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Title: Eukaryotic Acquisition of a Bacterial Operon

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.

Authors:
 [1];  [2];  [1];  [3];  [4];  [5];  [6];  [7];  [8];  [9];  [5];  [3];  [2]
  1. Univ. of Wisconsin, Madison, WI (United States). Lab. of Genetics, Genome Center of Wisconsin, Wisconsin Energy Inst., J.F. Crow Inst. for the Study of Evolution; Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center
  2. Univ. of Wisconsin, Madison, WI (United States). Lab. of Genetics, Genome Center of Wisconsin, Wisconsin Energy Inst., J.F. Crow Inst. for the Study of Evolution; Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center; Univ. of Wisconsin, Madison, WI (United States). Graduate Program in Cellular and Molecular Biology
  3. Vanderbilt Univ., Nashville, TN (United States). Dept. of Biological Sciences
  4. Vanderbilt Univ., Nashville, TN (United States). Dept. of Biological Sciences; South China Agricultural Univ., Guangzhou (China)
  5. US Dept. of Agriculture, Peoria, IL (United States). Mycotoxin Prevention and Applied Microbiology Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service
  6. Univ. of Wisconsin, Madison, WI (United States). Lab. of Genetics, Genome Center of Wisconsin, Wisconsin Energy Inst., J.F. Crow Inst. for the Study of Evolution
  7. Westerdijk Fungal Biodiversity Inst. CT, Utrecht (Netherlands)
  8. Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center
  9. Univ. of Wisconsin, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center, and Dept. of Biochemistry
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States).Great Lakes Bioenergy Research Center
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Contributing Org.:
Lucigen Corporation (Middleton, WI); University of Wisconsin Biotechnology Center DNA Sequencing Facility; Center for High-Throughput Computing at the University of Wisconsin-Madison
OSTI Identifier:
1547009
Grant/Contract Number:  
SC0018409
Resource Type:
Accepted Manuscript
Journal Name:
Cell
Additional Journal Information:
Journal Volume: 176; Journal Issue: 6; Journal ID: ISSN 0092-8674
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; central dogma of biology; horizontal gene transfer; operon; siderophore; biosynthesis; budding yeasts; Wickerhamiella; Starmerella; Saccharomycotina; enterobactin

Citation Formats

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, and Hittinger, Chris Todd. Eukaryotic Acquisition of a Bacterial Operon. United States: N. p., 2019. Web. doi:10.1016/j.cell.2019.01.034.
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. Eukaryotic Acquisition of a Bacterial Operon. United States. doi:10.1016/j.cell.2019.01.034.
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, and Hittinger, Chris Todd. Thu . "Eukaryotic Acquisition of a Bacterial Operon". United States. doi:10.1016/j.cell.2019.01.034.
@article{osti_1547009,
title = {Eukaryotic Acquisition of a Bacterial Operon},
author = {Kominek, Jacek and Doering, Drew T. and Opulente, Dana A. and Shen, Xing-Xing and Zhou, Xiaofan and DeVirgilio, Jeremy and Hulfachor, Amanda B. and Groenewald, Marizeth and Mcgee, Mcsean A. and Karlen, Steven D. and Kurtzman, Cletus P. and Rokas, Antonis and Hittinger, Chris Todd},
abstractNote = {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.},
doi = {10.1016/j.cell.2019.01.034},
journal = {Cell},
number = 6,
volume = 176,
place = {United States},
year = {2019},
month = {2}
}

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This content will become publicly available on February 21, 2020
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