Loss of YhcB results in dysregulation of coordinated peptidoglycan, LPS and phospholipid synthesis during Escherichia coli cell growth.
Cell Division
/ genetics
Cell Membrane
/ genetics
Cell Wall
/ genetics
Escherichia coli
/ genetics
Escherichia coli Proteins
/ genetics
Gene Expression Regulation, Bacterial
/ genetics
Lipopolysaccharides
/ biosynthesis
Mutagenesis
Oxidoreductases
/ genetics
Peptidoglycan
/ genetics
Phospholipids
/ biosynthesis
Journal
PLoS genetics
ISSN: 1553-7404
Titre abrégé: PLoS Genet
Pays: United States
ID NLM: 101239074
Informations de publication
Date de publication:
12 2021
12 2021
Historique:
received:
12
05
2021
accepted:
24
11
2021
revised:
07
01
2022
pubmed:
24
12
2021
medline:
17
2
2022
entrez:
23
12
2021
Statut:
epublish
Résumé
The cell envelope is essential for viability in all domains of life. It retains enzymes and substrates within a confined space while providing a protective barrier to the external environment. Destabilising the envelope of bacterial pathogens is a common strategy employed by antimicrobial treatment. However, even in one of the best studied organisms, Escherichia coli, there remain gaps in our understanding of how the synthesis of the successive layers of the cell envelope are coordinated during growth and cell division. Here, we used a whole-genome phenotypic screen to identify mutants with a defective cell envelope. We report that loss of yhcB, a conserved gene of unknown function, results in loss of envelope stability, increased cell permeability and dysregulated control of cell size. Using whole genome transposon mutagenesis strategies, we report the comprehensive genetic interaction network of yhcB, revealing all genes with a synthetic negative and a synthetic positive relationship. These genes include those previously reported to have a role in cell envelope biogenesis. Surprisingly, we identified genes previously annotated as essential that became non-essential in a ΔyhcB background. Subsequent analyses suggest that YhcB functions at the junction of several envelope biosynthetic pathways coordinating the spatiotemporal growth of the cell, highlighting YhcB as an as yet unexplored antimicrobial target.
Identifiants
pubmed: 34941903
doi: 10.1371/journal.pgen.1009586
pii: PGENETICS-D-21-00648
pmc: PMC8741058
doi:
Substances chimiques
Escherichia coli Proteins
0
Lipopolysaccharides
0
Peptidoglycan
0
Phospholipids
0
Oxidoreductases
EC 1.-
YhcB protein, E coli
EC 1.9.3.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1009586Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
PLoS Biol. 2009 Apr 28;7(4):e96
pubmed: 19402753
J Bacteriol. 1976 Jul;127(1):660-3
pubmed: 776946
Nucleic Acids Res. 2016 Jul 8;44(W1):W344-50
pubmed: 27166375
EcoSal Plus. 2019 Mar;8(2):
pubmed: 30900542
J Biol Chem. 1980 Feb 25;255(4):1623-9
pubmed: 6243645
FEMS Microbiol Rev. 2017 Sep 1;41(5):672-678
pubmed: 28961755
Cell. 2017 Apr 6;169(2):273-285.e17
pubmed: 28388411
Nat Rev Microbiol. 2016 Jun;14(6):337-45
pubmed: 27026255
Biochim Biophys Acta. 2012 Jun;1817(6):965-76
pubmed: 22201544
Can J Biochem Physiol. 1959 Aug;37(8):911-7
pubmed: 13671378
Nat Protoc. 2015 Jun;10(6):845-58
pubmed: 25950237
Nat Microbiol. 2017 Dec;2(12):1616-1623
pubmed: 29038444
Bioinformatics. 2016 Apr 1;32(7):1109-11
pubmed: 26794317
Cold Spring Harb Perspect Biol. 2010 May;2(5):a000414
pubmed: 20452953
Genomics. 1997 Nov 15;46(1):24-36
pubmed: 9403055
