Eukaryotic Acquisition of a Bacterial Operon.

Bacteria / genetics Escherichia coli / genetics Eukaryota / genetics Eukaryotic Cells Evolution, Molecular Gene Expression Regulation, Bacterial / genetics Gene Transfer, Horizontal / genetics Genes, Bacterial / genetics Genome, Bacterial / genetics Genome, Fungal / genetics Operon / genetics Saccharomycetales / genetics Siderophores / genetics
Saccharomycotina Starmerella Wickerhamiella budding yeasts central dogma of biology enterobactin horizontal gene transfer operon siderophore biosynthesis

Journal

Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066

Informations de publication

Date de publication:
07 03 2019
Historique:
received: 31 10 2018
revised: 20 12 2018
accepted: 23 01 2019
pubmed: 26 2 2019
medline: 7 1 2020
entrez: 26 2 2019
Statut: ppublish

Résumé

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.

Identifiants

DOI: 10.1016/j.cell.2019.01.034 PMID: 30799038 PMC: PMC7295392
pubmed: 30799038
pii: S0092-8674(19)30097-2
doi: 10.1016/j.cell.2019.01.034
pmc: PMC7295392
mid: NIHMS1589789
pii:
doi:

Substances chimiques

Siderophores 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

1356-1366.e10

Subventions

Organisme : NIAID NIH HHS
ID : R21 AI105619
Pays : United States
Organisme : NHGRI NIH HHS
ID : T32 HG002760
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2019 Elsevier Inc. All rights reserved.

