The Malic Enzyme Is Required for Optimal Photoautotrophic Growth of
            <i>Synechocystis</i>
            sp. Strain PCC 6803 under Continuous Light but Not under a Diurnal Light Regimen

Bricker, Terry M.; Zhang, Shulu; Laborde, Susan M.; Mayer, Paul R.; Frankel, Laurie K.; Moroney, James V.

doi:10.1128/jb.186.23.8144-8148.2004

Cited by 33 publications

(48 citation statements)

References 20 publications

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“…On the other hand, DCMU can alleviate pyruvate kinase inhibition by blocking LEF-based ATP synthesis, rendering malic en-zyme less important for pyruvate synthesis. The adverse effect of eliminating malic enzyme (⌬slr0721) on the growth of DCMUtreated Synechocystis PCC 6803 was shown to be much less significant than that in photoautotrophic or photomixotrophic cultures (37).…”

Section: Discussionmentioning

confidence: 99%

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Photoheterotrophic Fluxome in Synechocystis sp. Strain PCC 6803 and Its Implications for Cyanobacterial Bioenergetics

You

Tang

2015

J Bacteriol

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This study investigated metabolic responses in Synechocystis sp. strain PCC 6803 to photosynthetic impairment. We used 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU; a photosystem II inhibitor) to block O 2 evolution and ATP/NADPH generation by linear electron flow. Based on 13 C-metabolic flux analysis ( 13 C-MFA) and RNA sequencing, we have found that Synechocystis sp. PCC 6803 employs a unique photoheterotrophic metabolism. First, glucose catabolism forms a cyclic route that includes the oxidative pentose phosphate (OPP) pathway and the glucose-6-phosphate isomerase (PGI) reaction. Glucose-6-phosphate is extensively degraded by the OPP pathway for NADPH production and is replenished by the reversed PGI reaction. Second, the Calvin cycle is not fully functional, but RubisCO continues to fix CO 2 and synthesize 3-phosphoglycerate. Third, the relative flux through the complete tricarboxylic acid (TCA) cycle and succinate dehydrogenase is small under heterotrophic conditions, indicating that the newly discovered cyanobacterial TCA cycle (via the ␥-aminobutyric acid pathway or ␣-ketoglutarate decarboxylase/succinic semialdehyde dehydrogenase) plays a minimal role in energy metabolism. Fourth, NAD(P)H oxidation and the cyclic electron flow (CEF) around photosystem I are the two main ATP sources, and the CEF accounts for at least 40% of total ATP generation from photoheterotrophic metabolism (without considering maintenance loss). This study not only demonstrates a new topology for carbohydrate oxidation but also provides quantitative insights into metabolic bioenergetics in cyanobacteria. C yanobacteria, which first appeared in shallow marine settings as early as 3 billion years ago (1, 2), are now widely distributed in diverse nutrient and light environments (3-5). They can perform oxygenic photosynthesis and respiration simultaneously in the same compartment (6, 7). Cyanobacteria contain two photosystems to harvest light energy. Photosystem II (PSII) splits water and transports electrons sequentially through plastoquinone (PQ), cytochrome b 6 f, plastocyanin, and photosystem I (PSI), forming a linear electron flow (LEF) to produce ATP and NADPH. Alternatively, a cyclic electron flow (CEF) runs around PSI to generate ATP (8, 9). The cyanobacterial CEF involves respiratory electron transport reactions and PSI enzymes. NAD(P)H dehydrogenase complex (NDH-1) oxidizes NADPH and provides electrons for the PQ pool. Then the electrons from PQ flow to PSI and ferredoxin to regenerate NADPH via ferredoxin-NADP ϩ reductase (FNR). The CEF can regulate ATP and NADPH ratios for CO 2 fixation and respiration in plants (10). Cyanobacteria have a much larger PSI content than plants. For example, the PSI/PSII ratio in Synechocystis sp. strain PCC 6803 is about 5, suggesting the significant role of PSI in energy metabolism (6). To decipher photosynthesis mechanisms, researchers often use the herbicide 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) to block the PQ binding site of PSII so that the LEF is inactivated. Under DCMU treatm...

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Section: Discussionmentioning

confidence: 99%

“…Second, malic enzyme is the main route for supplying pyruvate in Synechocystis PCC 6803 under continuous light illumination, because pyruvate kinase is inhibited by ATP from photosynthesis (37). The malic enzyme activity has been revealed under photoautotrophic and photomixotrophic conditions (11)(12)(13) and with DCMU treatment.…”

Section: Discussionmentioning

confidence: 99%

Photoheterotrophic Fluxome in Synechocystis sp. Strain PCC 6803 and Its Implications for Cyanobacterial Bioenergetics

You

Tang

2015

J Bacteriol

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“…The reaction catalyzed by Ppc contributes to about 25% of the assimilated CO 2 under mixotrophic condition [72,73], indicating that Ppc is important for the fixation of CO 2 in cyanobacterial cells [79], where cyanobacterial cells fix significant amounts of carbon as C4 acids under light conditions. Considering that Mez in cyanobacteria is NADP-linked [80], it is more likely that Ppc and Mez serve as a device to fix a large amount of CO 2 as C4 acids and then release CO 2 and produce NADPH by the decarboxylation of malate. This Ppc and Mez pathways can effectively bypass the Pyk reaction, where its activity is repressed under light condition [77].…”

Section: Metabolism Of Cyanobacteriamentioning

confidence: 99%

An overview on biofuel and biochemical production by photosynthetic microorganisms with understanding of the metabolism and by metabolic engineering together with efficient cultivation and downstream processing

Sarkar

Shimizu

2015

Bioresour. Bioprocess.