Curr Protoc Mol Biol. 2007 Jul;Chapter 1:1.17.1-1.17.8
pubmed: 18265391
J Biol Chem. 1980 Dec 25;255(24):11949-56
pubmed: 7002930
J Mol Biol. 1999 Sep 17;292(2):195-202
pubmed: 10493868
Mol Microbiol. 2017 Nov;106(3):395-408
pubmed: 28815827
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
Nucleic Acids Res. 2017 Jun 20;45(11):e93
pubmed: 28334803
RNA Biol. 2018;15(10):1319-1335
pubmed: 30293519
J Bacteriol. 1998 Jan;180(1):100-6
pubmed: 9422599
J Bacteriol. 1999 May;181(9):2733-8
pubmed: 10217761
Mar Drugs. 2014 Feb 17;12(2):1023-42
pubmed: 24549203
J Bacteriol. 1978 Aug;135(2):559-74
pubmed: 355233
Bioinformatics. 2021 Jun 9;37(9):1312-1314
pubmed: 32956448
Mol Syst Biol. 2006;2:2006.0008
pubmed: 16738554
Chem Biol. 2005 May;12(5):507-9
pubmed: 15911368
Mol Microbiol. 2006 Jul;61(1):151-64
pubmed: 16824102
EMBO J. 1999 Aug 2;18(15):4108-17
pubmed: 10428950
Mol Microbiol. 2005 Sep;57(5):1450-9
pubmed: 16102012
Elife. 2016 Aug 16;5:
pubmed: 27529189
PLoS Genet. 2017 Jul 27;13(7):e1006934
pubmed: 28749938
EMBO J. 1997 Dec 1;16(23):6947-55
pubmed: 9384574
J Bacteriol. 2008 Jul;190(13):4460-9
pubmed: 18424520
Proc Natl Acad Sci U S A. 2014 Dec 2;111(48):17284-9
pubmed: 25404340
Nature. 2020 Aug;584(7821):479-483
pubmed: 32788728
DNA Res. 2007 Dec 31;14(6):237-46
pubmed: 18180259
Cell. 2005 Apr 22;121(2):235-45
pubmed: 15851030
J Gen Microbiol. 1958 Dec;19(3):592-606
pubmed: 13611202
J Biochem. 2004 Feb;135(2):185-91
pubmed: 15047720
Cell. 2012 Aug 17;150(4):752-63
pubmed: 22901807
Curr Biol. 2017 Jun 19;27(12):1757-1767.e5
pubmed: 28602657
EMBO J. 2000 Oct 2;19(19):5071-80
pubmed: 11013210
J Bacteriol. 1984 Nov;160(2):724-32
pubmed: 6094489
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
EMBO J. 2020 Mar 2;39(5):e102246
pubmed: 32009249
Proc Natl Acad Sci U S A. 2009 May 12;106(19):8009-14
pubmed: 19383799
Proc Natl Acad Sci U S A. 2018 Sep 4;115(36):E8518-E8527
pubmed: 30087182
Genome Res. 2009 Dec;19(12):2308-16
pubmed: 19826075
Microsc Res Tech. 1997 Mar 1;36(5):422-7
pubmed: 9140944
EMBO J. 2009 Feb 4;28(3):193-204
pubmed: 19078962
J Biol Chem. 2021 Jan-Jun;296:100700
pubmed: 33895137
J Bacteriol. 1999 Oct;181(20):6564-8
pubmed: 10515954
Infect Immun. 2011 Oct;79(10):4105-21
pubmed: 21768276
J Bacteriol. 1987 Apr;169(4):1454-9
pubmed: 3031013
Curr Opin Microbiol. 2015 Apr;24:96-103
pubmed: 25662920
PLoS One. 2014 Jun 26;9(6):e100941
pubmed: 24967819
Adv Exp Med Biol. 2019;1145:37-54
pubmed: 31364070
mBio. 2020 Apr 14;11(2):
pubmed: 32291302
Sci Rep. 2017 Aug 17;7(1):8608
pubmed: 28819315
Science. 2018 Feb 16;359(6377):798-801
pubmed: 29449493
Nucleic Acids Res. 2019 Jul 2;47(W1):W256-W259
pubmed: 30931475
mBio. 2019 Feb 5;10(1):
pubmed: 30723128
J Antimicrob Chemother. 2001 Jul;48 Suppl 1:5-16
pubmed: 11420333
FEMS Microbiol Rev. 2008 Mar;32(2):321-44
pubmed: 18291013
Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6640-5
pubmed: 10829079
ACS Chem Biol. 2021 Apr 16;16(4):691-700
pubmed: 33740380
Mol Microbiol. 1999 Feb;31(3):833-44
pubmed: 10048027
Nucleic Acids Res. 2019 Jul 2;47(W1):W402-W407
pubmed: 31251384
Biochim Biophys Acta. 2006 Jul;1757(7):860-4
pubmed: 16863643
Anal Biochem. 1988 Aug 1;172(2):451-64
pubmed: 3056100
Bioinformatics. 2010 Jan 1;26(1):139-40
pubmed: 19910308
Cold Spring Harb Perspect Med. 2016 Oct 3;6(10):
pubmed: 27503996
Mol Microbiol. 2014 Jan;91(1):145-57
pubmed: 24266962
mBio. 2020 May 19;11(3):
pubmed: 32430473
