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: Ana Traven, Amrei Jänicke, Paul Harrison, Angavai Swaminathan, Torsten Seemann, Traude H Beilharz
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Publicado: Public Library of Science (PLoS) 2012
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spelling oai:doaj.org-article:f61403612b5641c8af2ab77281d4083f2021-11-18T08:13:43ZTranscriptional profiling of a yeast colony provides new insight into the heterogeneity of multicellular fungal communities.1932-620310.1371/journal.pone.0046243https://doaj.org/article/f61403612b5641c8af2ab77281d4083f2012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23029448/?tool=EBIhttps://doaj.org/toc/1932-6203Understanding 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.Ana TravenAmrei JänickePaul HarrisonAngavai SwaminathanTorsten SeemannTraude H BeilharzPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 7, Iss 9, p e46243 (2012)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Ana Traven
Amrei Jänicke
Paul Harrison
Angavai Swaminathan
Torsten Seemann
Traude H Beilharz
Transcriptional profiling of a yeast colony provides new insight into the heterogeneity of multicellular fungal communities.
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.
format article
author Ana Traven
Amrei Jänicke
Paul Harrison
Angavai Swaminathan
Torsten Seemann
Traude H Beilharz
author_facet Ana Traven
Amrei Jänicke
Paul Harrison
Angavai Swaminathan
Torsten Seemann
Traude H Beilharz
author_sort Ana Traven
title 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_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_sort transcriptional profiling of a yeast colony provides new insight into the heterogeneity of multicellular fungal communities.
publisher Public Library of Science (PLoS)
publishDate 2012
url https://doaj.org/article/f61403612b5641c8af2ab77281d4083f
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