Essential gene acquisition destabilizes plasmid inheritance.


Journal

PLoS genetics
ISSN: 1553-7404
Titre abrégé: PLoS Genet
Pays: United States
ID NLM: 101239074

Informations de publication

Date de publication:
07 2021
Historique:
received: 07 12 2020
accepted: 09 06 2021
revised: 22 07 2021
pubmed: 13 7 2021
medline: 9 11 2021
entrez: 12 7 2021
Statut: epublish

Résumé

Extra-chromosomal genetic elements are important drivers of evolutionary transformations and ecological adaptations in prokaryotes with their evolutionary success often depending on their 'utility' to the host. Examples are plasmids encoding antibiotic resistance genes, which are known to proliferate in the presence of antibiotics. Plasmids carrying an essential host function are recognized as permanent residents in their host. Essential plasmids have been reported in several taxa where they often encode essential metabolic functions; nonetheless, their evolution remains poorly understood. Here we show that essential genes are rarely encoded on plasmids; evolving essential plasmids in Escherichia coli we further find that acquisition of an essential chromosomal gene by a plasmid can lead to plasmid extinction. A comparative genomics analysis of Escherichia isolates reveals few plasmid-encoded essential genes, yet these are often integrated into plasmid-related functions; an example is the GroEL/GroES chaperonin. Experimental evolution of a chaperonin-encoding plasmid shows that the acquisition of an essential gene reduces plasmid fitness regardless of the stability of plasmid inheritance. Our results suggest that essential plasmid emergence leads to a dose effect caused by gene redundancy. The detrimental effect of essential gene acquisition on plasmid inheritance constitutes a barrier for plasmid-mediated lateral gene transfer and supplies a mechanistic understanding for the rarity of essential genes in extra-chromosomal genetic elements.

Identifiants

pubmed: 34252089
doi: 10.1371/journal.pgen.1009656
pii: PGENETICS-D-20-01843
pmc: PMC8297927
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1009656

