Photorespiratory 2-phosphoglycolate (2PG) metabolism is essential for photosynthesis in higher plants but thought to be superfluous in cyanobacteria because of their ability to concentrate CO 2 internally and thereby inhibit photorespiration. Here, we show that 3 routes for 2PG metabolism are present in the model cyanobacterium Synechocystis sp. strain PCC 6803. In addition to the photorespiratory C2 cycle characterized in plants, this cyanobacterium also possesses the bacterial glycerate pathway and is able to completely decarboxylate glyoxylate via oxalate. A triple mutant with defects in all 3 routes of 2PG metabolism exhibited a high-CO 2-requiring (HCR) phenotype. All these catabolic routes start with glyoxylate, which can be synthesized by 2 different forms of glycolate dehydrogenase (GlcD). Mutants defective in one or both GlcD proteins accumulated glycolate under high CO 2 level and the double mutant ⌬glcD1/⌬glcD2 was unable to grow under low CO2. The HCR phenotype of both the double and the triple mutant could not be attributed to a significantly reduced affinity to CO2, such as in other cyanobacterial HCR mutants defective in the CO2-concentrating mechanism (CCM). These unexpected findings of an HCR phenotype in the presence of an active CCM indicate that 2PG metabolism is essential for the viability of all organisms that perform oxygenic photosynthesis, including cyanobacteria and C3 plants, at ambient CO 2 conditions. These data and phylogenetic analyses suggest cyanobacteria as the evolutionary origin not only of oxygenic photosynthesis but also of an ancient photorespiratory 2PG metabolism. I t is well established that the photorespiratory C2 pathway, whereby 2-phosphoglycolate (2PG) is metabolized (1), is essential for photosynthesis in the majority of plants (2). In contrast, the functioning of the C2 pathway and its importance are still under discussion for cyanobacteria. These organisms were the first to have evolved oxygenic photosynthesis, and endosymbiotic engulfment of an ancient cyanobacterium led to the evolution of plant chloroplasts (3). In cyanobacteria, as in C3 plants, the primary carbon fixation is catalyzed by ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco). Ribulose 1,5-bisphosphate reacts with either CO 2 , leading to the formation of 2 molecules of 3-phosphoglycerate (3PGA), or O 2 , generating 3PGA and 2PG. The latter compound is toxic to plant metabolism because it inhibits distinct steps in the carbon-fixing Calvin-Benson cycle (4, 5). Therefore, plants employ the socalled photorespiratory glycolate pathway (or C2 cycle), which degrades 2PG and converts 2 molecules of 2PG into 1 molecule each of 3PGA, CO 2 , and NH 4 ϩ (1, 6, 7). In a typical C3 plant, the ammonium is refixed at the expense of ATP, and 25% of the carbon entering the path is released as CO 2 . Generally, the photorespiratory cycle is indispensable for C3 plants, because mutations in single steps of the C2 cycle resulted in high-CO 2 -requiring (HCR) phenotypes (2,(8)(9)(10).In contrast to plants, ear...

BackgroundFlavodiiron proteins (FDPs) comprise a group of modular enzymes that function in oxygen and nitric oxide detoxification in Bacteria and Archaea. The FDPs in cyanobacteria have an extra domain as compared to major prokaryotic enzymes. The physiological role of cyanobacteria FDPs is mostly unknown. Of the four putative flavodiiron proteins (Flv1–4) in the cyanobacterium Synechocystis sp. PCC 6803, a physiological function in Mehler reaction has been suggested for Flv1 and Flv3.Principal FindingsWe demonstrate a novel and crucial function for Flv2 and Flv4 in photoprotection of photosystem II (PSII) in Synechocystis. It is shown that the expression of Flv2 and Flv4 is high under air level of CO2 and negligible at elevated CO2. Moreover, the rate of accumulation of flv2 and flv4 transcripts upon shift of cells from high to low CO2 is strongly dependent on light intensity. Characterization of FDP inactivation mutants of Synechocystis revealed a specific decline in PSII centers and impaired translation of the D1 protein in Δflv2 and Δflv4 when grown at air level CO2 whereas at high CO2 the Flvs were dispensable. Δflv2 and Δflv4 were also more susceptible to high light induced inhibition of PSII than WT or Δflv1 and Δflv3.SignificanceAnalysis of published sequences revealed the presence of cyanobacteria-like FDPs also in some oxygenic photosynthetic eukaryotes like green algae, mosses and lycophytes. Our data provide evidence that Flv2 and Flv4 have an important role in photoprotection of water-splitting PSII against oxidative stress when the cells are acclimated to air level CO2. It is conceivable that the function of FDPs has changed during evolution from protection against oxygen in anaerobic microbes to protection against reactive oxygen species thus making the sustainable function of oxygen evolving PSII possible. Higher plants lack FDPs and distinctly different mechanisms have evolved for photoprotection of PSII.

Cyanobacterial NDH-1 complexes belong to a family of energy converting NAD(P)H:Quinone oxidoreductases that includes bacterial type-I NADH dehydrogenase and mitochondrial Complex I. Several distinct NDH-1 complexes may coexist in cyanobacterial cells and thus be responsible for a variety of functions including respiration, cyclic electron flow around PSI and CO(2) uptake. The present review is focused on specific features that allow to regard the cyanobacterial NDH-1 complexes, together with NDH complexes from chloroplasts, as a separate sub-class of the Complex I family of enzymes. Here, we summarize our current knowledge about structure of functionally different NDH-1 complexes in cyanobacteria and consider implications for a functional mechanism. This article is part of a Special Issue entitled: Regulation of Electron Transport in Chloroplasts.

Concerted changes in the transcriptional pattern and physiological traits that result from long-term (here defined as up to 24 h) limitation of inorganic carbon (C i ) have been investigated for the cyanobacterium Synechocystis sp. strain PCC 6803. Results from reverse transcription-polymerase chain reaction and genome-wide DNA microarray analyses indicated stable up-regulation of genes for inducible CO 2 and HCO 3 2 uptake systems and of the rfb cluster that encodes enzymes involved in outer cell wall polysaccharide synthesis. Coordinated up-regulation of photosystem I genes was further found and supported by a higher photosystem I content and activity under low C i (LC) conditions. Bacterial-type glycerate pathway genes were induced by LC conditions, in contrast to the genes for the plant-like photorespiratory C2 cycle. Down-regulation was observed for nitrate assimilation genes and surprisingly also for almost all carboxysomal proteins. However, for the latter the observed elongation of the half-life time of the large subunit of Rubisco protein may render compensation. Mutants defective in glycolate turnover (DglcD and DgcvT) showed some transcriptional changes under high C i conditions that are characteristic for LC conditions in wild-type cells, like a modest down-regulation of carboxysomal genes. Properties under LC conditions were comparable to LC wild type, including the strong response of genes encoding inducible high-affinity C i uptake systems. Electron microscopy revealed a conspicuous increase in number of carboxysomes per cell in mutant DglcD already under high C i conditions. These data indicate that an increased level of photorespiratory intermediates may affect carboxysomal components but does not intervene with the expression of majority of LC inducible genes.