Characterization of trophic changes and a functional oxidative pentose phosphate pathway in Synechocystis sp. PCC 6803

Jansén, Tove; Kurian, Dominic; Raksajit, Wuttinun; York, Steve; Summers, Michael L.; Mäenpää, Pekka H.

doi:10.1007/s11738-009-0428-7

Cited by 14 publications

(10 citation statements)

References 24 publications

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“…Cyanobacteria have long been thought to degrade glucose mainly via the OPP pathway, rather than the EMP pathway (10,13,21,26). Furthermore, cyanobacterial glycolytic routes were perceived of being foremost important under heterotrophic conditions in the dark (10,13).…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, cyanobacterial glycolytic routes were perceived of being foremost important under heterotrophic conditions in the dark (10,13). However, evidence is accumulating that mixotrophy (uptake of organic carbon in the light) among phototrophic cyanobacteria and algae has been dramatically underestimated, especially in aquatic habitats (27,28).…”

Section: Discussionmentioning

confidence: 99%

“…Synechocystis is thought to phosphorylate glucose via glucokinase to glucose-6P, which is then further oxidized either via the EMP pathway or the OPP pathway ( Fig. 1) (13). We wondered whether the ΔpfkΔzwf mutant might bypass glucokinase via a concerted action of a glucose dehydrogenase (Gdh) and a gluconate kinase to form 6P-gluconate, which could then be further metabolized via Gnd in the OPP pathway ( Figs.…”

Section: Growth Behavior Of Mutants Missing Selected Enzymes Of Knownmentioning

confidence: 99%

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The Entner–Doudoroff pathway is an overlooked glycolytic route in cyanobacteria and plants

Chen

Schreiber

Appel

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

162

191

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Glucose degradation pathways are central for energy and carbon metabolism throughout all domains of life. They provide ATP, NAD(P)H, and biosynthetic precursors for amino acids, nucleotides, and fatty acids. It is general knowledge that cyanobacteria and plants oxidize carbohydrates via glycolysis [the Embden-Meyerhof-Parnas (EMP) pathway] and the oxidative pentose phosphate (OPP) pathway. However, we found that both possess a third, previously overlooked pathway of glucose breakdown: the Entner-Doudoroff (ED) pathway. Its key enzyme, 2-keto-3-deoxygluconate-6-phosphate (KDPG) aldolase, is widespread in cyanobacteria, moss, fern, algae, and plants and is even more common among cyanobacteria than phosphofructokinase (PFK), the key enzyme of the EMP pathway. Active KDPG aldolases from the cyanobacterium Synechocystis and the plant barley (Hordeum vulgare) were biochemically characterized in vitro. KDPG, a metabolite unique to the ED pathway, was detected in both in vivo, indicating an active ED pathway. Phylogenetic analyses revealed that photosynthetic eukaryotes acquired KDPG aldolase from the cyanobacterial ancestors of plastids via endosymbiotic gene transfer. Several Synechocystis mutants in which key enzymes of all three glucose degradation pathways were knocked out indicate that the ED pathway is physiologically significant, especially under mixotrophic conditions (light and glucose) and under autotrophic conditions in a day/ night cycle, which is probably the most common condition encountered in nature. The ED pathway has lower protein costs and ATP yields than the EMP pathway, in line with the observation that oxygenic photosynthesizers are nutrient-limited, rather than ATP-limited. Furthermore, the ED pathway does not generate futile cycles in organisms that fix CO 2 via the Calvin-Benson cycle. T he breakdown of glucose is central for energy and biosynthetic metabolism throughout all domains of life. The Embden-Meyerhof-Parnas (EMP) pathway (glycolysis) and the oxidative pentose phosphate (OPP) pathway are the backbones of eukaryotic carbon and energy metabolism (1, 2). They generate ATP, NAD(P)H, and biosynthetic precursors for amino acids, nucleotides, and fatty acids. Prokaryotes, in contrast, exhibit a broad diversity in sugar oxidation pathways (3-5). These routes differ in ATP yield, in the enzymes and cofactors involved, and in the chemical intermediates of the pathways. The most common glycolytic routes in prokaryotes are the EMP, ED, and OPP pathways (Fig. 1). The key enzyme unique to the ED pathway is 2-keto-3-deoxygluconate-6-phosphate (KDPG) aldolase (Eda), whereas phosphofructokinase (PFK) is unique to the EMP pathway in the catabolic direction (3, 6). KDPG as a metabolite is exclusively found in the ED pathway (Fig. 1). The first two steps of the OPP pathway are catalyzed by glucose 6-phosphate-dehydrogenase (Zwf) and 6-phosphogluconate dehydrogenase (Gnd). As the pentose phosphate pathway can either run in its oxidative mode (OPP pathway) to oxidize carbohydrates or in its reductive mode ...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Growth Behavior Of Mutants Missing Selected Enzymes Of Knownmentioning

confidence: 99%

See 1 more Smart Citation

The Entner–Doudoroff pathway is an overlooked glycolytic route in cyanobacteria and plants

Chen

Schreiber

Appel

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

162

191

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“…Moreover, metabolic flux analysis indicated elevated flux of the oxidative PPP under dark heterotrophic conditions [15]. Furthermore, deletion of the zwf gene, which encodes glucose‐6‐phosphate dehydrogenase, the first enzyme of oxidative PPP, prevents growth under heterotrophic conditions [16]. Collectively, these studies indicate that the oxidative PPP is an important pathway for catabolizing glucose and for synthesizing NADPH.…”