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

Microbiology (Reading). 1994 Jan;140 ( Pt 1):113-22
pubmed: 7909257
J Vis Exp. 2019 Dec 14;(154):
pubmed: 31885375
Plasmid. 2013 Nov;70(3):353-61
pubmed: 24042048
Gene. 1982 Oct;19(3):327-36
pubmed: 6295884
Nat Rev Genet. 2018 Jan;19(1):34-49
pubmed: 29033457
Trends Microbiol. 2012 Jun;20(6):262-7
pubmed: 22564249
Bioinformatics. 2009 Jul 15;25(14):1754-60
pubmed: 19451168
Nature. 2011 Oct 30;480(7376):241-4
pubmed: 22037308
Mol Biol Evol. 2008 Mar;25(3):559-67
pubmed: 18158322
Nat Microbiol. 2021 Mar;6(3):301-312
pubmed: 33462433
Mol Biol Evol. 2015 Dec;32(12):3079-88
pubmed: 25540453
Biochemistry. 2012 Dec 18;51(50):9941-53
pubmed: 23167595
Nature. 1998 Mar 12;392(6672):139
pubmed: 9515958
Nat Ecol Evol. 2017 Sep;1(9):1354-1363
pubmed: 29046540
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
Genetics. 2000 Aug;155(4):1505-19
pubmed: 10924453
Nat Commun. 2021 Apr 28;12(1):2460
pubmed: 33911082
BMC Bioinformatics. 2016 Apr 19;17:172
pubmed: 27094401
Mol Syst Biol. 2006;2:2006.0008
pubmed: 16738554
Genome Res. 2010 Sep;20(9):1297-303
pubmed: 20644199
Nature. 1988 Sep 22;335(6188):351-2
pubmed: 3047585
Proc Natl Acad Sci U S A. 1983 Sep;80(18):5480-4
pubmed: 6351061
Trends Genet. 2000 Jun;16(6):276-7
pubmed: 10827456
Nucleic Acids Res. 2020 Jan 8;48(D1):D517-D525
pubmed: 31665441
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
BMC Genomics. 2010 Oct 20;11:588
pubmed: 20961426
Trends Ecol Evol. 2013 Aug;28(8):489-95
pubmed: 23706556
Proc Natl Acad Sci U S A. 2015 Nov 17;112(46):14343-7
pubmed: 26534993
Science. 2007 Nov 30;318(5855):1449-52
pubmed: 17947550
J Bacteriol. 1989 Mar;171(3):1379-85
pubmed: 2563997
Biochem Cell Biol. 2010 Apr;88(2):185-94
pubmed: 20453921
J Bacteriol. 2008 May;190(10):3712-20
pubmed: 18359805
J Bacteriol. 2013 Jan;195(2):202-12
pubmed: 23123907
Curr Opin Microbiol. 2011 Jun;14(3):236-43
pubmed: 21546307
Gene. 2006 Mar 29;370:17-25
pubmed: 16413149
Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W609-12
pubmed: 16845082
Sci Rep. 2017 Jul 7;7(1):4853
pubmed: 28687759
Nat Microbiol. 2019 Mar;4(3):504-514
pubmed: 30742072
Mol Biol Evol. 2015 Oct;32(10):2681-93
pubmed: 26116858
Nucleic Acids Res. 2019 Jul 2;47(W1):W256-W259
pubmed: 30931475
Mol Biol Evol. 2011 Apr;28(4):1481-9
pubmed: 21149642
Science. 2001 Jul 27;293(5530):668-72
pubmed: 11474104
Nat Ecol Evol. 2018 May;2(5):873-881
pubmed: 29632354
mBio. 2014 Oct 07;5(5):e01918-14
pubmed: 25293762
Nat Commun. 2019 Jun 13;10(1):2595
pubmed: 31197163
mBio. 2018 Nov 6;9(6):
pubmed: 30401772
Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):3801-6
pubmed: 10097118
Nucleic Acids Res. 1999 Oct 1;27(19):3821-35
pubmed: 10481021
Front Microbiol. 2015 Mar 03;6:152
pubmed: 26074880
Cold Spring Harb Perspect Biol. 2015 Jun 01;7(6):
pubmed: 26032716
Sci Rep. 2018 Jan 10;8(1):390
pubmed: 29321680
Genetics. 1977 Oct;87(2):209-28
pubmed: 17248761
mBio. 2018 Feb 20;9(1):
pubmed: 29463657
Mol Microbiol. 1992 Jul;6(13):1785-99
pubmed: 1321324
Mol Biol Evol. 2017 Jul 1;34(7):1743-1757
pubmed: 28419279
Bioinformatics. 2020 Jul 1;36(Suppl_1):i21-i29
pubmed: 32657415
Mol Biol Evol. 2015 Jan;32(1):268-74
pubmed: 25371430
PLoS Genet. 2012;8(7):e1002764
pubmed: 22807683
Nucleic Acids Res. 2012 Dec;40(22):11189-201
pubmed: 23066108
FEMS Microbiol Ecol. 2007 Mar;59(3):738-48
pubmed: 17059480
Nature. 2002 May 23;417(6887):398
pubmed: 12024205
Nucleic Acids Res. 2002 Apr 1;30(7):1575-84
pubmed: 11917018
Curr Opin Microbiol. 2017 Aug;38:74-80
pubmed: 28538166
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Curr Biol. 2020 Oct 5;30(19):3841-3847.e4
pubmed: 32795438
ISME J. 2010 Dec;4(12):1568-80
pubmed: 20520653
FEMS Microbiol Rev. 2011 Sep;35(5):936-56
pubmed: 21711366
Genome Res. 2006 May;16(5):636-43
pubmed: 16651664
BMC Bioinformatics. 2009 Dec 15;10:421
pubmed: 20003500
Biotechnology. 1991;15:173-92
pubmed: 2009380
Trends Microbiol. 2010 Apr;18(4):141-8
pubmed: 20080407
J Bacteriol. 2007 Mar;189(5):1884-9
pubmed: 17158666
BMC Microbiol. 2020 Oct 28;20(1):326
pubmed: 33115402
PLoS One. 2011;6(9):e25334
pubmed: 21966500

Auteurs

Tanita Wein (T)

Institute of General Microbiology, Kiel University, Kiel, Germany.

Yiqing Wang (Y)

Institute of General Microbiology, Kiel University, Kiel, Germany.

Myriam Barz (M)

Institute of General Microbiology, Kiel University, Kiel, Germany.

Fenna T Stücker (FT)

Institute of General Microbiology, Kiel University, Kiel, Germany.

Katrin Hammerschmidt (K)

Institute of General Microbiology, Kiel University, Kiel, Germany.

Tal Dagan (T)

Institute of General Microbiology, Kiel University, Kiel, Germany.

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