The Crabtree Effect Shapes the <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content> Lag Phase during the Switch between Different Carbon Sources

ABSTRACT When faced with environmental changes, microbes often enter a temporary growth arrest during which they reprogram the expression of specific genes to adapt to the new conditions. A prime example of such a lag phase occurs when microbes need to switch from glucose to other, less-preferred ca...

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Autores principales:	Gemma Perez-Samper, Bram Cerulus, Abbas Jariani, Lieselotte Vermeersch, Nuria Barrajón Simancas, Markus M. M. Bisschops, Joost van den Brink, Daniel Solis-Escalante, Brigida Gallone, Dries De Maeyer, Elise van Bael, Tom Wenseleers, Jan Michiels, Kathleen Marchal, Pascale Daran-Lapujade, Kevin J. Verstrepen
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Crabtree effect lag phase respiration Saccharomyces cerevisiae diauxic growth Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/6649b93fa924416e8f37628fe37e2c28
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spelling	oai:doaj.org-article:6649b93fa924416e8f37628fe37e2c282021-11-15T15:58:20ZThe Crabtree Effect Shapes the <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content> Lag Phase during the Switch between Different Carbon Sources10.1128/mBio.01331-182150-7511https://doaj.org/article/6649b93fa924416e8f37628fe37e2c282018-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01331-18https://doaj.org/toc/2150-7511ABSTRACT When faced with environmental changes, microbes often enter a temporary growth arrest during which they reprogram the expression of specific genes to adapt to the new conditions. A prime example of such a lag phase occurs when microbes need to switch from glucose to other, less-preferred carbon sources. Despite its industrial relevance, the genetic network that determines the duration of the lag phase has not been studied in much detail. Here, we performed a genome-wide Bar-Seq screen to identify genetic determinants of the Saccharomyces cerevisiae glucose-to-galactose lag phase. The results show that genes involved in respiration, and specifically those encoding complexes III and IV of the electron transport chain, are needed for efficient growth resumption after the lag phase. Anaerobic growth experiments confirmed the importance of respiratory energy conversion in determining the lag phase duration. Moreover, overexpression of the central regulator of respiration, HAP4, leads to significantly shorter lag phases. Together, these results suggest that the glucose-induced repression of respiration, known as the Crabtree effect, is a major determinant of microbial fitness in fluctuating carbon environments. IMPORTANCE The lag phase is arguably one of the prime characteristics of microbial growth. Longer lag phases result in lower competitive fitness in variable environments, and the duration of the lag phase is also important in many industrial processes where long lag phases lead to sluggish, less efficient fermentations. Despite the immense importance of the lag phase, surprisingly little is known about the exact molecular processes that determine its duration. Our study uses the molecular toolbox of S. cerevisiae combined with detailed growth experiments to reveal how the transition from fermentative to respirative metabolism is a key bottleneck for cells to overcome the lag phase. Together, our findings not only yield insight into the key molecular processes and genes that influence lag duration but also open routes to increase the efficiency of industrial fermentations and offer an experimental framework to study other types of lag behavior.Gemma Perez-SamperBram CerulusAbbas JarianiLieselotte VermeerschNuria Barrajón SimancasMarkus M. M. BisschopsJoost van den BrinkDaniel Solis-EscalanteBrigida GalloneDries De MaeyerElise van BaelTom WenseleersJan MichielsKathleen MarchalPascale Daran-LapujadeKevin J. VerstrepenAmerican Society for MicrobiologyarticleCrabtree effectlag phaserespirationSaccharomyces cerevisiaediauxic growthMicrobiologyQR1-502ENmBio, Vol 9, Iss 5 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Crabtree effect lag phase respiration Saccharomyces cerevisiae diauxic growth Microbiology QR1-502
