Central carbon metabolism of Saccharomyces cerevisiae in anaerobic, oxygen-limited and fully aerobic steady-state conditions and following a shift to anaerobic conditions

Marilyn G. Wiebe (Corresponding Author), Eija Rintala, Anu Tamminen, Helena Simolin, Laura Salusjärvi, Mervi Toivari, Juha T. Kokkonen, Jari Kiuru, Raimo A. Ketola, Paula Jouhten, Anne Huuskonen, Hannu Maaheimo, Laura Ruohonen, Merja Penttilä

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Abstract

Saccharomyces cerevisiae CEN.PK113-1A was grown in glucose-limited chemostat culture with 0%, 0.5%, 1.0%, 2.8% or 20.9% O2 in the inlet gas (D=0.10 h-1, pH 5, 30°C) to determine the effects of oxygen on 17 metabolites and 69 genes related to central carbon metabolism. The concentrations of tricarboxylic acid cycle (TCA) metabolites and all glycolytic metabolites except 2-phosphoglycerate+3-phosphoglycerate and phosphoenolpyruvate were higher in anaerobic than in fully aerobic conditions. Provision of only 0.5-1% O2 reduced the concentrations of most metabolites, as compared with anaerobic conditions. Transcription of most genes analyzed was reduced in 0%, 0.5% or 1.0% O2 relative to cells grown in 2.8% or 20.9% O 2. Ethanol production was observed with 2.8% or less O2. After steady-state analysis in defined oxygen concentrations, the conditions were switched from aerobic to anaerobic. Metabolite and transcript levels were monitored for up to 96 h after the transition, and this showed that more than 30 h was required for the cells to fully adapt to anaerobiosis. Levels of metabolites of upper glycolysis and the TCA cycle increased following the transition to anaerobic conditions, whereas those of metabolites of lower glycolysis generally decreased. Gene regulation was more complex, with some genes showing transient upregulation or downregulation during the adaptation to anaerobic conditions.

Original languageEnglish
Pages (from-to)140-154
JournalFEMS Yeast Research
Volume8
Issue number1
DOIs
Publication statusPublished - 1 Feb 2008
MoE publication typeA1 Journal article-refereed

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Saccharomyces cerevisiae
Carbon
Oxygen
Citric Acid Cycle
Glycolysis
Genes
Anaerobiosis
Phosphoenolpyruvate
Ethanol
Up-Regulation
Down-Regulation
Gases
Glucose

Keywords

  • Gene transcription
  • Hypoxic transient
  • Metabolites
  • Oxygen
  • Saccharomyces cerevisiae
  • Systems biology

Cite this

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title = "Central carbon metabolism of Saccharomyces cerevisiae in anaerobic, oxygen-limited and fully aerobic steady-state conditions and following a shift to anaerobic conditions",
abstract = "Saccharomyces cerevisiae CEN.PK113-1A was grown in glucose-limited chemostat culture with 0{\%}, 0.5{\%}, 1.0{\%}, 2.8{\%} or 20.9{\%} O2 in the inlet gas (D=0.10 h-1, pH 5, 30°C) to determine the effects of oxygen on 17 metabolites and 69 genes related to central carbon metabolism. The concentrations of tricarboxylic acid cycle (TCA) metabolites and all glycolytic metabolites except 2-phosphoglycerate+3-phosphoglycerate and phosphoenolpyruvate were higher in anaerobic than in fully aerobic conditions. Provision of only 0.5-1{\%} O2 reduced the concentrations of most metabolites, as compared with anaerobic conditions. Transcription of most genes analyzed was reduced in 0{\%}, 0.5{\%} or 1.0{\%} O2 relative to cells grown in 2.8{\%} or 20.9{\%} O 2. Ethanol production was observed with 2.8{\%} or less O2. After steady-state analysis in defined oxygen concentrations, the conditions were switched from aerobic to anaerobic. Metabolite and transcript levels were monitored for up to 96 h after the transition, and this showed that more than 30 h was required for the cells to fully adapt to anaerobiosis. Levels of metabolites of upper glycolysis and the TCA cycle increased following the transition to anaerobic conditions, whereas those of metabolites of lower glycolysis generally decreased. Gene regulation was more complex, with some genes showing transient upregulation or downregulation during the adaptation to anaerobic conditions.",
keywords = "Gene transcription, Hypoxic transient, Metabolites, Oxygen, Saccharomyces cerevisiae, Systems biology",
author = "Wiebe, {Marilyn G.} and Eija Rintala and Anu Tamminen and Helena Simolin and Laura Salusj{\"a}rvi and Mervi Toivari and Kokkonen, {Juha T.} and Jari Kiuru and Ketola, {Raimo A.} and Paula Jouhten and Anne Huuskonen and Hannu Maaheimo and Laura Ruohonen and Merja Penttil{\"a}",
year = "2008",
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language = "English",
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T1 - Central carbon metabolism of Saccharomyces cerevisiae in anaerobic, oxygen-limited and fully aerobic steady-state conditions and following a shift to anaerobic conditions

AU - Wiebe, Marilyn G.

