Outer membrane lipoprotein NlpI scaffolds peptidoglycan hydrolases within multi-enzyme complexes in Escherichia coli.
bacterial cell envelope
endopeptidase
outer membrane lipoprotein
penicillin-binding protein
peptidoglycan
Journal
The EMBO journal
ISSN: 1460-2075
Titre abrégé: EMBO J
Pays: England
ID NLM: 8208664
Informations de publication
Date de publication:
02 03 2020
02 03 2020
Historique:
received:
15
04
2019
revised:
20
12
2019
accepted:
14
01
2020
pubmed:
6
2
2020
medline:
3
11
2020
entrez:
4
2
2020
Statut:
ppublish
Résumé
The peptidoglycan (PG) sacculus provides bacteria with the mechanical strength to maintain cell shape and resist osmotic stress. Enlargement of the mesh-like sacculus requires the combined activity of peptidoglycan synthases and hydrolases. In Escherichia coli, the activity of two PG synthases is driven by lipoproteins anchored in the outer membrane (OM). However, the regulation of PG hydrolases is less well understood, with only regulators for PG amidases having been described. Here, we identify the OM lipoprotein NlpI as a general adaptor protein for PG hydrolases. NlpI binds to different classes of hydrolases and can specifically form complexes with various PG endopeptidases. In addition, NlpI seems to contribute both to PG elongation and division biosynthetic complexes based on its localization and genetic interactions. Consistent with such a role, we reconstitute PG multi-enzyme complexes containing NlpI, the PG synthesis regulator LpoA, its cognate bifunctional synthase, PBP1A, and different endopeptidases. Our results indicate that peptidoglycan regulators and adaptors are part of PG biosynthetic multi-enzyme complexes, regulating and potentially coordinating the spatiotemporal action of PG synthases and hydrolases.
Identifiants
pubmed: 32009249
doi: 10.15252/embj.2019102246
pmc: PMC7049810
doi:
Substances chimiques
Escherichia coli Proteins
0
Lipoproteins
0
Multienzyme Complexes
0
NlpI protein, E coli
0
Peptidoglycan
0
peptidoglycan endopeptidase
0
Endopeptidases
EC 3.4.-
N-Acetylmuramoyl-L-alanine Amidase
EC 3.5.1.28
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e102246Subventions
Organisme : Volkswagen Foundation (VolkswagenStiftung)
Pays : International
Organisme : European Molecular Biology Laboratory (EMBL)
ID : 664726
Pays : International
Organisme : EC|H2020|H2020 Priority Excellent Science|H2020 European Research Council (ERC)
ID : 679980
Pays : International
Organisme : Medical Research Council
ID : MR/N002679/1
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Agence Nationale de la Recherche (ANR)
ID : ANR-10-LABX-62-IBEID
Pays : International
Organisme : Wellcome Trust (WT)
ID : 101824/Z/13/Z
Pays : International
Organisme : Royal Society
ID : RGS\R1\191041
Pays : International
Organisme : Medical Research Council
ID : MR/N501840/1
Pays : United Kingdom
Informations de copyright
© 2020 The Authors. Published under the terms of the CC BY 4.0 license.
Références
Structure. 2014 Jul 8;22(7):1047-54
pubmed: 24954617
Biophys J. 2000 Mar;78(3):1606-19
pubmed: 10692345
Microbiol Mol Biol Rev. 1998 Mar;62(1):181-203
pubmed: 9529891
EMBO J. 2020 Mar 2;39(5):e102246
pubmed: 32009249
Front Microbiol. 2015 Jun 11;6:586
pubmed: 26124755
Nat Microbiol. 2017 Feb 17;2:17014
pubmed: 28211844
Mol Microbiol. 2013 Aug;89(4):690-701
pubmed: 23796240
Nature. 2011 May 19;473(7347):337-42
pubmed: 21593866
Curr Opin Microbiol. 2017 Apr;36:55-61
pubmed: 28214390
Nat Protoc. 2015 Oct;10(10):1567-93
