Horizontal Transfer of Bacterial Operons into Eukaryote Genomes

Abstract In prokaryotes, functionally linked genes are typically clustered into operons, which are transcribed into a single mRNA, providing for the coregulation of the production of the respective proteins, whereas eukaryotes generally lack operons. We explored the possibility that some prokaryotic operons persist in eukaryotic genomes after horizontal gene transfer (HGT) from bacteria. Extensive comparative analysis of prokaryote and eukaryote genomes revealed 33 gene pairs originating from bacterial operons, mostly encoding enzymes of the same metabolic pathways, and represented in distinct clades of fungi or amoebozoa. This amount of HGT is about an order of magnitude less than that observed for the respective individual genes. These operon fragments appear to be relatively recent acquisitions as indicated by their narrow phylogenetic spread and low intron density. In 20 of the 33 horizontally acquired operonic gene pairs, the genes are fused in the respective group of eukaryotes so that the encoded proteins become domains of a multifunctional protein ensuring coregulation and correct stoichiometry. We hypothesize that bacterial operons acquired via HGT initially persist in eukaryotic genomes under a neutral evolution regime and subsequently are either disrupted by genome rearrangement or undergo gene fusion which is then maintained by selection.