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: Slavov, Nikolai, Budnik, Bogdan A., Schwab, David, Airoldi, Edoardo M., van Oudenaarden, Alexander
Other Authors: Massachusetts Institute of Technology. Department of Biology
Format: Article
Language:en_US
Published: Elsevier 2015
Online Access:http://hdl.handle.net/1721.1/96921
https://orcid.org/0000-0003-2035-1820
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author Slavov, Nikolai
Budnik, Bogdan A.
Schwab, David
Airoldi, Edoardo M.
van Oudenaarden, Alexander
author2 Massachusetts Institute of Technology. Department of Biology
author_facet Massachusetts Institute of Technology. Department of Biology
Slavov, Nikolai
Budnik, Bogdan A.
Schwab, David
Airoldi, Edoardo M.
van Oudenaarden, Alexander
author_sort Slavov, Nikolai
collection MIT
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 O[subscript 2] consumption, CO[subscript 2] 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 mit-1721.1/969212022-10-02T08:33:39Z Constant Growth Rate Can Be Supported by Decreasing Energy Flux and Increasing Aerobic Glycolysis Slavov, Nikolai Budnik, Bogdan A. Schwab, David Airoldi, Edoardo M. van Oudenaarden, Alexander Massachusetts Institute of Technology. Department of Biology Massachusetts Institute of Technology. Department of Physics Koch Institute for Integrative Cancer Research at MIT Slavov, Nikolai Slavov, Nikolai van Oudenaarden, Alexander 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 O[subscript 2] consumption, CO[subscript 2] 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. National Institutes of Health (U.S.) (Grant DP1 CA174420) National Institutes of Health (U.S.) (Grant R01-GM068957) National Institutes of Health (U.S.) (Grant U54CA143874) 2015-05-06T13:47:45Z 2015-05-06T13:47:45Z 2014-04 2014-02 Article http://purl.org/eprint/type/JournalArticle 22111247 http://hdl.handle.net/1721.1/96921 Slavov, Nikolai, Bogdan A. Budnik, David Schwab, Edoardo M. Airoldi, and Alexander van Oudenaarden. “Constant Growth Rate Can Be Supported by Decreasing Energy Flux and Increasing Aerobic Glycolysis.” Cell Reports 7, no. 3 (May 2014): 705–714. https://orcid.org/0000-0003-2035-1820 en_US http://dx.doi.org/10.1016/j.celrep.2014.03.057 Cell Reports Creative Commons Attribution http://creativecommons.org/licenses/by/3.0/ application/pdf Elsevier Slavov
spellingShingle Slavov, Nikolai
Budnik, Bogdan A.
Schwab, David
Airoldi, Edoardo M.
van Oudenaarden, Alexander
Constant Growth Rate Can Be Supported by Decreasing Energy Flux and Increasing Aerobic Glycolysis
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://hdl.handle.net/1721.1/96921
https://orcid.org/0000-0003-2035-1820
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