Light/dark cycling causes delayed lipid accumulation and increased photoperiod-based biomass yield by altering metabolic flux in oleaginous Chlamydomonas sp.

Yuichi Kato, Yusuke Fujihara, Christopher J. Vavricka, Jo Shu Chang, Tomohisa Hasunuma, Akihiko Kondo

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

Background: Light/dark cycling is an inevitable outdoor culture condition for microalgal biofuel production; however, the influence of this cycling on cellular lipid production has not been clearly established. The general aim of this study was to determine the influence of light/dark cycling on microalgal biomass production and lipid accumulation. To achieve this goal, specific causative mechanisms were investigated using a metabolomics approach. Laboratory scale photoautotrophic cultivations of the oleaginous green microalga Chlamydomonas sp. JSC4 were performed under continuous light (LL) and light/dark (LD) conditions. Results: Lipid accumulation and carbohydrate degradation were delayed under the LD condition compared with that under the LL condition. Metabolomic analysis revealed accumulation of phosphoenolpyruvate and decrease of glycerol 3-phosphate under the LD condition, suggesting that the imbalance of these metabolites is a source of delayed lipid accumulation. When accounting for light dosage, biomass yield under the LD condition was significantly higher than that under the LL condition. Dynamic metabolic profiling showed higher levels of lipid/carbohydrate anabolism (including production of 3-phosphoglycerate, fructose 6-phosphate, glucose 6-phosphate, phosphoenolpyruvate and acetyl-CoA) from CO 2 under the LD condition, indicating higher CO 2 fixation than that of the LL condition. Conclusions: Photoperiods define lipid accumulation and biomass production, and light/dark cycling was determined as a critical obstacle for lipid production in JSC4. Conversions of phosphoenolpyruvate to pyruvate and 3-phosphoglycerate to glycerol 3-phosphate are the candidate rate-limiting steps responsible for delayed lipid accumulation. The accumulation of substrates including ribulose 5-phosphate could be explained by the close relationship of increased biomass yield with enhanced CO 2 fixation. The present study investigated the influence of light/dark cycling on lipid production by direct comparison with continuous illumination for the first time, and revealed underlying metabolic mechanisms and candidate metabolic rate-limiting steps during light/dark cycling. These findings suggest promising targets to metabolically engineer improved lipid production.

Original languageEnglish
Article number39
JournalBiotechnology for Biofuels
Volume12
Issue number1
DOIs
Publication statusPublished - 2019 Feb 21

Fingerprint

Chlamydomonas
Photoperiod
photoperiod
Biomass
Lipids
lipid
Fluxes
Light
biomass
Phosphates
Phosphoenolpyruvate
phosphate
Carbon Monoxide
Metabolomics
Carbohydrates
Glycerol
fixation
carbohydrate
Glucose-6-Phosphate
Acetyl Coenzyme A

All Science Journal Classification (ASJC) codes

  • Biotechnology
  • Applied Microbiology and Biotechnology
  • Renewable Energy, Sustainability and the Environment
  • Energy(all)
  • Management, Monitoring, Policy and Law

Cite this

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title = "Light/dark cycling causes delayed lipid accumulation and increased photoperiod-based biomass yield by altering metabolic flux in oleaginous Chlamydomonas sp.",
abstract = "Background: Light/dark cycling is an inevitable outdoor culture condition for microalgal biofuel production; however, the influence of this cycling on cellular lipid production has not been clearly established. The general aim of this study was to determine the influence of light/dark cycling on microalgal biomass production and lipid accumulation. To achieve this goal, specific causative mechanisms were investigated using a metabolomics approach. Laboratory scale photoautotrophic cultivations of the oleaginous green microalga Chlamydomonas sp. JSC4 were performed under continuous light (LL) and light/dark (LD) conditions. Results: Lipid accumulation and carbohydrate degradation were delayed under the LD condition compared with that under the LL condition. Metabolomic analysis revealed accumulation of phosphoenolpyruvate and decrease of glycerol 3-phosphate under the LD condition, suggesting that the imbalance of these metabolites is a source of delayed lipid accumulation. When accounting for light dosage, biomass yield under the LD condition was significantly higher than that under the LL condition. Dynamic metabolic profiling showed higher levels of lipid/carbohydrate anabolism (including production of 3-phosphoglycerate, fructose 6-phosphate, glucose 6-phosphate, phosphoenolpyruvate and acetyl-CoA) from CO 2 under the LD condition, indicating higher CO 2 fixation than that of the LL condition. Conclusions: Photoperiods define lipid accumulation and biomass production, and light/dark cycling was determined as a critical obstacle for lipid production in JSC4. Conversions of phosphoenolpyruvate to pyruvate and 3-phosphoglycerate to glycerol 3-phosphate are the candidate rate-limiting steps responsible for delayed lipid accumulation. The accumulation of substrates including ribulose 5-phosphate could be explained by the close relationship of increased biomass yield with enhanced CO 2 fixation. The present study investigated the influence of light/dark cycling on lipid production by direct comparison with continuous illumination for the first time, and revealed underlying metabolic mechanisms and candidate metabolic rate-limiting steps during light/dark cycling. These findings suggest promising targets to metabolically engineer improved lipid production.",
author = "Yuichi Kato and Yusuke Fujihara and Vavricka, {Christopher J.} and Chang, {Jo Shu} and Tomohisa Hasunuma and Akihiko Kondo",
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Light/dark cycling causes delayed lipid accumulation and increased photoperiod-based biomass yield by altering metabolic flux in oleaginous Chlamydomonas sp. / Kato, Yuichi; Fujihara, Yusuke; Vavricka, Christopher J.; Chang, Jo Shu; Hasunuma, Tomohisa; Kondo, Akihiko.

