Entropy-driven translocation of disordered proteins through the Gram-positive bacterial cell wall.


Journal

Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869

Informations de publication

Date de publication:
08 2021
Historique:
received: 17 12 2020
accepted: 28 06 2021
entrez: 30 7 2021
pubmed: 31 7 2021
medline: 18 9 2021
Statut: ppublish

Résumé

In Gram-positive bacteria, a thick cross-linked cell wall separates the membrane from the extracellular space. Some surface-exposed proteins, such as the Listeria monocytogenes actin nucleation-promoting factor ActA, remain associated with the bacterial membrane but somehow thread through tens of nanometres of cell wall to expose their amino terminus to the exterior. Here, we report that entropy enables the translocation of disordered transmembrane proteins through the Gram-positive cell wall. We build a physical model, which predicts that the entropic constraint imposed by a thin periplasm is sufficient to drive the translocation of an intrinsically disordered protein such as ActA across a porous barrier similar to a peptidoglycan cell wall. We experimentally validate our model and show that ActA translocation depends on the cell-envelope dimensions and disordered-protein length, and that translocation is reversible. We also show that disordered regions of eukaryotic proteins can translocate Gram-positive cell walls via entropy. We propose that entropic forces are sufficient to drive the translocation of specific proteins to the outer surface.

Identifiants

pubmed: 34326523
doi: 10.1038/s41564-021-00942-8
pii: 10.1038/s41564-021-00942-8
pmc: PMC10265014
mid: NIHMS1763494
doi:

Substances chimiques

Bacterial Proteins 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

1055-1065

Subventions

Organisme : NCCIH NIH HHS
ID : R01 AT001006
Pays : United States
Organisme : NCCIH NIH HHS
ID : R01 AT001028
Pays : United States
Organisme : Howard Hughes Medical Institute
Pays : United States
Organisme : NIAID NIH HHS
ID : R37 AI036929
Pays : United States
Organisme : NCCIH NIH HHS
ID : R21 AT001025
Pays : United States
Organisme : NCRR NIH HHS
ID : S10 RR026780
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2021. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Phys Rev E Stat Nonlin Soft Matter Phys. 2009 Aug;80(2 Pt 1):021907
pubmed: 19792151
Phys Rev E. 2016 Nov;94(5-1):052102
pubmed: 27967042
J Bacteriol. 2003 Nov;185(21):6295-307
pubmed: 14563864
Phys Rev Lett. 2001 Apr 2;86(14):3188-91
pubmed: 11290139
Bioinformatics. 2007 Jan 1;23(1):127-8
pubmed: 17050570
Cell. 2006 Feb 24;124(4):715-27
pubmed: 16497583
Mol Microbiol. 2012 May;84(3):405-13
pubmed: 22471582
J Mol Biol. 2001 Jan 19;305(3):567-80
pubmed: 11152613
Infect Immun. 1995 Jul;63(7):2729-37
pubmed: 7790091
J Bacteriol. 2002 Aug;184(15):4177-86
pubmed: 12107135
BMC Biol. 2017 Feb 21;15(1):17
pubmed: 28222723
J Bacteriol. 1963 Sep;86:414-28
pubmed: 14066417
Philos Trans A Math Phys Eng Sci. 2003 Mar 15;361(1804):539-56
pubmed: 12662453
Phys Rev Lett. 2007 Nov 30;99(22):228106
pubmed: 18233335
Nature. 1970 Aug 15;227(5259):680-5
pubmed: 5432063
Cold Spring Harb Perspect Biol. 2010 May;2(5):a000414
pubmed: 20452953
Mol Microbiol. 2012 Jan;83(1):10-3
pubmed: 22126136
Mol Microbiol. 2002 Apr;44(2):335-49
pubmed: 11972774
Mol Cell Proteomics. 2010 Oct;9(10):2205-24
pubmed: 20368288
Plasmid. 2005 Nov;54(3):241-8
pubmed: 16005967
J Bacteriol. 2006 Sep;188(18):6652-60
pubmed: 16952957
J Cell Biol. 1989 Oct;109(4 Pt 1):1597-608
pubmed: 2507553
J Mol Biol. 2004 Jul 16;340(4):783-95
pubmed: 15223320
Philos Trans R Soc Lond B Biol Sci. 2012 Apr 19;367(1592):1123-39
pubmed: 22411983
Phys Rev Lett. 1996 Jul 22;77(4):783-786
pubmed: 10062901
Res Microbiol. 1996 Jun;147(5):371-84
pubmed: 8763623
Cell. 1998 Dec 11;95(6):741-8
pubmed: 9865692
Mol Microbiol. 1990 Sep;4(9):1603-5
pubmed: 2287281
Annu Rev Biochem. 2008;77:643-67
pubmed: 18078384
J Bacteriol. 2007 Jun;189(12):4473-84
pubmed: 17416657
J Bacteriol. 1997 Nov;179(22):7174-80
pubmed: 9371468
Mol Gen Genet. 1995 Jul 22;248(1):114-20
pubmed: 7651322
Infect Immun. 2010 Nov;78(11):4944-57
pubmed: 20823208
Mol Microbiol. 1995 Nov;18(3):413-23
pubmed: 8748026
J Ultrastruct Res. 1963 Oct;59:187-97
pubmed: 14072875
Science. 2013 Jun 28;340(6140):1570-4
pubmed: 23812713
FEMS Microbiol Lett. 1995 Oct 1;132(1-2):181-2
pubmed: 7590161
Genes Dev. 2006 Dec 1;20(23):3283-95
pubmed: 17158746
BMC Bioinformatics. 2011 Mar 02;12:66
pubmed: 21366926
Microbiol Mol Biol Rev. 1997 Jun;61(2):136-69
pubmed: 9184008
Cell. 2014 Jun 5;157(6):1416-1429
pubmed: 24906156
J Bacteriol. 1991 Aug;173(16):4952-8
pubmed: 1907264
J Biol Chem. 2008 Aug 29;283(35):23852-62
pubmed: 18577520
Science. 2012 Nov 30;338(6111):1214-7
pubmed: 23138981
Phys Rev Lett. 2006 Jun 16;96(23):238104
pubmed: 16803411
Methods Enzymol. 2014;541:3-10
pubmed: 24674058
Mol Microbiol. 2006 Feb;59(4):1262-79
pubmed: 16430699
BMC Bioinformatics. 2006 Apr 17;7:208
pubmed: 16618368
Cell. 1992 Jul 24;70(2):267-81
pubmed: 1638631
Cell. 1992 Feb 7;68(3):521-31
pubmed: 1739966
J Bacteriol. 1996 Feb;178(3):768-73
pubmed: 8550511
Science. 1998 Jul 3;281(5373):105-8
pubmed: 9651243
EMBO J. 1993 Dec;12(12):4803-11
pubmed: 8223489
EMBO J. 2008 Oct 22;27(20):2656-68
pubmed: 18800056
Mol Microbiol. 2008 Dec;70(6):1307-22
pubmed: 19019149
Mol Microbiol. 2005 Apr;56(1):240-51
pubmed: 15773993
J Biol Chem. 2002 Jan 4;277(1):243-50
pubmed: 11684686
Mol Microbiol. 1995 Sep;17(5):945-51
pubmed: 8596443
J Bacteriol. 2006 Feb;188(3):1011-21
pubmed: 16428405

Auteurs

David K Halladin (DK)

Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA, USA.
Department of Biochemistry and Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, CA, USA.

Fabian E Ortega (FE)

Department of Biochemistry and Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, CA, USA.

Katharine M Ng (KM)

Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA, USA.
Department of Bioengineering, Stanford University, Stanford, CA, USA.

Matthew J Footer (MJ)

Department of Biochemistry and Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, CA, USA.
Department of Biology and Howard Hughes Medical Institute, University of Washington, Seattle, WA, USA.

Nenad S Mitić (NS)

Faculty of Mathematics, University of Belgrade, Belgrade, Serbia.

Saša N Malkov (SN)

Faculty of Mathematics, University of Belgrade, Belgrade, Serbia.

Ajay Gopinathan (A)

Department of Physics, University of California, Merced, CA, USA.

Kerwyn Casey Huang (KC)

Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA, USA. kchuang@stanford.edu.
Department of Bioengineering, Stanford University, Stanford, CA, USA. kchuang@stanford.edu.
Chan Zuckerberg Biohub, San Francisco, CA, USA. kchuang@stanford.edu.

Julie A Theriot (JA)

Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA, USA. jtheriot@uw.edu.
Department of Biochemistry and Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, CA, USA. jtheriot@uw.edu.
Department of Biology and Howard Hughes Medical Institute, University of Washington, Seattle, WA, USA. jtheriot@uw.edu.

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