EMBO J. 1995 Jul 17;14(14):3365-72
pubmed: 7628437
Cell Res. 2020 Dec;30(12):1127-1135
pubmed: 32884137
ISRN Mol Biol. 2012 Sep 03;2012:304021
pubmed: 27335665
Philos Trans R Soc Lond B Biol Sci. 2015 Oct 5;370(1679):
pubmed: 26370941
PLoS Comput Biol. 2020 Jul 17;16(7):e1007980
pubmed: 32678849
J Bacteriol. 2003 Sep;185(17):5328-32
pubmed: 12923112
J Bacteriol. 1988 May;170(5):2031-9
pubmed: 3283102
PLoS Comput Biol. 2011 Oct;7(10):e1002195
pubmed: 22039361
mBio. 2018 Mar 20;9(2):
pubmed: 29559571
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
mBio. 2018 Feb 20;9(1):
pubmed: 29463657
Proc Natl Acad Sci U S A. 2015 Sep 1;112(35):10956-61
pubmed: 26283368
Infect Immun. 2000 Aug;68(8):4485-91
pubmed: 10899846
J Biol Chem. 2014 May 23;289(21):14829-53
pubmed: 24722986
J Antimicrob Chemother. 2020 Nov 1;75(11):3144-3151
pubmed: 32756955
J Biol Chem. 1980 Apr 25;255(8):3263-5
pubmed: 6988423
Mol Microbiol. 2019 Jul;112(1):233-248
pubmed: 31022322
Microbiol Rev. 1985 Mar;49(1):1-32
pubmed: 2580220
Mol Biol Evol. 2015 Jan;32(1):268-74
pubmed: 25371430
Cell. 2011 Jan 7;144(1):143-56
pubmed: 21185072
Nat Commun. 2014 Jun 27;5:4244
pubmed: 24968740
J Bacteriol. 1999 Jan;181(2):483-92
pubmed: 9882662
Eur J Biochem. 2000 May;267(10):2871-81
pubmed: 10806384
Nat Rev Microbiol. 2009 Mar;7(3):206-14
pubmed: 19182809
J Bacteriol. 1998 Nov;180(22):5875-84
pubmed: 9811644
Antimicrob Agents Chemother. 1986 May;29(5):781-8
pubmed: 3015004
Nat Rev Genet. 2020 Sep;21(9):526-540
pubmed: 32533119
Nat Cell Biol. 2000 Apr;2(4):212-8
pubmed: 10783239
J Bacteriol. 2000 Mar;182(6):1714-21
pubmed: 10692378
J Biol Chem. 1964 Jun;239:1720-6
pubmed: 14213340
Nucleic Acids Res. 2017 Jan 4;45(D1):D543-D550
pubmed: 27899573
Curr Biol. 2005 Jul 12;15(13):R514-26
pubmed: 16005287
J Bacteriol. 2001 May;183(10):3055-64
pubmed: 11325933
Mol Microbiol. 2020 Dec;114(6):991-1005
pubmed: 32808719
Proc Natl Acad Sci U S A. 2016 Mar 15;113(11):E1565-74
pubmed: 26929379
Cell. 2005 Apr 22;121(2):307-17
pubmed: 15851036
Nature. 1953 Jul 25;172(4369):160-1
pubmed: 13072617
Biochim Biophys Acta Mol Cell Biol Lipids. 2017 Nov;1862(11):1404-1413
pubmed: 27956138
Mol Microbiol. 2012 Dec;86(5):1036-51
pubmed: 23062283
PLoS Genet. 2013;9(7):e1003663
pubmed: 23935518
EMBO J. 2008 Dec 3;27(23):3081-91
pubmed: 19008860
Nucleic Acids Res. 2021 Jan 8;49(D1):D394-D403
pubmed: 33290554
Genome Res. 2012 Mar;22(3):568-76
pubmed: 22300766
Biochemistry. 2019 Jan 15;58(2):114-119
pubmed: 30284446
Mol Biol Cell. 2012 May;23(10):1826-37
pubmed: 22456503
Nat Methods. 2017 Jun;14(6):587-589
pubmed: 28481363
Nat Microbiol. 2019 Oct;4(10):1692-1705
pubmed: 31235958
Bioinformatics. 2000 Oct;16(10):944-5
pubmed: 11120685
J Proteome Res. 2011 Apr 1;10(4):1848-59
pubmed: 21210718
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
J Biol Chem. 2019 Sep 27;294(39):14175-14184
pubmed: 31420446
Philos Trans R Soc Lond B Biol Sci. 2015 Oct 5;370(1679):
pubmed: 26370939
Mol Microbiol. 2016 Apr;100(1):1-14
pubmed: 26593043
Sci Rep. 2017 Feb 15;7:42483
pubmed: 28198411
Nat Rev Microbiol. 2020 Aug;18(8):446-460
pubmed: 32424210
Annu Rev Microbiol. 2011;65:239-59
pubmed: 21663440
Mol Microbiol. 2015 Dec;98(6):1133-46
pubmed: 26314242
Nucleic Acids Res. 2019 Jan 8;47(D1):D309-D314
pubmed: 30418610
J Biol Chem. 2004 Oct 22;279(43):44966-75
pubmed: 15319435
J Microbiol. 2020 Jul;58(7):598-605
pubmed: 32323199
Methods Mol Biol. 2014;1151:165-88
pubmed: 24838886