ArticleThe Journal of biological chemistry2012
13C-flux analysis reveals NADPH-balancing transhydrogenation cycles in stationary phase of nitrogen-starving Bacillus subtilis.
Article in The Journal of biological chemistry, 2012. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 23 papers.
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Who cites it
23 citing papers in PubMed, 59 citations in OpenAlex.
- Advances in genome-scale metabolic modeling of Bacillus subtilis.Biotechnology letters · 2026Review
- Acetol biosynthesis enables NADPH balance during nitrogen limitation in engineered Escherichia coli.Microbial cell factories · 2025Article
- Local flux coordination and global gene expression regulation in metabolic modeling.Nature communications · 2023Article
- A Programmable CRISPR/Cas9 Toolkit Improves Lycopene Production in Bacillus subtilis.Applied and environmental microbiology · 2023Article
- Constitutive glucose dehydrogenase elevates intracellular NADPH levels and luciferase luminescence in Bacillus subtilis.Microbial cell factories · 2022Article
- The coordinated population redistribution betweenBiofilm · 2022Article
- Article
- Disruption of the Oxidative Pentose Phosphate Pathway Stimulates High-Yield Production Using Resting Corynebacterium glutamicum in the Absence of External Electron Acceptors.Applied and environmental microbiology · 2020Article
- High-level production of poly-γ-glutamic acid from untreated molasses by Bacillus siamensis IR10.Microbial cell factories · 2020Article
- Different Metabolomic Responses to Carbon Starvation between Light and Dark Conditions in the Purple Photosynthetic Bacterium, Rhodopseudomonas palustris.Microbes and environments · 2018Article
- Reverse engineering the cancer metabolic network using flux analysis to understand drivers of human disease.Metabolic engineering · 2018Review
- A new-generation of Bacillus subtilis cell factory for further elevated scyllo-inositol production.Microbial cell factories · 2017Article
- Spatiotemporal Analysis of a Glycolytic Activity Gradient Linked to Mouse Embryo Mesoderm Development.Developmental cell · 2017Article
- The Blueprint of a Minimal Cell: MiniBacillus.Microbiology and molecular biology reviews : MMBR · 2016Review
- Transhydrogenase promotes the robustness and evolvability of E. coli deficient in NADPH production.PLoS genetics · 2015Article
- Estimating relative changes of metabolic fluxes.PLoS computational biology · 2014Article
- The key to acetate: metabolic fluxes of acetic acid bacteria under cocoa pulp fermentation-simulating conditions.Applied and environmental microbiology · 2014Article
- Tracing compartmentalized NADPH metabolism in the cytosol and mitochondria of mammalian cells.Molecular cell · 2014Article
- Reliable Metabolic Flux Estimation in Escherichia coli Central Carbon Metabolism Using Intracellular Free Amino Acids.Metabolites · 2014Article
- Environmental dependence of stationary-phase metabolism in Bacillus subtilis and Escherichia coli.Applied and environmental microbiology · 2014Article
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Authors and funding
4 authors at 2 institutions in 2 countries.
Funding
No grant is acknowledged in the PubMed record.
Abstract
In their natural habitat, microorganisms are typically confronted with nutritional limitations that restrict growth and force them to persevere in a stationary phase. Despite the importance of this phase, little is known about the metabolic state(s) that sustains it. Here, we investigate metabolically active but non-growing Bacillus subtilis during nitrogen starvation. In the absence of biomass formation as the major NADPH sink, the intracellular flux distribution in these resting B. subtilis reveals a large apparent catabolic NADPH overproduction of 5.0 ± 0.6 mmol g(-1)h(-1) that was partly caused by high pentose phosphate pathway fluxes. Combining transcriptome analysis, stationary (13)C-flux analysis in metabolic deletion mutants, (2)H-labeling experiments, and kinetic flux profiling, we demonstrate that about half of the catabolic excess NADPH is oxidized by two transhydrogenation cycles, i.e. isoenzyme pairs of dehydrogenases with different cofactor specificities that operate in reverse directions. These transhydrogenation cycles were constituted by the combined activities of the glyceraldehyde 3-phosphate dehydrogenases GapA/GapB and the malic enzymes MalS/YtsJ. At least an additional 6% of the overproduced NADPH is reoxidized by continuous cycling between ana- and catabolism of glutamate. Furthermore, in vitro enzyme data show that a not yet identified transhydrogenase could potentially reoxidize ∼20% of the overproduced NADPH. Overall, we demonstrate the interplay between several metabolic mechanisms that concertedly enable network-wide NADPH homeostasis under conditions of high catabolic NADPH production in the absence of cell growth in B. subtilis.
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