Glyceraldehyde-3-phosphate dehydrogenase gene diversity in eubacteria and eukaryotes: evidence for intra- and inter-kingdom gene transfer

Abstract

Cyanobacteria contain up to three highly divergent glyceraldehyde-3-phosphate dehydrogenase (GAPDH) genes: gap1, gap2, and gap3. Genes gap1 and gap2 are closely related at the sequence level to the nuclear genes encoding cytosolic and chloroplast GAPDH of higher plants and have recently been shown to play distinct key roles in catabolic and anabolic carbon flow, respectively, of the unicellular cyanobacterium Synechocystis sp. PCC6803. In the present study, sequences of 10 GAPDH genes distributed across the cyanobacteria Prochloron didemni, Gloeobacter violaceus PCC7421, and Synechococcus PCC7942 and the alpha-proteobacterium Paracoccus denitrificans and the beta-proteobacterium Ralstonia solanacearum were determined. Prochloron didemni possesses homologs to the gap2 and gap3 genes from Anabaena, Gloeobacter harbors gap1 and gap2 homologs, and Synechococcus possesses gap1, gap2, and gap3. Paracoccus harbors two highly divergent gap genes that are related to gap3, and Ralstonia possesses a homolog of the gap1 gene. Phylogenetic analyses of these sequences in the context of other eubacterial and eukaryotic GAPDH genes reveal that divergence across eubacterial gap1, and gap2, and gap3 genes is greater than that between eubacterial gap1 and eukaroytic glycolytic GapC or between eubacterial gap2 and eukaryotic Calvin cycle GapAB. These data strongly support previous analyses which suggested that eukaryotes acquired their nuclear genes for GapC and GapAB via endosymbiotic gene transfer from the antecedents of mitochondria and chloroplasts, and extend the known range of sequence diversity of the antecedent eubacterial genes. Analyses of available GAPDH sequences from other eubacterial sources indicate that the glycosomal gap gene from trypanosomes (cytosolic in Euglena) and the gap gene from the spirochete Treponema pallidum are each other's closest relatives. This specific relationship can therefore not reflect organismal evolution but must be the result of an interkingdom gene transfer, the direction of which cannot be determined with certainty at present. Contrary to this, the origin of the cytosolic Gap gene from trypanosomes can now be clearly defined as gamma-proteobacterial, since the newly established Ralstonia sequence (beta-proteobacteria) branches basally to the gamma-proteobacterial/trypanosomal assemblage.

Plant-like traits associated with metabolism of Trypanosoma parasites

“…Trypanosomatid GAPDH and its counterpart from Euglena gracilis are close relatives of the GAPDH isoenzyme 1 from cyanobacteria, but are clearly distinct from the plastid GAPDH of plants, which has been derived from the cyanobacterial isoenzyme 3 (28,29). The three closely related trypanosomatid PGK isoenzymes (30) are clearly distinct from their eukaryotic homologs, including those of protists such as the ciliates Tetrahymena and Euplotes and the apicomplexan Plasmodium, in that they lack a typical eukaryotic 11-aa insertion (www.icp.ucl.ac.be/ϳopperd/Supplementary/table.html), and in a phylogenetic analysis they clustered robustly with the prokaryotic sequences, including the cyanobacterial ones.…”

The global phylogeny of glycolytic enzymes

“…Scattered findings of other individual bacterial taxa among eukaryotic clusters of enzymes have been offered as evidence for the descent of eukaryotic glycolytic enzymes from the bacterial lineage that gave rise to the mitochondria (3,17,18,21,22). In effect, these authors have interpreted the anomalous placement of a nominal bacterial homologue within a eukaryotic cluster as evidence that the bacterium is at the root of that eukaryotic lineage.…”

Ribulose bisphosphate carboxylase activity and a Calvin cycle gene cluster in Sulfobacillus species

“…Using a yeast enzyme sequence outgroup, there was poor bootstrap support for the branching order close to the S. acidophilus sequence, which was among those from a varied collection of mostly Gram-positive bacteria, and separate from most sequences previously described as cbbT-encoded (data not shown). In relation to three groups of divergent, class I glyceraldehyde-3-phosphate dehydrogenases (GAP) (Figge et al, 1999), the S. acidophilus cbbG gene product sequence was placed with those of the GAP II subgroup (Fig. 3g).…”