Evolutionary Origins of the Eukaryotic Shikimate Pathway: Gene Fusions, Horizontal Gene Transfer, and Endosymbiotic Replacements

Abstract

Currently the shikimate pathway is reported as a metabolic feature of prokaryotes, ascomycete fungi, apicomplexans, and plants. The plant shikimate pathway enzymes have similarities to prokaryote homologues and are largely active in chloroplasts, suggesting ancestry from the plastid progenitor genome. Toxoplasma gondii, which also possesses an alga-derived plastid organelle, encodes a shikimate pathway with similarities to ascomycete genes, including a five-enzyme pentafunctional arom. These data suggests that the shikimate pathway and the pentafunctional arom either had an ancient origin in the eukaryotes or was conveyed by eukaryote-to-eukaryote horizontal gene transfer (HGT). We expand sampling and analyses of the shikimate pathway genes to include the oomycetes, ciliates, diatoms, basidiomycetes, zygomycetes, and the green and red algae. Sequencing of cDNA from Tetrahymena thermophila confirmed the presence of a pentafused arom, as in fungi and T. gondii. Phylogenies and taxon distribution suggest that the arom gene fusion event may be an ancient eukaryotic innovation. Conversely, the Plantae lineage (represented here by both Viridaeplantae and the red algae) acquired different prokaryotic genes for all seven steps of the shikimate pathway. Two of the phylogenies suggest a derivation of the Plantae genes from the cyanobacterial plastid progenitor genome, but if the full Plantae pathway was originally of cyanobacterial origin, then the five other shikimate pathway genes were obtained from a minimum of two other eubacterial genomes. Thus, the phylogenies demonstrate both separate HGTs and shared derived HGTs within the Plantae clade either by primary HGT transfer or secondarily via the plastid progenitor genome. The shared derived characters support the holophyly of the Plantae lineage and a single ancestral primary plastid endosymbiosis. Our analyses also pinpoints a minimum of 50 gene/domain loss events, demonstrating that loss and replacement events have been an important process in eukaryote genome evolution.

Enzymes of the shikimic acid pathway encoded in the genome of a basal metazoan, Nematostella vectensis , have microbial origins

“…The anabolic shikimic acid pathway has seven steps [supporting information (SI) Scheme 1], which may be catalyzed by seven different polypeptides or by fewer multifunctional polypeptides (22). The enzymes for five of the biosynthetic steps are homologous in all organisms that possess the pathway.…”

Horizontal gene transfers and cell fusions in microbiology, immunology and oncology (Review)

“…The shikimic acid pathway in the sea anemone Nematostella vectensis is encoded by genes acquired through HGT from bacterial and eukaryotic (dinoflagellate) donors (115,116). Tenacibaculum species (T. aiptasiae, T. adriaticum) infect anemones and bryozoans (117,118) and tenacibaculum-like gene orthologs, including 16S rRNA of Flavobacteriaceae origin, are present in the anemones' genomes (116).…”

“…The biosynthesis of certain aromatic compounds follows the shikimic acid (shikimate) pathway (115,116). The shikimic acid pathway in the sea anemone Nematostella vectensis is encoded by genes acquired through HGT from bacterial and eukaryotic (dinoflagellate) donors (115,116).…”

Lateral genetic transfer: open issues

“…In Drosophila, 2 per cent of the transferred Wolbachia genes are expressed (Dunning Hotopp et al 2007). Plant-associated nematodes appear to have acquired cellulases and pectinases from plant-associated bacteria (Mitreva et al 2005), while genes of probable prokaryotic origin are responsible for cellulose synthesis (Nakashima et al 2004), starch degradation (Da Lage et al 2007), shikimate biosynthesis (Richards et al 2006) and detoxification (Burroughs et al 2006) in various animals. Gene flow in the opposite direction appears to be less common, although possible examples have been put forward (Ponting et al 1999;Jenkins et al 2002;Chen et al 2007).…”