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Eukaryotic Acquisition of a Bacterial Operon

Kominek, Jacek, Doering, Drew T., Opulente, Dana A., Shen, Xing-Xing, Zhou, Xiaofan, DeVirgilio, Jeremy, Hulfachor, Amanda B., Groenewald, Marizeth, Mcgee, Mcsean A., Karlen, Steven D., Kurtzman, Cletus P., Rokas, Antonis, Hittinger, Chris Todd
Cell 2019 v.176 no.6 pp. 1356-1366.e10
Escherichia coli, biosynthesis, eukaryotic cells, gene expression, iron, messenger RNA, operon, siderophores, transcription (genetics), yeasts
Operons are a hallmark of bacterial genomes, where they allow concerted expression of 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 siderophore biosynthesis pathway from relatives of Escherichia coli into a group of budding yeast taxa. We further show that the co-linearly arranged secondary metabolism genes are expressed, exhibit eukaryotic transcriptional features, and enable the sequestration and uptake of iron. After transfer, several genetic changes occurred during subsequent evolution, including the gain of new transcription start sites that were sometimes within protein-coding sequences, acquisition of polyadenylation sites, structural rearrangements, and integration of eukaryotic genes into the cluster. We conclude that the genes were likely acquired as a unit, modified for eukaryotic gene expression, and maintained by selection to adapt to the highly competitive, iron-limited environment.