Section: Introductionmentioning

confidence: 99%

Integrated transcriptomic and metabolomic analysis of the central metabolism of Synechocystis sp. PCC 6803 under different trophic conditions

Yoshikawa

Hirasawa

Ogawa

et al. 2013

Biotechnology Journal

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Cyanobacteria have received considerable attention as a sustainable energy resource because of their organic material production capacity using light energy and CO2 as a carbon source. Therefore, it is important to understand the cellular metabolism of cyanobacteria for metabolic engineering. In this study, to shed light on the central metabolism of cyanobacteria, we performed transcriptomic and metabolomic analyses of a glucose-tolerant strain of the cyanobacterium Synechocystis sp. PCC 6803, which was cultured under auto- and mixotrophic conditions. Our results indicate that the oxidative pentose phosphate pathway and glycolysis are activated under mixotrophic conditions rather than autotrophic conditions. Moreover, we examined the effect of atrazine, a photosynthesis inhibitor, on the metabolism of PCC 6803 under mixotrophic conditions, which was defined as photoheterotrophic conditions, by transcriptomics and metabolomics. We demonstrated that the activity of the glycolytic pathway decreased due to the indirect effect of atrazine. In addition, the difference in transcriptional and metabolic changes between auto- and photoheterotrophic conditions could also be captured. The omics dataset reported herein provides clues for understanding the metabolism of cyanobacteria.

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“…These three pathways are conserved and complete in all cyanobacteria including T. elongatus and are generally crucial for mixotrophic or heterotrophic competence. Blocks either in glycogen synthesis , in OPP pathway or in glycolysis resulted in a reversed incapability (sensitivity) of organic carbon assimilation. The OPP pathway, the glycolysis and the TCA cycle are directly involved in both exogenous (e.g.…”

Section: Discussionmentioning

confidence: 99%

Unexpected capacity for organic carbon assimilation by Thermosynechococcus elongatus, a crucial photosynthetic model organism

Zilliges

Dau

2016

FEBS Letters

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Genetic modification of key residues of photosystems is essential to identify functionally crucial processes by spectroscopic and crystallographic investigation; the required protein stability favours use of thermophilic species. The currently unique thermophilic photosynthetic model organism is the cyanobacterial genus Thermosynechococcus. We report the ability of Thermosynechococcus elongatus to assimilate organic carbon, specifically D-fructose. Growth in the presence of a photosynthesis inhibitor opens the door towards crucial amino acid substitutions in photosystems by the rescue of otherwise lethal mutations. Yet depression of batch-culture growth after 7 days implies that additional developments are needed.Keywords: carbon metabolism; cyanobacteria; mixotrophy and photoheterotrophy; photosystem II Two of the crucial protein complexes for life on earth are the photosystems (PS) of oxygenic photosynthesis, PSI and PSII (for review see [1]). Specifically the light-driven water splitting (water oxidation) by PSII is a hot spot of topical research, inter alia because PSII serves as a 'role model' for water oxidation in synthetic system for sustainable production of nonfossil fuels [2,3]. Thermophilic cyanobacteria play a key role in the endeavour to obtain a thorough mechanistic understanding of photosynthetic water oxidation. Their superior stability of the protein complexes has facilitated crystallisation and structure elucidation [4], first of PSI [5] and then of intact PSII [6][7][8]. Notably, crystallisation of intact PSII containing the active site of water oxidation, a proteinbound manganese-calcium-oxo cluster, has been achieved only for two closely related thermophilic cyanobacteria, specifically Thermosynechococcus elongatus and Thermosynechococcus vulcanus. Moreover, the superior thermostability of purified PSII from thermophilic cyanobacteria is highly favourable for spectroscopic investigations. However, there has been a serious drawback regarding the use of thermophilic cyanobacteria in photosynthesis research: These organisms are mostly believed to be incapable of growing in the absence of a functional PSII, rendering genetic modification of key amino acid residues impossible. The unexpected ability of T. elongatus to use external carbon sources for growing photoheterotrophically, without light-driven water oxidation by PSII, is the subject of our study.For many decades, most cyanobacteria including all thermophilic species such as T. elongatus have been considered as obligate photolithoautotrophic prokaryotes using light, H 2 O and solely CO 2 as energy, electron and carbon source respectively [9]. Just for a few mesophilic species, for example, Synechocystis sp. PCC 6803, the capacity for metabolisation of organic carbon sources, namely D-glucose, has been well known for a long time [10]. This ability of Synechocystis Abbreviations DCMU, 3-(3,4-dichlorophenyl)-1,1-dimethylurea; LAHG, light-activated heterotrophic growth; NDH-1 complex, bacterial-type I NAD(P)H-quinone oxidoreductase; OD 750 , ...

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Characterization of trophic changes and a functional oxidative pentose phosphate pathway in Synechocystis sp. PCC 6803

Cited by 14 publications

References 24 publications

The Entner–Doudoroff pathway is an overlooked glycolytic route in cyanobacteria and plants

The Entner–Doudoroff pathway is an overlooked glycolytic route in cyanobacteria and plants

Integrated transcriptomic and metabolomic analysis of the central metabolism of Synechocystis sp. PCC 6803 under different trophic conditions

Unexpected capacity for organic carbon assimilation by Thermosynechococcus elongatus, a crucial photosynthetic model organism

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