AU - Rintala, Eija

AU - Tamminen, Anu

AU - Simolin, Helena

AU - Salusjärvi, Laura

AU - Toivari, Mervi

AU - Kokkonen, Juha T.

AU - Kiuru, Jari

AU - Ketola, Raimo A.

AU - Jouhten, Paula

AU - Huuskonen, Anne

AU - Maaheimo, Hannu

AU - Ruohonen, Laura

AU - Penttilä, Merja

PY - 2008/2/1

Y1 - 2008/2/1

N2 - Saccharomyces cerevisiae CEN.PK113-1A was grown in glucose-limited chemostat culture with 0%, 0.5%, 1.0%, 2.8% or 20.9% O2 in the inlet gas (D=0.10 h-1, pH 5, 30°C) to determine the effects of oxygen on 17 metabolites and 69 genes related to central carbon metabolism. The concentrations of tricarboxylic acid cycle (TCA) metabolites and all glycolytic metabolites except 2-phosphoglycerate+3-phosphoglycerate and phosphoenolpyruvate were higher in anaerobic than in fully aerobic conditions. Provision of only 0.5-1% O2 reduced the concentrations of most metabolites, as compared with anaerobic conditions. Transcription of most genes analyzed was reduced in 0%, 0.5% or 1.0% O2 relative to cells grown in 2.8% or 20.9% O 2. Ethanol production was observed with 2.8% or less O2. After steady-state analysis in defined oxygen concentrations, the conditions were switched from aerobic to anaerobic. Metabolite and transcript levels were monitored for up to 96 h after the transition, and this showed that more than 30 h was required for the cells to fully adapt to anaerobiosis. Levels of metabolites of upper glycolysis and the TCA cycle increased following the transition to anaerobic conditions, whereas those of metabolites of lower glycolysis generally decreased. Gene regulation was more complex, with some genes showing transient upregulation or downregulation during the adaptation to anaerobic conditions.

AB - Saccharomyces cerevisiae CEN.PK113-1A was grown in glucose-limited chemostat culture with 0%, 0.5%, 1.0%, 2.8% or 20.9% O2 in the inlet gas (D=0.10 h-1, pH 5, 30°C) to determine the effects of oxygen on 17 metabolites and 69 genes related to central carbon metabolism. The concentrations of tricarboxylic acid cycle (TCA) metabolites and all glycolytic metabolites except 2-phosphoglycerate+3-phosphoglycerate and phosphoenolpyruvate were higher in anaerobic than in fully aerobic conditions. Provision of only 0.5-1% O2 reduced the concentrations of most metabolites, as compared with anaerobic conditions. Transcription of most genes analyzed was reduced in 0%, 0.5% or 1.0% O2 relative to cells grown in 2.8% or 20.9% O 2. Ethanol production was observed with 2.8% or less O2. After steady-state analysis in defined oxygen concentrations, the conditions were switched from aerobic to anaerobic. Metabolite and transcript levels were monitored for up to 96 h after the transition, and this showed that more than 30 h was required for the cells to fully adapt to anaerobiosis. Levels of metabolites of upper glycolysis and the TCA cycle increased following the transition to anaerobic conditions, whereas those of metabolites of lower glycolysis generally decreased. Gene regulation was more complex, with some genes showing transient upregulation or downregulation during the adaptation to anaerobic conditions.

KW - Gene transcription

KW - Hypoxic transient

KW - Metabolites

KW - Oxygen

KW - Saccharomyces cerevisiae

KW - Systems biology

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DO - 10.1111/j.1567-1364.2007.00234.x

M3 - Article

C2 - 17425669

AN - SCOPUS:38349121328

VL - 8

SP - 140

EP - 154

JO - FEMS Yeast Research

JF - FEMS Yeast Research

SN - 1567-1356

IS - 1

ER -