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Eukaryotic Acquisition of a Bacterial Operon

Jacek Kominek, Drew T. Doering, Dana A. Opulente, Xing-Xing Shen, Xiaofan Zhou, Jeremy De Virgilio, Amanda B. Hulfachor, Cletus P. Kurtzman, Antonis Rokas, View ORCID ProfileChris Todd Hittinger
doi: https://doi.org/10.1101/399394
Jacek Kominek
1Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI 53706, USA
2DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, WI 53706, USA
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Drew T. Doering
1Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI 53706, USA
3Graduate Program in Cellular and Molecular Biology, University of Wisconsin-Madison, Madison, WI 53706, USA
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Dana A. Opulente
1Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI 53706, USA
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Xing-Xing Shen
4Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA
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Xiaofan Zhou
4Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA
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Jeremy De Virgilio
5Mycotoxin Prevention and Applied Microbiology Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, US Department of Agriculture, Peoria, IL 61604, USA
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Amanda B. Hulfachor
3Graduate Program in Cellular and Molecular Biology, University of Wisconsin-Madison, Madison, WI 53706, USA
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Cletus P. Kurtzman
5Mycotoxin Prevention and Applied Microbiology Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, US Department of Agriculture, Peoria, IL 61604, USA
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Antonis Rokas
4Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA
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Chris Todd Hittinger
1Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI 53706, USA
2DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, WI 53706, USA
3Graduate Program in Cellular and Molecular Biology, University of Wisconsin-Madison, Madison, WI 53706, USA
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  • ORCID record for Chris Todd Hittinger
  • For correspondence: cthittinger@wisc.edu
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Abstract

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.

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Posted August 24, 2018.
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Eukaryotic Acquisition of a Bacterial Operon
Jacek Kominek, Drew T. Doering, Dana A. Opulente, Xing-Xing Shen, Xiaofan Zhou, Jeremy De Virgilio, Amanda B. Hulfachor, Cletus P. Kurtzman, Antonis Rokas, Chris Todd Hittinger
bioRxiv 399394; doi: https://doi.org/10.1101/399394
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Eukaryotic Acquisition of a Bacterial Operon
Jacek Kominek, Drew T. Doering, Dana A. Opulente, Xing-Xing Shen, Xiaofan Zhou, Jeremy De Virgilio, Amanda B. Hulfachor, Cletus P. Kurtzman, Antonis Rokas, Chris Todd Hittinger
bioRxiv 399394; doi: https://doi.org/10.1101/399394

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