Références

Mol Biol Evol. 2008 Jul;25(7):1307-20
pubmed: 18367465
Biometals. 2002 Dec;15(4):325-39
pubmed: 12405526
FEMS Yeast Res. 2001 Apr;1(1):1-8
pubmed: 12702457
Mol Cell Biol. 2004 Sep;24(17):7795-805
pubmed: 15314184
Proc Natl Acad Sci U S A. 2006 Apr 4;103(14):5320-5
pubmed: 16569694
Curr Biol. 2014 Jun 2;24(11):1176-86
pubmed: 24856215
Proc Natl Acad Sci U S A. 2016 Sep 13;113(37):E5416-24
pubmed: 27573819
Nat Rev Genet. 2015 Aug;16(8):472-82
pubmed: 26184597
Nature. 2007 Oct 11;449(7163):677-81
pubmed: 17928853
J Microbiol Methods. 2007 Jul;70(1):127-31
pubmed: 17507108
Elife. 2018 Apr 12;7:
pubmed: 29648535
Nat Commun. 2014 Sep 15;5:4910
pubmed: 25222563
Trends Genet. 1998 Aug;14(8):307-11
pubmed: 9724962
Genome Res. 2008 Feb;18(2):272-80
pubmed: 18073380
FEMS Microbiol Lett. 2012 Apr;329(1):1-8
pubmed: 22112233
Mycologia. 2013 Sep-Oct;105(5):1126-34
pubmed: 23921237
Proc Natl Acad Sci U S A. 2010 Jun 1;107(22):10136-41
pubmed: 20479238
Genetics. 1996 Aug;143(4):1843-60
pubmed: 8844169
Science. 2008 May 30;320(5880):1210-3
pubmed: 18511688
Bioinformatics. 2008 Mar 1;24(5):637-44
pubmed: 18218656
PLoS Pathog. 2014 Jan 30;10(1):e1003859
pubmed: 24497825
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
Nat Biotechnol. 2011 May 15;29(7):644-52
pubmed: 21572440
Science. 1997 Sep 5;277(5331):1453-62
pubmed: 9278503
Proc Natl Acad Sci U S A. 2012 Jun 26;109(26):10426-31
pubmed: 22699510
PLoS Pathog. 2010 Aug 12;6(8):e1000949
pubmed: 20711357
Proc Natl Acad Sci U S A. 2002 Sep 17;99(19):12246-51
pubmed: 12218172
C R Biol. 2011 Aug-Sep;334(8-9):662-70
pubmed: 21819948
BMC Bioinformatics. 2011 Dec 22;12:491
pubmed: 22192575
Bioinformatics. 2014 May 1;30(9):1312-3
pubmed: 24451623
Genome Biol Evol. 2014 Sep;6(9):2543-56
pubmed: 25364803
Curr Biol. 2011 Jan 25;21(2):134-9
pubmed: 21194949
Genes Dev. 2001 Feb 1;15(3):294-303
pubmed: 11159910
Genome Biol. 2003;4(9):R55
pubmed: 12952534
Annu Rev Phytopathol. 2006;44:305-36
pubmed: 16704357
Nat Rev Genet. 2004 Feb;5(2):123-35
pubmed: 14735123
Front Microbiol. 2015 Mar 03;6:161
pubmed: 25784900
Mol Microbiol. 2013 Oct;90(2):290-306
pubmed: 23937442
Science. 2007 Sep 21;317(5845):1753-6
pubmed: 17761848
Cell. 2013 Jun 20;153(7):1567-78
pubmed: 23791183
Genome Biol. 2008 Jan 24;9(1):R18
pubmed: 18218086
Trends Endocrinol Metab. 2010 May;21(5):302-14
pubmed: 20060739
Proc Natl Acad Sci U S A. 2012 Feb 7;109(6):1907-12
pubmed: 22308402
Nature. 2010 Mar 4;464(7285):54-8
pubmed: 20164837
Bioinformatics. 2015 Oct 1;31(19):3210-2
pubmed: 26059717
Nature. 1989 Jul 20;340(6230):205-9
pubmed: 2666856
Nat Rev Genet. 2010 May;11(5):345-55
pubmed: 20376054
J Invertebr Pathol. 1998 Sep;72(2):104-11
pubmed: 9709009
Open Biol. 2016 Nov;6(11):
pubmed: 27906133
Nat Biotechnol. 2015 Mar;33(3):290-5
pubmed: 25690850
Trends Genet. 2015 Nov;31(11):627-636
pubmed: 26431675
Int J Syst Evol Microbiol. 2016 Dec;66(12):5575-5599
pubmed: 27620848
Trends Microbiol. 2008 Jun;16(6):261-8
pubmed: 18467097
Cell. 1993 May 7;73(3):521-32
pubmed: 8098272
Proc Natl Acad Sci U S A. 2011 Sep 13;108(37):15258-63
pubmed: 21878562
Nature. 2013 Aug 22;500(7463):453-7
pubmed: 23873043
J Bacteriol. 2007 Oct;189(19):7112-26
pubmed: 17675380
Curr Microbiol. 1998 Nov;37(5):352-5
pubmed: 9767717
Bioinformatics. 2010 Apr 1;26(7):873-81
pubmed: 20147302
Proc Natl Acad Sci U S A. 2002 Oct 29;99(22):14280-5
pubmed: 12386340
Nature. 2013 May 2;497(7447):127-31
pubmed: 23615609
Mol Cell Biol. 1990 Apr;10(4):1769-72
pubmed: 1690851
G3 (Bethesda). 2016 Dec 7;6(12):3927-3939
pubmed: 27672114
FEMS Microbiol Rev. 2003 Jun;27(2-3):215-37
pubmed: 12829269
Genome Res. 2008 Dec;18(12):1979-90
pubmed: 18757608
Lett Appl Microbiol. 2003;36(3):177-81
pubmed: 12581379
Trends Genet. 2010 Jan;26(1):5-8
pubmed: 19969385
G3 (Bethesda). 2016 Nov 8;6(11):3655-3662
pubmed: 27638685
Annu Rev Microbiol. 2004;58:611-47
pubmed: 15487950
Mol Biol Evol. 2016 Aug;33(8):1979-87
pubmed: 27189567
Mol Biol Evol. 2015 Jan;32(1):268-74
pubmed: 25371430
BMC Syst Biol. 2013 Jun 11;7:46
pubmed: 23758866
ISME J. 2018 Sep;12(9):2163-2175
pubmed: 29880910
Bioinformatics. 2013 Apr 15;29(8):1072-5
pubmed: 23422339
Nat Rev Genet. 2008 Aug;9(8):605-18
pubmed: 18591983
PLoS One. 2012;7(2):e31643
pubmed: 22328943
Annu Rev Genet. 2008;42:165-90
pubmed: 18983256
Nat Rev Microbiol. 2018 Feb;16(2):67-79
pubmed: 29176581
J Bacteriol. 1988 Sep;170(9):3817-26
pubmed: 3045077
Nucleic Acids Res. 2007;35(20):6762-77
pubmed: 17921503
Proc Natl Acad Sci U S A. 2016 Feb 23;113(8):2247-51
pubmed: 26787874
Annu Rev Phytopathol. 2008;46:149-87
pubmed: 18680426
Microbiol Mol Biol Rev. 2000 Dec;64(4):786-820
pubmed: 11104819
Curr Biol. 2006 Sep 19;16(18):1857-64
pubmed: 16979565
Cell. 2018 Nov 29;175(6):1533-1545.e20
pubmed: 30415838
Proc Natl Acad Sci U S A. 2016 Apr 12;113(15):4116-21
pubmed: 27035945
Bioinformatics. 2015 Aug 1;31(15):2577-9
pubmed: 25819675
Proc Natl Acad Sci U S A. 2018 Oct 23;115(43):11030-11035
pubmed: 30297402
FEMS Yeast Res. 2003 Dec;4(3):271-5
pubmed: 14654431
J Mol Biol. 1990 Oct 5;215(3):403-10
pubmed: 2231712
Nucleic Acids Res. 2009 Jul;37(Web Server issue):W202-8
pubmed: 19458158
Nat Rev Genet. 2003 Feb;4(2):112-20
pubmed: 12560808
BMC Evol Biol. 2013 Feb 13;13:40
pubmed: 23405862
BMC Bioinformatics. 2004 May 14;5:59
pubmed: 15144565
Genetics. 2017 Jun;206(2):717-750
pubmed: 28592505
Int J Syst Bacteriol. 1998 Oct;48 Pt 4:1413-7
pubmed: 9828444
Anal Biochem. 1987 Apr;162(1):156-9
pubmed: 2440339

