The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiontically to plants - PubMed (original) (raw)

The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiontically to plants

Marion Eisenhut et al. Proc Natl Acad Sci U S A. 2008.

Abstract

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 DeltaglcD1/DeltaglcD2 was unable to grow under low CO(2). The HCR phenotype of both the double and the triple mutant could not be attributed to a significantly reduced affinity to CO(2), such as in other cyanobacterial HCR mutants defective in the CO(2)-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.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Fig. 1.

A scheme displaying the 2PG metabolism in Synechocystis sp. strain PCC 6803, which employs 3 different routes: C2 cycle, glycerate pathway, and the decarboxylating branch. Enzymatic steps mutated in strains used for this study are indicated in bold.

Fig. 2.

Fig. 2.

Genotypic and phenotypic characterization of the triple mutant Δ_gcvT_/Δ_tsr_/Δ_odc_. (A) Complete segregation of the mutant Δ_gcvT_/Δ_tsr_/Δ_odc_ was verified by PCR with gene-specific primers (see

SI Table 1

). (B) Growth of WT, single mutant Δ_odc_ blocked in the decarboxylation branch, double mutant Δ_odc_/Δ_gcvT_ blocked in the decarboxylation branch and C2 cycle, and triple mutant Δ_gcvT_/Δ_tsr_/Δ_odc_ blocked in all 3 branches of 2PG metabolism (see Fig. 1), respectively, under HC or LC. Strains were plated on BG11, pH 7, solidified by 0.9% Kobe agar, and incubated under continuous illumination of 30 μmol of photons per s per m2 at 30 °C for 7 d. (C) Resistance of WT, single mutant Δ_odc_, double mutant Δ_odc_/Δ_gcvT_, and triple mutant Δ_gcvT_/Δ_tsr_/Δ_odc_ toward oxalate (Ox). Strains were plated on BG11 agar plates, pH 8, supplemented by different amounts of oxalate. Cells were incubated under continuous illumination of 30 μmol of photons per s per m2 at 30 °C and HC for 7 d. [C reproduced with permission from ref. 41].

Fig. 3.

Fig. 3.

Phenotypic characterization of single mutants and a double mutant of Synechocystis defective in GlcDs. (A) Quantification of intracellular glycolate in cells of single- (Δ_glcD1_, Δ_glcD2_) and double- (Δ_glcD1_/Δ_glcD2_) mutants in the glycolate converting step. Samples were taken 3 h after shift from HC to LC and glycolate was quantified by HPLC. *, WT cells contained only traces of glycolate under these conditions. (B) Growth of WT, single mutants Δ_glcD1_ or Δ_glcD2_, and double mutant Δ_glcD1_/Δ_glcD2_ under HC or LC. Strains were plated on BG11, pH 7, solidified by 0.9% Kobe agar, and incubated under continuous illumination of 30 μmol of photons per s per m2 at 30 °C for 7 d. (C) Photosynthesis rates of cells of the WT and the double mutant Δ_glcD1_/Δ_glcD2_ at different concentrations of HCO3− as a source for Ci. The cells were grown in liquid BG11 medium at HC or transferred to aeration by ambient air (LC) for 6 h.

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