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ARS Home » Midwest Area » Peoria, Illinois » National Center for Agricultural Utilization Research » Mycotoxin Prevention and Applied Microbiology Research » Research » Publications at this Location » Publication #344720
Title: Eukaryotic acquisition of a bacterial operons

Author
item KOMINEK, JACEK - University Of Wisconsin
item DOERING, DREW - University Of Wisconsin
item OPULENTE, DANA - University Of Wisconsin
item SHEN, XING-XING - Vanderbilt University
item ZHOU, XIAOFAN - Vanderbilt University
item DEVIRGILIO, JEREMY - Former ARS Employee
item HULFACHOR, AMANDA - University Of Wisconsin
item Kurtzman, Cletus
item ROKAS, ANTONIS - Vanderbilt University
item HITTINGER, CHRIS - University Of Wisconsin

Submitted to: Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/7/2019
Publication Date: 3/7/2019
Citation: Kominek, J., Doering, D.T., Opulente, D.A., Shen, X.-X., Zhou, X., DeVirgilio, J., Hulfachor, A.B., Kurtzman, C.P., Rokas, A., Hittinger, C.T., et al. 2019. Eukaryotic acquisition of a bacterial operon. Cell. 176(6):1356-1366. https://doi.org/10.1016/j.cell.2019.01.034.
DOI: https://doi.org/10.1016/j.cell.2019.01.034

Interpretive Summary: We are examining the genome sequences from nearly all ascomycete yeasts with the goal of discovering novel metabolic pathways and for development of a system of classification based on natural relationships that will allow prediction of species with novel properties. We discovered that a cluster of bacterial genetic material (operon) encoding the genes for biosynthesis of compounds that bind iron were transferred from a bacterium related to E. coli into a group of budding yeasts. This is the first known example of a higher organism (eukaryote) acquiring an entire operon from a bacterium by normal horizontal gene transfer. Because the yeasts that acquired this new genetic material are biotechnologically important for synthesis of biochemicals, this new knowledge is expected to help with strain improvement for more efficient production of novel biochemical compounds.

Technical Abstract: Operons are a hallmark of bacterial genomes, where they allow concerted expression of multiple functionally related genes as polycistronic transcripts under a single promoter. They are rare in eukaryotes, where transcription generally occurs from genes as 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 both bacterial and eukaryotic transcriptional features, and enable the sequestration and uptake of iron. After transfer to the eukaryotic host, several genetic changes occurred, including structural rearrangements, integration of additional eukaryotic genes, and secondary loss of the horizontally acquired genes 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.