Auteurs

Jacek Kominek (J)

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.

Drew T Doering (DT)

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.

Dana A Opulente (DA)

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.

Xing-Xing Shen (XX)

Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA.

Xiaofan Zhou (X)

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.

Jeremy DeVirgilio (J)

Mycotoxin Prevention and Applied Microbiology Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, US Department of Agriculture, Peoria, IL 61604, USA.

Amanda B Hulfachor (AB)

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.

Marizeth Groenewald (M)

Westerdijk Fungal Biodiversity Institute, 3584 CT, Utrecht, Netherlands.

Mcsean A Mcgee (MA)

DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI 53706, USA.

Steven D Karlen (SD)

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.

Cletus P Kurtzman (CP)

Mycotoxin Prevention and Applied Microbiology Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, US Department of Agriculture, Peoria, IL 61604, USA.

Antonis Rokas (A)

Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA.

Chris Todd Hittinger (CT)

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.

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Classifications MeSH

questionsmedicales.fr › Bactéries › Eukaryotic Acquisition of a Bacterial Operon.
questionsmedicales.fr › Bactéries › Proteobacteria › Gammaproteobacteria › Enterobacteriaceae › Escherichia › Escherichia coli › Eukaryotic Acquisition of a Bacterial Operon.
questionsmedicales.fr › Eucaryotes › Eukaryotic Acquisition of a Bacterial Operon.
questionsmedicales.fr › Cellules › Cellules eucaryotes › Eukaryotic Acquisition of a Bacterial Operon.
questionsmedicales.fr › Phénomènes biologiques › Évolution biologique › Évolution moléculaire › Eukaryotic Acquisition of a Bacterial Operon.
questionsmedicales.fr › Phénomènes génétiques › Régulation de l'expression des gènes › Régulation de l'expression des gènes bactériens › Eukaryotic Acquisition of a Bacterial Operon.
questionsmedicales.fr › Phénomènes génétiques › Recombinaison génétique › Transfert horizontal de gène › Eukaryotic Acquisition of a Bacterial Operon.
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Génome microbien › Génome bactérien › Gènes bactériens › Eukaryotic Acquisition of a Bacterial Operon.
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Génome microbien › Génome bactérien › Eukaryotic Acquisition of a Bacterial Operon.
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Génome microbien › Génome fongique › Eukaryotic Acquisition of a Bacterial Operon.
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Génome microbien › Génome bactérien › Opéron › Eukaryotic Acquisition of a Bacterial Operon.
questionsmedicales.fr › Eucaryotes › Champignons › Ascomycota › Saccharomycetales › Eukaryotic Acquisition of a Bacterial Operon.
questionsmedicales.fr › Actions chimiques et utilisations › Utilisations spécialisées de produits chimiques › Agents séquestrants › Chélateurs › Agents chélateurs du fer › Sidérophores › Eukaryotic Acquisition of a Bacterial Operon.