Occurrence of multiple, independent gene fusion events for the fifth and sixth enzymes of pyrimidine biosynthesis in different eukaryotic groups

The genes encoding orotate phosphoribosyltransferase (OPRT) and orotidine-5′-monophosphate decarboxylase (OMPDC), the fifth and sixth enzymes in the de novo pyrimidine biosynthetic pathway, are fused as OPRT–OMPDC in most eukaryotic groups. On the other hand, the inversely linked OMPDC–OPRT fusion is present in trypanosomatids, belonging to kinetoplastids together with bodonids in a supergroup, Euglenozoa. Here, we show the presence of OMPDC–OPRT in the bodonid, Bodo caudatus, while OPRT–OMPDC in Euglena gracilis, another euglenozoan species belonging to euglenoids. These results suggest that the OMPDC–OPRT fusion event occurred in a common ancestor of kinetoplastids. Genome sequence database searches further revealed the presence of OMPDC–OPRT in stramenopiles and cyanobacteria. Phylogenetic reconstruction of OPRT and OMPDC rejected statistically the monophyly of the OPRT domains of stramenopile and kinetoplastid OMPDC–OPRT, demonstrating that these gene fusions do not share a common evolutionary origin, despite the identical gene order. Thus, the OMPDC–OPRT fusion is likely to have emerged independently in these eukaryotic groups. Phylogenetic analyses also suggested that cyanobacterial OMPDC–OPRT arose via lateral transfer. We conclude that gene fusion events occur more frequently than previously thought and that lateral gene transfer has made a marked contribution to establishment of the rearranged structure of OPRT and OMPDC genes in eukaryotes.