pubmed: 26379230
J Biol Chem. 2006 Sep 15;281(37):26985-93
pubmed: 16840781
FEBS J. 2005 Jan;272(1):166-79
pubmed: 15634341
Cell. 2010 Dec 23;143(7):1097-109
pubmed: 21183073
Curr Opin Microbiol. 2017 Apr;36:85-94
pubmed: 28254403
J Bacteriol. 2009 Aug;191(16):5094-107
pubmed: 19525345
J Biol Chem. 2005 Nov 11;280(45):38096-101
pubmed: 16154998
Cold Spring Harb Perspect Biol. 2010 May;2(5):a000414
pubmed: 20452953
J Gen Microbiol. 1985 Oct;131(10):2839-45
pubmed: 3906031
Infect Immun. 2014 May;82(5):2115-24
pubmed: 24614657
Bioinformatics. 2002;18 Suppl 1:S96-104
pubmed: 12169536
Anal Biochem. 1976 May 7;72:248-54
pubmed: 942051
Mol Microbiol. 2018 Nov;110(3):335-356
pubmed: 30044025
Mol Syst Biol. 2006;2:2006.0008
pubmed: 16738554
Sci Rep. 2015 Dec 08;5:18190
pubmed: 26643979
Mol Microbiol. 2012 Jul;85(1):179-94
pubmed: 22606933
Mol Microbiol. 2012 Aug;85(4):768-81
pubmed: 22715947
Assay Drug Dev Technol. 2011 Aug;9(4):342-53
pubmed: 21812660
Cell. 2018 May 31;173(6):1495-1507.e18
pubmed: 29706546
PLoS Genet. 2017 Jul 27;13(7):e1006934
pubmed: 28749938
Mol Microbiol. 2003 Jan;47(2):539-47
pubmed: 12519203
Nat Rev Microbiol. 2015 Sep;13(9):559-72
pubmed: 26256789
Mol Microbiol. 2018 Mar;107(6):676-687
pubmed: 29315884
Nucleic Acids Res. 2015 Apr 20;43(7):e47
pubmed: 25605792
EMBO J. 2010 Apr 21;29(8):1412-22
pubmed: 20300061
Infect Immun. 2010 Jul;78(7):3090-6
pubmed: 20421385
Nat Biotechnol. 2008 Dec;26(12):1367-72
pubmed: 19029910
Microbiologyopen. 2015 Jun;4(3):375-89
pubmed: 25755088
Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6640-5
pubmed: 10829079
Proc Natl Acad Sci U S A. 2018 Mar 20;115(12):3150-3155
pubmed: 29507210
mBio. 2019 Feb 5;10(1):
pubmed: 30723128
Anal Biochem. 1988 Aug 1;172(2):451-64
pubmed: 3056100
Microbiol Mol Biol Rev. 2011 Dec;75(4):636-63
pubmed: 22126997
Gene. 1995 May 26;158(1):9-14
pubmed: 7789817
Proc Natl Acad Sci U S A. 2019 Apr 16;116(16):7825-7830
pubmed: 30940749
Bioessays. 1999 Nov;21(11):932-9
pubmed: 10517866
Science. 2014 Oct 3;346(6205):1255784
pubmed: 25278616
FEMS Microbiol Rev. 2008 Mar;32(2):149-67
pubmed: 18194336
EMBO J. 1998 Mar 2;17(5):1192-9
pubmed: 9482716
Proc Natl Acad Sci U S A. 2015 Sep 1;112(35):10956-61
pubmed: 26283368
PLoS Genet. 2014 Jan;10(1):e1004056
pubmed: 24391520
Protein Sci. 2006 May;15(5):1193-8
pubmed: 16641492
Eur Biophys J. 2010 Feb;39(3):423-35
pubmed: 19234696
PLoS Genet. 2017 Jul 14;13(7):e1006888
pubmed: 28708841
Cell. 2010 Dec 23;143(7):1110-20
pubmed: 21183074
Nat Commun. 2017 Nov 15;8(1):1516
pubmed: 29138488
Mol Microbiol. 2016 Feb;99(4):700-18
pubmed: 26507882
Mol Syst Biol. 2018 Jul 6;14(7):e8242
pubmed: 29980614
Proc Natl Acad Sci U S A. 2014 Jun 3;111(22):8197-202
pubmed: 24821816
Nat Rev Microbiol. 2011 Dec 28;10(2):123-36
pubmed: 22203377
Mol Microbiol. 2012 Dec;86(5):1036-51
pubmed: 23062283
J Biol Chem. 2003 May 30;278(22):19898-903
pubmed: 12663672
Cell. 2014 Apr 24;157(3):624-35
pubmed: 24766808
Biochemistry. 2006 Jan 24;45(3):783-92
pubmed: 16411754
Nature. 2016 Sep 29;537(7622):634-638
pubmed: 27525505
Structure. 2012 Mar 7;20(3):397-405
pubmed: 22404999
FEMS Microbiol Rev. 2008 Mar;32(2):259-86
pubmed: 18266855
Elife. 2015 May 07;4:
pubmed: 25951518
J Bacteriol. 1999 Jul;181(14):4318-25
pubmed: 10400590
BMC Biol. 2017 Feb 21;15(1):17
pubmed: 28222723
J Biol Chem. 1999 Mar 5;274(10):6726-34
pubmed: 10037771
Nat Rev Microbiol. 2017 Apr;15(4):197-204
pubmed: 28216659
Proc Natl Acad Sci U S A. 1958 Jun;44(6):590-4
pubmed: 16590247