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Dynamic metabolic profiling of cyanobacterial glycogen biosynthesis under conditions of nitrate depletion
Open accessAbstract
Cyanobacteria represent a globally important biomass because they are responsible for a substantial proportion of primary production in the hydrosphere. Arthrospira platensis is a fast-growing halophilic cyanobacterium capable of accumulating glycogen and has the potential to serve as a feedstock in the fermentative production of third-generation biofuels. Accordingly, enhancing cyanobacterial glycogen production is a promising biofuel production strategy. However, the regulatory mechanism of glycogen metabolism in cyanobacteria is poorly understood. The aim of the present study was to determine the metabolic flux of glycogen biosynthesis using a dynamic metabolomic approach. Time-course profiling of widely targeted cyanobacterial metabolic intermediates demonstrated a global metabolic reprogramming that involves transient increases in the levels of some amino acids during the glycogen production phase induced by nitrate depletion. Also, in vivo labelling with NaH(13)CO3 enabled direct measurement of metabolic intermediate turnover in A. platensis, revealing that under conditions of nitrate depletion glycogen is biosynthesized with carbon derived from amino acids released from proteins via gluconeogenesis. This dynamic metabolic profiling approach provided conclusive evidence of temporal alterations in the metabolic profile in cyanobacterial cells.
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“In the presence of nitrate, the glycogen and protein contents remained nearly constant at ~15% DW and ~50% DW, respectively.”
From Arthrospira platensis as a Feasible Feedstock for Bioethanol Production (2021) · cites this paper as [64]
In the citing paper
“Time-course profiling of metabolites demonstrated transient increases in the levels of other amino acids (glycine, histidine, isoleucine, leucine, methionine, phenylalanine, proline, threonine, and tyrosine).”
From Arthrospira platensis as a Feasible Feedstock for Bioethanol Production (2021) · cites this paper as [64]
In the citing paper
“Analyzing the metabolic intermediates, they observed that shifting the cyanobacterial cells into nitrogen depletion and cultivating them for 72 h resulted in global metabolic modifications that involved reductions in the levels of several free amino acids (aspartate, glutamate, and glutamine), and increased in the levels of organic acids (2-ketoglutarate, malate, and succinate).”
From Arthrospira platensis as a Feasible Feedstock for Bioethanol Production (2021) · cites this paper as [64]
In the citing paper
“In contrast, in the absence of nitrate, the glycogen content increased to 63.2% DW while the protein content decreased to 15.4%.”
From Arthrospira platensis as a Feasible Feedstock for Bioethanol Production (2021) · cites this paper as [64]
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“1 3 The previous study of nitrogen-deprived Arthrospira and Synechocystis found the transient increase in amino acid levels concomitant with glycogen production which suggest that glycogen is biosynthesized from carbons derived from amino acids released from proteins via gluconeogenesis (Hasunuma et al. 2013).”
BackgroundUy, A. L. T., Yamamoto, A., Matsuda, M., Arae, T., Hasunuma, T., Demura, T., & Ohtani, M. (2023) · Plant and Cell Physiology · doi:10.1093/pcp/pcad130 · Cited by 10
“Carbon 13 ( 13 C) is currently the most popular tracer used in metabolic flux analysis in microbes, animals and plants (Hasunuma et al. 2010, 2013, 2018, Crown and Antoniewicz 2013, Zhang et al. 2018, Tanaka et al. 2022).”
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“Regarding cyanobacteria, the metabolism of nitrogen and carbon is functionally bridged; thus, nitrogen limitation will lead to excessive carbon accumulation (Hasunuma et al. 2013; Yue et al. 2015), which will accelerate the sedimentation of algae.”
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“The method to extract metabolites from the medium (Yukawa et al., 2021) and cells (Inokuma et al., 2018), and running parameters (Hasunuma et al., 2013) was described in the previous reports. pH in the fermentation medium was determined using compact pH meter (LAQUA twin; HORIBA,).”
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“In fact, nitrogen deficiency adaptation is characterized by an increase in the C/N ratio, leading to accumulation of glycogen, partially supported by carbon recycled from degraded phycobiliproteins (Figure 1c and Hasunuma et al. 2013; Ortega-Martínez et al. 2023).”
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“Although it has previously been elucidated that glycogen production increases upon limitation of another nutrient, such as nitrogen (Hasunuma et al. 2013), this approach may not be as useful when the aim is also to enhance the overall growth and, hence, the total biomass of the cyanobacterial cells.”
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Metadata
- Authors
- Hasunuma, T., Kikuyama, F., Matsuda, M., Aikawa, S., Izumi, Y., & Kondo, A.
- Affiliations
- Japan Science and Technology Agency (JP)
- Kobe University (JP)
- Corresponding author
- Hasunuma, Tomohisa
- Venue
- Journal of Experimental Botany
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-05-08
- Volume
- 64
- Issue
- 10
- Pages
- 2943-2954
- ISSN
- 0022-0957 (ISSN-L)
- 1460-2431
- PMC
- PMC3697948
- OpenAlex
- W2103644949
- Cited by
- 160
- References
- 45
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 10 · 2023: 8 · 2022: 16 · 2021: 18 · 2020: 10 · 2019: 15 · 2018: 12 · 2017: 12 · 2016: 17 · 2015: 13 · 2014: 17 · 2013: 1
- FWCI
- 7.16
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- Journal of Experimental Botany (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Funders
- Japan Science and Technology Agency
- Precursory Research for Embryonic Science and Technology
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Algal biology and biofuel production
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
- Keywords
- Spirulina platensis, nitrate depletion, metabolic flux, metabolic reprogramming, amino acid accumulation, gluconeogenesis, metabolic intermediates, third-generation biofuels, halophilic cyanobacteria
- MeSH terms
- Cyanobacteria, Amino Acids, Gluconeogenesis, Glycogen, Nitrates, Metabolome, Biofuels
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