Different levels of catabolite repression optimize growth in stable and variable environments.

Organisms respond to environmental changes by adapting the expression of key genes. However, such transcriptional reprogramming requires time and energy, and may also leave the organism ill-adapted when the original environment returns. Here, we study the dynamics of transcriptional reprogramming an...

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Autores principales:	Aaron M New, Bram Cerulus, Sander K Govers, Gemma Perez-Samper, Bo Zhu, Sarah Boogmans, Joao B Xavier, Kevin J Verstrepen
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2014
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/a1d9798d97464802ae637b7fa65fec36
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spelling	oai:doaj.org-article:a1d9798d97464802ae637b7fa65fec362021-11-18T05:37:38ZDifferent levels of catabolite repression optimize growth in stable and variable environments.1544-91731545-788510.1371/journal.pbio.1001764https://doaj.org/article/a1d9798d97464802ae637b7fa65fec362014-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24453942/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Organisms respond to environmental changes by adapting the expression of key genes. However, such transcriptional reprogramming requires time and energy, and may also leave the organism ill-adapted when the original environment returns. Here, we study the dynamics of transcriptional reprogramming and fitness in the model eukaryote Saccharomyces cerevisiae in response to changing carbon environments. Population and single-cell analyses reveal that some wild yeast strains rapidly and uniformly adapt gene expression and growth to changing carbon sources, whereas other strains respond more slowly, resulting in long periods of slow growth (the so-called "lag phase") and large differences between individual cells within the population. We exploit this natural heterogeneity to evolve a set of mutants that demonstrate how the frequency and duration of changes in carbon source can favor different carbon catabolite repression strategies. At one end of this spectrum are "specialist" strategies that display high rates of growth in stable environments, with more stringent catabolite repression and slower transcriptional reprogramming. The other mutants display less stringent catabolite repression, resulting in leaky expression of genes that are not required for growth in glucose. This "generalist" strategy reduces fitness in glucose, but allows faster transcriptional reprogramming and shorter lag phases when the cells need to shift to alternative carbon sources. Whole-genome sequencing of these mutants reveals that mutations in key regulatory genes such as HXK2 and STD1 adjust the regulation and transcriptional noise of metabolic genes, with some mutations leading to alternative gene regulatory strategies that allow "stochastic sensing" of the environment. Together, our study unmasks how variable and stable environments favor distinct strategies of transcriptional reprogramming and growth.Aaron M NewBram CerulusSander K GoversGemma Perez-SamperBo ZhuSarah BoogmansJoao B XavierKevin J VerstrepenPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 12, Iss 1, p e1001764 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Aaron M New Bram Cerulus Sander K Govers Gemma Perez-Samper Bo Zhu Sarah Boogmans Joao B Xavier Kevin J Verstrepen Different levels of catabolite repression optimize growth in stable and variable environments.
description	Organisms respond to environmental changes by adapting the expression of key genes. However, such transcriptional reprogramming requires time and energy, and may also leave the organism ill-adapted when the original environment returns. Here, we study the dynamics of transcriptional reprogramming and fitness in the model eukaryote Saccharomyces cerevisiae in response to changing carbon environments. Population and single-cell analyses reveal that some wild yeast strains rapidly and uniformly adapt gene expression and growth to changing carbon sources, whereas other strains respond more slowly, resulting in long periods of slow growth (the so-called "lag phase") and large differences between individual cells within the population. We exploit this natural heterogeneity to evolve a set of mutants that demonstrate how the frequency and duration of changes in carbon source can favor different carbon catabolite repression strategies. At one end of this spectrum are "specialist" strategies that display high rates of growth in stable environments, with more stringent catabolite repression and slower transcriptional reprogramming. The other mutants display less stringent catabolite repression, resulting in leaky expression of genes that are not required for growth in glucose. This "generalist" strategy reduces fitness in glucose, but allows faster transcriptional reprogramming and shorter lag phases when the cells need to shift to alternative carbon sources. Whole-genome sequencing of these mutants reveals that mutations in key regulatory genes such as HXK2 and STD1 adjust the regulation and transcriptional noise of metabolic genes, with some mutations leading to alternative gene regulatory strategies that allow "stochastic sensing" of the environment. Together, our study unmasks how variable and stable environments favor distinct strategies of transcriptional reprogramming and growth.
format	article
author	Aaron M New Bram Cerulus Sander K Govers Gemma Perez-Samper Bo Zhu Sarah Boogmans Joao B Xavier Kevin J Verstrepen
author_facet	Aaron M New Bram Cerulus Sander K Govers Gemma Perez-Samper Bo Zhu Sarah Boogmans Joao B Xavier Kevin J Verstrepen
author_sort	Aaron M New
title	Different levels of catabolite repression optimize growth in stable and variable environments.
title_short	Different levels of catabolite repression optimize growth in stable and variable environments.
title_full	Different levels of catabolite repression optimize growth in stable and variable environments.
title_fullStr	Different levels of catabolite repression optimize growth in stable and variable environments.
title_full_unstemmed	Different levels of catabolite repression optimize growth in stable and variable environments.
title_sort	different levels of catabolite repression optimize growth in stable and variable environments.
publisher	Public Library of Science (PLoS)
publishDate	2014
url	https://doaj.org/article/a1d9798d97464802ae637b7fa65fec36
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Different levels of catabolite repression optimize growth in stable and variable environments.

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