesis enzymes and cell wall proteins, while the inside cells express cell wall degrading enzymes. Our study also suggests that noncoding transcription and posttranscriptional mRNA regulation play important roles during growth of yeast in colonies, setting the scene for investigating these pathways in the development of multicellular fungal communities. Public Library of Science 2012-09-28 /pmc/articles/PMC3460911/ /pubmed/23029448 http://dx.doi.org/10.1371/journal.pone.0046243 Text en © 2012 Traven et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Traven, Ana
Jänicke, Amrei
Harrison, Paul
Swaminathan, Angavai
Seemann, Torsten
Beilharz, Traude H.
Transcriptional Profiling of a Yeast Colony Provides New Insight into the Heterogeneity of Multicellular Fungal Communities
title Transcriptional Profiling of a Yeast Colony Provides New Insight into the Heterogeneity of Multicellular Fungal Communities
title_full Transcriptional Profiling of a Yeast Colony Provides New Insight into the Heterogeneity of Multicellular Fungal Communities
title_fullStr Transcriptional Profiling of a Yeast Colony Provides New Insight into the Heterogeneity of Multicellular Fungal Communities
title_full_unstemmed Transcriptional Profiling of a Yeast Colony Provides New Insight into the Heterogeneity of Multicellular Fungal Communities
title_short Transcriptional Profiling of a Yeast Colony Provides New Insight into the Heterogeneity of Multicellular Fungal Communities
title_sort transcriptional profiling of a yeast colony provides new insight into the heterogeneity of multicellular fungal communities
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3460911/
https://www.ncbi.nlm.nih.gov/pubmed/23029448
http://dx.doi.org/10.1371/journal.pone.0046243
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