Eukaryotic Acquisition of a Bacterial Operon

Operons are a hallmark of bacterial genomes, where they allow concerted expression of multiple functionally related genes as single polycistronic transcripts. They are rare in eukaryotes, where each gene usually drives expression of its own independent messenger RNAs. Here we report the horizontal operon transfer of a catecholate-class siderophore biosynthesis pathway from Enterobacteriaceae into a group of closely related yeast taxa. We further show that the co-linearly arranged secondary metabolism genes are actively expressed, exhibit mainly eukaryotic transcriptional features, and enable the sequestration and uptake of iron. After transfer to the eukaryotic host, several genetic changes occurred, including the acquisition of polyadenylation sites, structural rearrangements, integration of eukaryotic genes, and secondary loss in some lineages. We conclude that the operon genes were likely captured in the shared insect gut habitat, modified for eukaryotic gene expression, and maintained by selection to adapt to the highly-competitive, iron-limited environment.