In: Biotechnology for Biofuels, Vol. 12, No. 1, 39, 21.02.2019.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Light/dark cycling causes delayed lipid accumulation and increased photoperiod-based biomass yield by altering metabolic flux in oleaginous Chlamydomonas sp.

AU - Kato, Yuichi

AU - Fujihara, Yusuke

AU - Vavricka, Christopher J.

AU - Chang, Jo Shu

AU - Hasunuma, Tomohisa

AU - Kondo, Akihiko

PY - 2019/2/21

Y1 - 2019/2/21

N2 - Background: Light/dark cycling is an inevitable outdoor culture condition for microalgal biofuel production; however, the influence of this cycling on cellular lipid production has not been clearly established. The general aim of this study was to determine the influence of light/dark cycling on microalgal biomass production and lipid accumulation. To achieve this goal, specific causative mechanisms were investigated using a metabolomics approach. Laboratory scale photoautotrophic cultivations of the oleaginous green microalga Chlamydomonas sp. JSC4 were performed under continuous light (LL) and light/dark (LD) conditions. Results: Lipid accumulation and carbohydrate degradation were delayed under the LD condition compared with that under the LL condition. Metabolomic analysis revealed accumulation of phosphoenolpyruvate and decrease of glycerol 3-phosphate under the LD condition, suggesting that the imbalance of these metabolites is a source of delayed lipid accumulation. When accounting for light dosage, biomass yield under the LD condition was significantly higher than that under the LL condition. Dynamic metabolic profiling showed higher levels of lipid/carbohydrate anabolism (including production of 3-phosphoglycerate, fructose 6-phosphate, glucose 6-phosphate, phosphoenolpyruvate and acetyl-CoA) from CO 2 under the LD condition, indicating higher CO 2 fixation than that of the LL condition. Conclusions: Photoperiods define lipid accumulation and biomass production, and light/dark cycling was determined as a critical obstacle for lipid production in JSC4. Conversions of phosphoenolpyruvate to pyruvate and 3-phosphoglycerate to glycerol 3-phosphate are the candidate rate-limiting steps responsible for delayed lipid accumulation. The accumulation of substrates including ribulose 5-phosphate could be explained by the close relationship of increased biomass yield with enhanced CO 2 fixation. The present study investigated the influence of light/dark cycling on lipid production by direct comparison with continuous illumination for the first time, and revealed underlying metabolic mechanisms and candidate metabolic rate-limiting steps during light/dark cycling. These findings suggest promising targets to metabolically engineer improved lipid production.

AB - Background: Light/dark cycling is an inevitable outdoor culture condition for microalgal biofuel production; however, the influence of this cycling on cellular lipid production has not been clearly established. The general aim of this study was to determine the influence of light/dark cycling on microalgal biomass production and lipid accumulation. To achieve this goal, specific causative mechanisms were investigated using a metabolomics approach. Laboratory scale photoautotrophic cultivations of the oleaginous green microalga Chlamydomonas sp. JSC4 were performed under continuous light (LL) and light/dark (LD) conditions. Results: Lipid accumulation and carbohydrate degradation were delayed under the LD condition compared with that under the LL condition. Metabolomic analysis revealed accumulation of phosphoenolpyruvate and decrease of glycerol 3-phosphate under the LD condition, suggesting that the imbalance of these metabolites is a source of delayed lipid accumulation. When accounting for light dosage, biomass yield under the LD condition was significantly higher than that under the LL condition. Dynamic metabolic profiling showed higher levels of lipid/carbohydrate anabolism (including production of 3-phosphoglycerate, fructose 6-phosphate, glucose 6-phosphate, phosphoenolpyruvate and acetyl-CoA) from CO 2 under the LD condition, indicating higher CO 2 fixation than that of the LL condition. Conclusions: Photoperiods define lipid accumulation and biomass production, and light/dark cycling was determined as a critical obstacle for lipid production in JSC4. Conversions of phosphoenolpyruvate to pyruvate and 3-phosphoglycerate to glycerol 3-phosphate are the candidate rate-limiting steps responsible for delayed lipid accumulation. The accumulation of substrates including ribulose 5-phosphate could be explained by the close relationship of increased biomass yield with enhanced CO 2 fixation. The present study investigated the influence of light/dark cycling on lipid production by direct comparison with continuous illumination for the first time, and revealed underlying metabolic mechanisms and candidate metabolic rate-limiting steps during light/dark cycling. These findings suggest promising targets to metabolically engineer improved lipid production.

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