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Biofuel and biochemical production by photosynthetic microorganisms such as cyanobacteria and algae is attractive to improve energy security and to reduce CO 2 emission, contributing to the environmental problems such as global warming. Although biofuel production by photosynthetic microorganisms is called as the third generation biofuels, and significant innovation is necessary for the feasibility in practice, these fuels are attractive due to renewable and potentially carbon neutral resources. Moreover, photosynthetic microorganisms are attractive since they can grow on non-arable land and utilize saline and wastewater streams. Highly versatile and genetically tractable photosynthetic microorganisms need to capture solar energy and convert atmospheric and waste CO 2 to high-energy chemical products. Understanding of the metabolism and the efficient metabolic engineering of the photosynthetic organisms together with cultivation and separation processes as well as increased CO 2 assimilation enables the enhancement of the feasibility of biofuel and biochemical production.

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“…Earlier, we have used this technique to identify previously undescribed components of the cyanobacterial carbon-concentrating mechanism (19) and have also elucidated a differential role for the malic enzyme in carbon metabolism under continuous versus diurnal illumination (20). In the current study, a cyanobac-terial mutant (designated Tsll0606) bearing a transposon insertion in the sll0606 gene was isolated.…”

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confidence: 99%

The Sll0606 Protein Is Required for Photosystem II Assembly/Stability in the Cyanobacterium Synechocystis sp. PCC 6803

Zhang

Frankel

Bricker

2010

Journal of Biological Chemistry

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An insertional transposon mutation in the sll0606 gene was found to lead to a loss of photoautotrophy but not photoheterotrophy in the cyanobacterium Synechocystis sp. PCC 6803. Complementation analysis of this mutant (Tsll0606) indicated that an intact sll0606 gene could fully restore photoautotrophic growth. Gene organization in the vicinity of sll0606 indicates that it is not contained in an operon. No electron transport activity was detected in Tsll0606 using water as an electron donor and 2,6-dichlorobenzoquinone as an electron acceptor, indicating that Photosystem II (PS II) was defective. Electron transport activity using dichlorophenol indolephenol plus ascorbate as an electron donor to methyl viologen, however, was the same as observed in the control strain. This indicated that electron flow through Photosystem I was normal. Fluorescence induction and decay parameters verified that Photosystem II was highly compromised. The quantum yield for energy trapping by Photosystem II (F V /F M ) in the mutant was less than 10% of that observed in the control strain. The small variable fluorescence yield observed after a single saturating flash exhibited aberrant Q A ؊ reoxidation kinetics that were insensitive to dichloromethylurea. Immunological analysis indicated that whereas the D2 and CP47 proteins were modestly affected, the D1 and CP43 components were dramatically reduced. Analysis of twodimensional blue native/lithium dodecyl sulfate-polyacrylamide gels indicated that no intact PS II monomer or dimers were observed in the mutant. The CP43-less PS II monomer did accumulate to detectable levels. Our results indicate that the Sll0606 protein is required for the assembly/stability of a functionally competent Photosystem II.In higher plants, algae, and cyanobacteria, at least six intrinsic proteins appear to be required for oxygen evolution by PS II 2 (1-3). These are CP47, CP43, the D1 and D2 proteins, and the ␣ and ␤ subunits of cytochrome b 559 . Insertional inactivation or deletion of the genes for these components results in the absence of PS II complex assembly and the complete loss of oxygen evolution activity (for a review, see Ref. 4). For maximal rates of oxygen evolution in cyanobacteria, the extrinsic proteins PsbO, PsbU, PsbV, and PsbQ must also be present (5). Additionally, a large number of other intrinsic membrane components are present in PS II complexes (6 -8), although the functions of many of these proteins remain obscure. The most recent crystal structure of the thermophilic cyanobacterium Thermosynechococcus elongatus (9) indicates that PS II contains 20 protein components (it should be noted that PsbQ, which is essential for maximum PS II activity in cyanobacteria (10), is missing from the current crystal structure).PS II assembly and turnover requires a variety of other protein components (for a comprehensive review, see Ref. 11). Although many of these proteins are conserved in all oxygenic organisms, a subset is present only in the cyanobacteria. These include the Synechocystis sp. PC...

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The Malic Enzyme Is Required for Optimal Photoautotrophic Growth of Synechocystis sp. Strain PCC 6803 under Continuous Light but Not under a Diurnal Light Regimen

Cited by 33 publications

References 20 publications

Photoheterotrophic Fluxome in Synechocystis sp. Strain PCC 6803 and Its Implications for Cyanobacterial Bioenergetics

Photoheterotrophic Fluxome in Synechocystis sp. Strain PCC 6803 and Its Implications for Cyanobacterial Bioenergetics

An overview on biofuel and biochemical production by photosynthetic microorganisms with understanding of the metabolism and by metabolic engineering together with efficient cultivation and downstream processing

The Sll0606 Protein Is Required for Photosystem II Assembly/Stability in the Cyanobacterium Synechocystis sp. PCC 6803

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