spellingShingle	Crabtree effect lag phase respiration Saccharomyces cerevisiae diauxic growth Microbiology QR1-502 Gemma Perez-Samper Bram Cerulus Abbas Jariani Lieselotte Vermeersch Nuria Barrajón Simancas Markus M. M. Bisschops Joost van den Brink Daniel Solis-Escalante Brigida Gallone Dries De Maeyer Elise van Bael Tom Wenseleers Jan Michiels Kathleen Marchal Pascale Daran-Lapujade Kevin J. Verstrepen The Crabtree Effect Shapes the <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content> Lag Phase during the Switch between Different Carbon Sources
description	ABSTRACT When faced with environmental changes, microbes often enter a temporary growth arrest during which they reprogram the expression of specific genes to adapt to the new conditions. A prime example of such a lag phase occurs when microbes need to switch from glucose to other, less-preferred carbon sources. Despite its industrial relevance, the genetic network that determines the duration of the lag phase has not been studied in much detail. Here, we performed a genome-wide Bar-Seq screen to identify genetic determinants of the Saccharomyces cerevisiae glucose-to-galactose lag phase. The results show that genes involved in respiration, and specifically those encoding complexes III and IV of the electron transport chain, are needed for efficient growth resumption after the lag phase. Anaerobic growth experiments confirmed the importance of respiratory energy conversion in determining the lag phase duration. Moreover, overexpression of the central regulator of respiration, HAP4, leads to significantly shorter lag phases. Together, these results suggest that the glucose-induced repression of respiration, known as the Crabtree effect, is a major determinant of microbial fitness in fluctuating carbon environments. IMPORTANCE The lag phase is arguably one of the prime characteristics of microbial growth. Longer lag phases result in lower competitive fitness in variable environments, and the duration of the lag phase is also important in many industrial processes where long lag phases lead to sluggish, less efficient fermentations. Despite the immense importance of the lag phase, surprisingly little is known about the exact molecular processes that determine its duration. Our study uses the molecular toolbox of S. cerevisiae combined with detailed growth experiments to reveal how the transition from fermentative to respirative metabolism is a key bottleneck for cells to overcome the lag phase. Together, our findings not only yield insight into the key molecular processes and genes that influence lag duration but also open routes to increase the efficiency of industrial fermentations and offer an experimental framework to study other types of lag behavior.
format	article
author	Gemma Perez-Samper Bram Cerulus Abbas Jariani Lieselotte Vermeersch Nuria Barrajón Simancas Markus M. M. Bisschops Joost van den Brink Daniel Solis-Escalante Brigida Gallone Dries De Maeyer Elise van Bael Tom Wenseleers Jan Michiels Kathleen Marchal Pascale Daran-Lapujade Kevin J. Verstrepen
author_facet	Gemma Perez-Samper Bram Cerulus Abbas Jariani Lieselotte Vermeersch Nuria Barrajón Simancas Markus M. M. Bisschops Joost van den Brink Daniel Solis-Escalante Brigida Gallone Dries De Maeyer Elise van Bael Tom Wenseleers Jan Michiels Kathleen Marchal Pascale Daran-Lapujade Kevin J. Verstrepen
author_sort	Gemma Perez-Samper
title	The Crabtree Effect Shapes the <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content> Lag Phase during the Switch between Different Carbon Sources
title_short	The Crabtree Effect Shapes the <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content> Lag Phase during the Switch between Different Carbon Sources
title_full	The Crabtree Effect Shapes the <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content> Lag Phase during the Switch between Different Carbon Sources
title_fullStr	The Crabtree Effect Shapes the <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content> Lag Phase during the Switch between Different Carbon Sources
title_full_unstemmed	The Crabtree Effect Shapes the <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content> Lag Phase during the Switch between Different Carbon Sources
title_sort	crabtree effect shapes the <named-content content-type="genus-species">saccharomyces cerevisiae</named-content> lag phase during the switch between different carbon sources
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/6649b93fa924416e8f37628fe37e2c28
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The Crabtree Effect Shapes the <named-content content-type="genus-species">Saccharomyces cerevisiae</named-content> Lag Phase during the Switch between Different Carbon Sources

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