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Cell. 2019 Mar 7;176(6):1356-1366.e10. doi: 10.1016/j.cell.2019.01.034. Epub 2019 Feb 21.

Eukaryotic Acquisition of a Bacterial Operon.

Author information

1
Laboratory 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; DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI 53706, USA.
2
Laboratory 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; DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI 53706, USA; Graduate Program in Cellular and Molecular Biology, University of Wisconsin-Madison, Madison, WI 53706, USA.
3
Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA.
4
Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA; Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural University, 510642 Guangzhou, China.
5
Mycotoxin Prevention and Applied Microbiology Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, US Department of Agriculture, Peoria, IL 61604, USA.
6
Laboratory 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.
7
Westerdijk Fungal Biodiversity Institute, 3584 CT, Utrecht, Netherlands.
8
DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI 53706, USA.
9
DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI 53706, USA; Department of Biochemistry, University of Wisconsin-Madison, Madison, WI 53706, USA.
10
Laboratory 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; DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI 53706, USA; Graduate Program in Cellular and Molecular Biology, University of Wisconsin-Madison, Madison, WI 53706, USA. Electronic address: cthittinger@wisc.edu.

Abstract

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.

KEYWORDS:

Saccharomycotina; Starmerella; Wickerhamiella; budding yeasts; central dogma of biology; enterobactin; horizontal gene transfer; operon; siderophore biosynthesis

PMID:
30799038
DOI:
10.1016/j.cell.2019.01.034

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