Constant Growth Rate Can Be Supported by Decreasing Energy Flux and Increasing Aerobic Glycolysis

Fermenting glucose in the presence of enough oxygen to support respiration, known as aerobic glycolysis, is believed to maximize growth rate. We observed increasing aerobic glycolysis during exponential growth, suggesting additional physiological roles for aerobic glycolysis. We investigated such ro...

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Main Authors: Nikolai Slavov, Bogdan A. Budnik, David Schwab, Edoardo M. Airoldi, Alexander van Oudenaarden
Format: Article
Language:English
Published: Elsevier 2014-05-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S221112471400254X
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author Nikolai Slavov
Bogdan A. Budnik
David Schwab
Edoardo M. Airoldi
Alexander van Oudenaarden
author_facet Nikolai Slavov
Bogdan A. Budnik
David Schwab
Edoardo M. Airoldi
Alexander van Oudenaarden
author_sort Nikolai Slavov
collection DOAJ
description Fermenting glucose in the presence of enough oxygen to support respiration, known as aerobic glycolysis, is believed to maximize growth rate. We observed increasing aerobic glycolysis during exponential growth, suggesting additional physiological roles for aerobic glycolysis. We investigated such roles in yeast batch cultures by quantifying O2 consumption, CO2 production, amino acids, mRNAs, proteins, posttranslational modifications, and stress sensitivity in the course of nine doublings at constant rate. During this course, the cells support a constant biomass-production rate with decreasing rates of respiration and ATP production but also decrease their stress resistance. As the respiration rate decreases, so do the levels of enzymes catalyzing rate-determining reactions of the tricarboxylic-acid cycle (providing NADH for respiration) and of mitochondrial folate-mediated NADPH production (required for oxidative defense). The findings demonstrate that exponential growth can represent not a single metabolic/physiological state but a continuum of changing states and that aerobic glycolysis can reduce the energy demands associated with respiratory metabolism and stress survival.
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spelling doaj.art-76bce71237c8417f8b8e1eec4f553c452022-12-21T23:57:13ZengElsevierCell Reports2211-12472014-05-017370571410.1016/j.celrep.2014.03.057Constant Growth Rate Can Be Supported by Decreasing Energy Flux and Increasing Aerobic GlycolysisNikolai Slavov0Bogdan A. Budnik1David Schwab2Edoardo M. Airoldi3Alexander van Oudenaarden4Departments of Physics and Biology and Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA 02139, USADepartment of Statistics and FAS Center for Systems Biology, Harvard University, Cambridge, MA 02138, USADepartment of Physics and Lewis-Sigler Institute, Princeton University, Princeton, NJ 08544, USADepartment of Statistics and FAS Center for Systems Biology, Harvard University, Cambridge, MA 02138, USADepartments of Physics and Biology and Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA 02139, USAFermenting glucose in the presence of enough oxygen to support respiration, known as aerobic glycolysis, is believed to maximize growth rate. We observed increasing aerobic glycolysis during exponential growth, suggesting additional physiological roles for aerobic glycolysis. We investigated such roles in yeast batch cultures by quantifying O2 consumption, CO2 production, amino acids, mRNAs, proteins, posttranslational modifications, and stress sensitivity in the course of nine doublings at constant rate. During this course, the cells support a constant biomass-production rate with decreasing rates of respiration and ATP production but also decrease their stress resistance. As the respiration rate decreases, so do the levels of enzymes catalyzing rate-determining reactions of the tricarboxylic-acid cycle (providing NADH for respiration) and of mitochondrial folate-mediated NADPH production (required for oxidative defense). The findings demonstrate that exponential growth can represent not a single metabolic/physiological state but a continuum of changing states and that aerobic glycolysis can reduce the energy demands associated with respiratory metabolism and stress survival.http://www.sciencedirect.com/science/article/pii/S221112471400254X
spellingShingle Nikolai Slavov
Bogdan A. Budnik
David Schwab
Edoardo M. Airoldi
Alexander van Oudenaarden
Constant Growth Rate Can Be Supported by Decreasing Energy Flux and Increasing Aerobic Glycolysis
Cell Reports
title Constant Growth Rate Can Be Supported by Decreasing Energy Flux and Increasing Aerobic Glycolysis
title_full Constant Growth Rate Can Be Supported by Decreasing Energy Flux and Increasing Aerobic Glycolysis
title_fullStr Constant Growth Rate Can Be Supported by Decreasing Energy Flux and Increasing Aerobic Glycolysis
title_full_unstemmed Constant Growth Rate Can Be Supported by Decreasing Energy Flux and Increasing Aerobic Glycolysis
title_short Constant Growth Rate Can Be Supported by Decreasing Energy Flux and Increasing Aerobic Glycolysis
title_sort constant growth rate can be supported by decreasing energy flux and increasing aerobic glycolysis
url http://www.sciencedirect.com/science/article/pii/S221112471400254X
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AT davidschwab constantgrowthratecanbesupportedbydecreasingenergyfluxandincreasingaerobicglycolysis
AT edoardomairoldi constantgrowthratecanbesupportedbydecreasingenergyfluxandincreasingaerobicglycolysis
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