Eukaryotic origin of glyceraldehyde-3-phosphate dehydrogenase genes in Clostridium thermocellum and Clostridium cellulolyticum genomes and putative fates of the exogenous gene in the subsequent genome evolution

Although lateral gene transfer (LGT) events have been frequently documented in the evolution of glyceraldehyde-3-phosphate dehydrogenase (GAPDH), no eukaryote-to-prokaryote transfer has been reported so far. Here we describe the first case of the GAPDH gene transfer from a eukaryote to a subset of Clostridium species (Bacteria, Firmicutes). A series of phylogenetic analyses of GAPDH homologues revealed that Clostridium thermocellum and Clostridium cellulolyticum homologues have the evolutionary affinity to the eukaryotic homologues, rather than to those of bacterial species closely related to the two Clostridium species in the organismal phylogeny. These results suggest that the GAPDH genes in the two Clostridium species are of eukaryotic origin, which is the first reported case of eukaryote-to-bacterium GAPDH gene transfer. Since a previously published 16S ribosomal DNA phylogeny and our GAPDH phylogeny commonly suggest an intimate evolutionary relationship between C. thermocellum and C. cellulolyticum, a common ancestor of the two species likely acquired the eukaryotic GAPDH gene. In the C. cellulolyticum genome, the exogenous GAPDH gene was physically separated from other glycolytic genes, suggesting that this gene organization was likely achieved by a random insertion of the laterally transferred gene. On the other hand, in the C. thermocellum genome, the laterally transferred GAPDH gene clusters with other bacterial glycolytic genes. We discuss possible scenarios for the evolutionarily chimeric glycolytic gene cluster in the C. thermocellum genome.