Evolution of enzymes involved in the photorespiratory 2-phosphoglycolate cycle from cyanobacteria via algae toward plants

Abstract

The photorespiratory pathway was shown to be essential for organisms performing oxygenic photosynthesis, cyanobacteria, algae, and plants, in the present day O(2)-containing atmosphere. The identification of a plant-like 2-phosphoglycolate cycle in cyanobacteria indicated that not only genes of oxygenic photosynthesis but also genes encoding photorespiratory enzymes were endosymbiotically conveyed from ancient cyanobacteria to eukaryotic oxygenic phototrophs. Here, we investigated the origin of the photorespiratory pathway in photosynthetic eukaryotes by phylogenetic analysis. We found that a mixture of photorespiratory enzymes of either cyanobacterial or α-proteobacterial origin is present in algae and higher plants. Three enzymes in eukaryotic phototrophs clustered closely with cyanobacterial homologs: glycolate oxidase, glycerate kinase, and hydroxypyruvate reductase. On the other hand, the mitochondrial enzymes of the photorespiratory cycle in algae and plants, glycine decarboxylase subunits and serine hydroxymethyltransferase, evolved from proteobacteria. Other than most genes for proteins of the photosynthetic machinery, nearly all enzymes involved in the 2-phosphogylcolate metabolism coexist in the genomes of cyanobacteria and heterotrophic bacteria.

Algal evolution in relation to atmospheric CO 2 : carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles

“…Since DNA damage and its repair must have occurred before oxygenic photosynthesis, the 2-phosphoglycolate phosphatase in oxygenic photosynthetic organisms could have been recruited from bacteria lacking autotrophic 2-phosphoglycolate synthesis. However, the 2-phosphoglycolate phosphatase from eukaryotes does not seem to have been derived from the 2-phospho-glycolate phosphatase of cyanobacteria [88].…”

“…Plantae), although some of the genes in eukaryotes came from a-proteobacteria rather than cyanobacteria [88]. The b-cyanobacterial plastid ancestor gave rise to the glycolate oxidase, glycerate kinase and hydroxypyruvate reductase of algae and embryophytes, while serine hydroxymethyl transferase and the L, P and T subunits of glycine decarboxylase came from a-proteobacteria by horizontal gene transfer [88]. The origin of the other eukaryotic PCOC genes, i.e.…”

“…The origin of the other eukaryotic PCOC genes, i.e. those encoding the H subunit of glycine decarboxylase, glutamate-glyoxylate aminotransferase and serine-glyoxylate aminotransferase, has not yet been established [88].…”

“…The other pathway from glycolate to 3-phosphoglycerate involves tartronic semialdehyde, and is called the tartronic semialdehyde pathway by phycologists; bacteriologists call it the glycerate pathway, even though glycerate is also an intermediate of the PCOC [85,[88][89][90]. Parts of the PCOC (glycerate dehydrogenase, serine transminases and serine hydroxymethyltransferase) could have been recruited from core metabolism synthesizing serine and glycine from glycolytic intermediates, while others (glycolate dehydrogenase/oxidase, glycine decarboxylase and glycerate kinase) have no known roles other than in the metabolism of glycolate to PCRC intermediates [93,94].…”

Metabolic and Transcriptomic Phenotyping of Inorganic Carbon Acclimation in the Cyanobacterium Synechococcus elongatus PCC 7942

“…Corresponding to the increased demand for photorespiratory 2PG detoxification, an increased transcript level of genes for putative 2PG phosphatases (orf0217 and orf2613) was detected. The majority of the other genes coding for enzymes in the plant-like photorespiratory 2PG cycle (Kern et al, 2011) remained unchanged. Only transcripts for two subunits of the Gly cleavage system were found to be increased, and those for the Ser hydroxymethyltransferase gene were decreased (Table I).…”