Extreme Antagonism Arising from Gene-Environment Interactions.
Journal
Biophysical journal
ISSN: 1542-0086
Titre abrégé: Biophys J
Pays: United States
ID NLM: 0370626
Informations de publication
Date de publication:
17 11 2020
17 11 2020
Historique:
received:
12
05
2020
revised:
27
08
2020
accepted:
21
09
2020
pubmed:
18
10
2020
medline:
15
5
2021
entrez:
17
10
2020
Statut:
ppublish
Résumé
Antagonistic interactions in biological systems, which occur when one perturbation blunts the effect of another, are typically interpreted as evidence that the two perturbations impact the same cellular pathway or function. Yet, this interpretation ignores extreme antagonistic interactions wherein an otherwise deleterious perturbation compensates for the function lost because of a prior perturbation. Here, we report on gene-environment interactions involving genetic mutations that are deleterious in a permissive environment but beneficial in a specific environment that restricts growth. These extreme antagonistic interactions constitute gene-environment analogs of synthetic rescues previously observed for gene-gene interactions. Our approach uses two independent adaptive evolution steps to address the lack of experimental methods to systematically identify such extreme interactions. We apply the approach to Escherichia coli by successively adapting it to defined glucose media without and with the antibiotic rifampicin. The approach identified multiple mutations that are beneficial in the presence of rifampicin and deleterious in its absence. The analysis of transcription shows that the antagonistic adaptive mutations repress a stringent response-like transcriptional program, whereas nonantagonistic mutations have an opposite transcriptional profile. Our approach represents a step toward the systematic characterization of extreme antagonistic gene-drug interactions, which can be used to identify targets to select against antibiotic resistance.
Identifiants
pubmed: 33068537
pii: S0006-3495(20)30776-1
doi: 10.1016/j.bpj.2020.09.038
pmc: PMC7732749
pii:
doi:
Substances chimiques
Rifampin
VJT6J7R4TR
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
2074-2086Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM113238
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM131762
Pays : United States
Organisme : NIDDK NIH HHS
ID : T32 DK007074
Pays : United States
Informations de copyright
Copyright © 2020 Biophysical Society. Published by Elsevier Inc. All rights reserved.
Références
Biochem Soc Trans. 2006 Dec;34(Pt 6):1062-6
pubmed: 17073751
PLoS Biol. 2013;11(4):e1001540
pubmed: 23630452
PLoS Genet. 2011 Feb 10;7(2):e1001294
pubmed: 21347328
Evolution. 2005 Jun;59(6):1165-74
pubmed: 16050094
Proc Natl Acad Sci U S A. 2010 Nov 23;107(47):20500-5
pubmed: 21057108
Methods Mol Biol. 2014;1151:165-88
pubmed: 24838886
J Theor Biol. 2005 Dec 21;237(4):401-11
pubmed: 15975601
PLoS Genet. 2012 Jan;8(1):e1002444
pubmed: 22253602
Mol Biol Evol. 2020 May 1;37(5):1394-1406
pubmed: 31851309
Evolution. 2014 Dec;68(12):3537-54
pubmed: 25311558
Trends Genet. 2011 Aug;27(8):323-31
pubmed: 21684621
J Evol Biol. 2013 Aug;26(8):1655-64
pubmed: 23701170
Mol Biol Evol. 2010 Jun;27(6):1338-47
pubmed: 20106907
DNA Repair (Amst). 2003 May 13;2(5):593-608
pubmed: 12713816
PLoS Pathog. 2020 Mar 2;16(3):e1008278
pubmed: 32119717
Proc Natl Acad Sci U S A. 2015 Sep 1;112(35):11048-53
pubmed: 26283394
Nature. 2007 Apr 5;446(7136):668-71
pubmed: 17410176
Nat Methods. 2008 Sep;5(9):781-7
pubmed: 19160513
Mol Cell. 2013 May 9;50(3):420-9
pubmed: 23623682
Nature. 2013 Feb 28;494(7438):463-7
pubmed: 23395960
Sci Transl Med. 2015 Jul 22;7(297):297ra114
pubmed: 26203082
Nat Genet. 2004 Apr;36(4):423-6
pubmed: 15072075
Mol Syst Biol. 2008;4:168
pubmed: 18277384
Antimicrob Agents Chemother. 2018 May 25;62(6):
pubmed: 29661864
Nat Commun. 2014 Jul 08;5:4352
pubmed: 25000950
PLoS Genet. 2009 Jul;5(7):e1000578
