Aggregate Filamentous Growth Responses in Yeast

ABSTRACT Many fungal species, including pathogens, undergo a morphogenetic response called filamentous growth, where cells differentiate into a specialized cell type to promote nutrient foraging and surface colonization. Despite the fact that filamentous growth is required for virulence in some plan...

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Autores principales:	Jacky Chow, Heather M. Dionne, Aditi Prabhakar, Amit Mehrotra, Jenn Somboonthum, Beatriz Gonzalez, Mira Edgerton, Paul J. Cullen
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	MAP kinase Rho GTPase cell differentiation cell polarity cell shape collective cellular responses Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8aa66c02cd194fceb358a336039158af
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spelling	oai:doaj.org-article:8aa66c02cd194fceb358a336039158af2021-11-15T15:22:22ZAggregate Filamentous Growth Responses in Yeast10.1128/mSphere.00702-182379-5042https://doaj.org/article/8aa66c02cd194fceb358a336039158af2019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00702-18https://doaj.org/toc/2379-5042ABSTRACT Many fungal species, including pathogens, undergo a morphogenetic response called filamentous growth, where cells differentiate into a specialized cell type to promote nutrient foraging and surface colonization. Despite the fact that filamentous growth is required for virulence in some plant and animal pathogens, certain aspects of this behavior remain poorly understood. By examining filamentous growth in the budding yeast Saccharomyces cerevisiae and the opportunistic pathogen Candida albicans, we identify responses where cells undergo filamentous growth in groups of cells or aggregates. In S. cerevisiae, aggregate invasive growth was regulated by signaling pathways that control normal filamentous growth. These pathways promoted aggregation in part by fostering aspects of microbial cooperation. For example, aggregate invasive growth required cellular contacts mediated by the flocculin Flo11p, which was produced at higher levels in aggregates than cells undergoing regular invasive growth. Aggregate invasive growth was also stimulated by secreted enzymes, like invertase, which produce metabolites that are shared among cells. Aggregate invasive growth was also induced by alcohols that promote density-dependent filamentous growth in yeast. Aggregate invasive growth also required highly polarized cell morphologies, which may affect the packing or organization of cells. A directed selection experiment for aggregating phenotypes uncovered roles for the fMAPK and RAS pathways, which indicates that these pathways play a general role in regulating aggregate-based responses in yeast. Our study extends the range of responses controlled by filamentation regulatory pathways and has implications in understanding aspects of fungal biology that may be relevant to fungal pathogenesis. IMPORTANCE Filamentous growth is a fungal morphogenetic response that is critical for virulence in some fungal species. Many aspects of filamentous growth remain poorly understood. We have identified an aspect of filamentous growth in the budding yeast Saccharomyces cerevisiae and the human pathogen Candida albicans where cells behave collectively to invade surfaces in aggregates. These responses may reflect an extension of normal filamentous growth, as they share the same signaling pathways and effector processes. Aggregate responses may involve cooperation among individual cells, because aggregation was stimulated by cell adhesion molecules, secreted enzymes, and diffusible molecules that promote quorum sensing. Our study may provide insights into the genetic basis of collective cellular responses in fungi. The study may have ramifications in fungal pathogenesis, in situations where collective responses occur to promote virulence.Jacky ChowHeather M. DionneAditi PrabhakarAmit MehrotraJenn SomboonthumBeatriz GonzalezMira EdgertonPaul J. CullenAmerican Society for MicrobiologyarticleMAP kinaseRho GTPasecell differentiationcell polaritycell shapecollective cellular responsesMicrobiologyQR1-502ENmSphere, Vol 4, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	MAP kinase Rho GTPase cell differentiation cell polarity cell shape collective cellular responses Microbiology QR1-502
spellingShingle	MAP kinase Rho GTPase cell differentiation cell polarity cell shape collective cellular responses Microbiology QR1-502 Jacky Chow Heather M. Dionne Aditi Prabhakar Amit Mehrotra Jenn Somboonthum Beatriz Gonzalez Mira Edgerton Paul J. Cullen Aggregate Filamentous Growth Responses in Yeast
description	ABSTRACT Many fungal species, including pathogens, undergo a morphogenetic response called filamentous growth, where cells differentiate into a specialized cell type to promote nutrient foraging and surface colonization. Despite the fact that filamentous growth is required for virulence in some plant and animal pathogens, certain aspects of this behavior remain poorly understood. By examining filamentous growth in the budding yeast Saccharomyces cerevisiae and the opportunistic pathogen Candida albicans, we identify responses where cells undergo filamentous growth in groups of cells or aggregates. In S. cerevisiae, aggregate invasive growth was regulated by signaling pathways that control normal filamentous growth. These pathways promoted aggregation in part by fostering aspects of microbial cooperation. For example, aggregate invasive growth required cellular contacts mediated by the flocculin Flo11p, which was produced at higher levels in aggregates than cells undergoing regular invasive growth. Aggregate invasive growth was also stimulated by secreted enzymes, like invertase, which produce metabolites that are shared among cells. Aggregate invasive growth was also induced by alcohols that promote density-dependent filamentous growth in yeast. Aggregate invasive growth also required highly polarized cell morphologies, which may affect the packing or organization of cells. A directed selection experiment for aggregating phenotypes uncovered roles for the fMAPK and RAS pathways, which indicates that these pathways play a general role in regulating aggregate-based responses in yeast. Our study extends the range of responses controlled by filamentation regulatory pathways and has implications in understanding aspects of fungal biology that may be relevant to fungal pathogenesis. IMPORTANCE Filamentous growth is a fungal morphogenetic response that is critical for virulence in some fungal species. Many aspects of filamentous growth remain poorly understood. We have identified an aspect of filamentous growth in the budding yeast Saccharomyces cerevisiae and the human pathogen Candida albicans where cells behave collectively to invade surfaces in aggregates. These responses may reflect an extension of normal filamentous growth, as they share the same signaling pathways and effector processes. Aggregate responses may involve cooperation among individual cells, because aggregation was stimulated by cell adhesion molecules, secreted enzymes, and diffusible molecules that promote quorum sensing. Our study may provide insights into the genetic basis of collective cellular responses in fungi. The study may have ramifications in fungal pathogenesis, in situations where collective responses occur to promote virulence.
format	article
author	Jacky Chow Heather M. Dionne Aditi Prabhakar Amit Mehrotra Jenn Somboonthum Beatriz Gonzalez Mira Edgerton Paul J. Cullen
author_facet	Jacky Chow Heather M. Dionne Aditi Prabhakar Amit Mehrotra Jenn Somboonthum Beatriz Gonzalez Mira Edgerton Paul J. Cullen
author_sort	Jacky Chow
title	Aggregate Filamentous Growth Responses in Yeast
title_short	Aggregate Filamentous Growth Responses in Yeast
title_full	Aggregate Filamentous Growth Responses in Yeast
title_fullStr	Aggregate Filamentous Growth Responses in Yeast
title_full_unstemmed	Aggregate Filamentous Growth Responses in Yeast
title_sort	aggregate filamentous growth responses in yeast
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/8aa66c02cd194fceb358a336039158af
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_version_	1718428017400741888

Aggregate Filamentous Growth Responses in Yeast

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