pubmed: 19629166
Nat Commun. 2019 Jan 18;10(1):334
pubmed: 30659188
PLoS Biol. 2019 Oct 25;17(10):e3000515
pubmed: 31652256
Appl Microbiol Biotechnol. 2019 Mar;103(5):2155-2170
pubmed: 30623201
Bioessays. 2010 Mar;32(3):236-45
pubmed: 20127700
Nucleic Acids Res. 2015 Jan;43(Database issue):D261-9
pubmed: 25428365
PLoS Genet. 2018 Mar 27;14(3):e1007284
pubmed: 29584733
Environ Microbiol Rep. 2017 Oct;9(5):635-641
pubmed: 28677342
Cell. 2009 Nov 13;139(4):707-18
pubmed: 19914165
Proc Natl Acad Sci U S A. 2008 Mar 4;105(9):3461-6
pubmed: 18305163
Nat Genet. 2011 Dec 18;44(1):106-10
pubmed: 22179134
Cell. 2001 Mar 23;104(6):901-12
pubmed: 11290327
J Biol. 2003;2(2):14
pubmed: 12775217
Evol Appl. 2019 Aug 11;12(9):1721-1742
pubmed: 31548853
Nat Commun. 2019 Dec 4;10(1):5536
pubmed: 31797920
Bioinformatics. 2019 Jun 1;35(12):2084-2092
pubmed: 30395178
Proc Natl Acad Sci U S A. 2016 Sep 13;113(37):10442-7
pubmed: 27562164
Science. 2001 May 18;292(5520):1315-6
pubmed: 11360989
Mol Biol Evol. 2018 Nov 1;35(11):2669-2684
pubmed: 30169679
Proc Natl Acad Sci U S A. 2019 Dec 10;116(50):25162-25171
pubmed: 31754027
J Biol Chem. 2013 Jan 25;288(4):2700-10
pubmed: 23223236
BMC Bioinformatics. 2019 Mar 7;20(1):117
pubmed: 30845912
J Bacteriol. 2008 Feb;190(3):1084-96
pubmed: 18039766
Proc Natl Acad Sci U S A. 2012 Oct 9;109(41):E2774-83
pubmed: 22991466
Nat Methods. 2008 Sep;5(9):789-95
pubmed: 18677321
Science. 2014 Jun 13;344(6189):1285-9
pubmed: 24926020
BMC Syst Biol. 2012 May 25;6:48
pubmed: 22631053
PLoS One. 2014 Apr 08;9(4):e93960
pubmed: 24713621
Proc Biol Sci. 2016 Jan 13;283(1822):
pubmed: 26763710
Ecol Lett. 2015 Sep;18(9):892-8
pubmed: 26119065
Evolution. 2019 Oct;73(10):2094-2105
pubmed: 31418459
BMC Evol Biol. 2013 Aug 02;13:163
pubmed: 23914906
Behav Brain Res. 2001 Nov 1;125(1-2):279-84
pubmed: 11682119
Cell. 2011 Apr 1;145(1):30-8
pubmed: 21458666
Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6640-5
pubmed: 10829079
Evolution. 2013 Dec;67(12):3512-22
pubmed: 24299404
Proc Natl Acad Sci U S A. 2005 May 24;102(21):7695-700
pubmed: 15897462
Environ Microbiol. 2016 Jan;18(1):100-17
pubmed: 25808978
Cell Syst. 2019 Nov 27;9(5):423-433.e3
pubmed: 31734160
Nucleic Acids Res. 2019 Jan 8;47(D1):D212-D220
pubmed: 30395280
Proc Natl Acad Sci U S A. 2005 May 31;102(22):7841-6
pubmed: 15908506
J Mol Biol. 1988 Jul 5;202(1):45-58
pubmed: 3050121
Genetics. 2009 Oct;183(2):539-46, 1SI-2SI
pubmed: 19652179
Cell. 2011 Aug 5;146(3):462-70
pubmed: 21802129
Science. 2016 Sep 23;353(6306):
pubmed: 27708008
Nat Commun. 2018 Sep 18;9(1):3796
pubmed: 30228271
Mol Biol Evol. 2019 Jul 1;36(7):1533-1550
pubmed: 30982891
Proc Natl Acad Sci U S A. 2008 Nov 25;105(47):18159-64
pubmed: 19017803
Proc Natl Acad Sci U S A. 2006 Jun 13;103(24):9107-12
pubmed: 16751270
Leukemia. 1999 Dec;13(12):2031-5
pubmed: 10602425
Annu Rev Microbiol. 2012;66:103-23
pubmed: 22994490
Science. 2004 Feb 6;303(5659):808-13
pubmed: 14764870
EMBO J. 2002 Dec 16;21(24):6944-53
pubmed: 12486015
Science. 2016 Jan 1;351(6268):aad3292
pubmed: 26722002
Proc Natl Acad Sci U S A. 2011 Feb 22;108(8):3124-9
pubmed: 21300895
Sci Adv. 2016 Jan 22;2(1):e1500921
pubmed: 26844293
Sci Transl Med. 2013 Sep 25;5(204):204ra132
pubmed: 24068739
Nature. 2016 Jan 21;529(7586):336-43
pubmed: 26791724
Genetics. 2011 Mar;187(3):817-22
pubmed: 21220359
J Biol. 2006;5(4):11
pubmed: 16762047
Proc Natl Acad Sci U S A. 2018 Sep 25;115(39):9767-9772
pubmed: 30209218
J Mol Biol. 1988 Jul 20;202(2):245-53
pubmed: 3050123
Nat Methods. 2009 Oct;6(10):767-72
pubmed: 19767758
J Mol Biol. 2006 Mar 10;356(5):1163-79
pubmed: 16405998
Nucleic Acids Res. 2019 Jan 8;47(D1):D419-D426
pubmed: 30407594
J Antimicrob Chemother. 2004 Feb;53(2):203-7
pubmed: 14688044
Mol Syst Biol. 2015 Aug 31;11(8):827
pubmed: 26324468
Nature. 2015 Dec 3;528(7580):99-104
pubmed: 26632588
Elife. 2019 Oct 29;8:
pubmed: 31658946
Sci Rep. 2015 Nov 04;5:16025
pubmed: 26531810