Low membrane fluidity triggers lipid phase separation and protein segregation in living bacteria.
homeoviscous adaptation
lipid domains
lipid phase separation
membrane fluidity
protein partitioning
Journal
The EMBO journal
ISSN: 1460-2075
Titre abrégé: EMBO J
Pays: England
ID NLM: 8208664
Informations de publication
Date de publication:
01 03 2022
01 03 2022
Historique:
revised:
19
12
2021
received:
24
09
2021
accepted:
21
12
2021
pubmed:
18
1
2022
medline:
9
3
2022
entrez:
17
1
2022
Statut:
ppublish
Résumé
All living organisms adapt their membrane lipid composition in response to changes in their environment or diet. These conserved membrane-adaptive processes have been studied extensively. However, key concepts of membrane biology linked to regulation of lipid composition including homeoviscous adaptation maintaining stable levels of membrane fluidity, and gel-fluid phase separation resulting in domain formation, heavily rely upon in vitro studies with model membranes or lipid extracts. Using the bacterial model organisms Escherichia coli and Bacillus subtilis, we now show that inadequate in vivo membrane fluidity interferes with essential complex cellular processes including cytokinesis, envelope expansion, chromosome replication/segregation and maintenance of membrane potential. Furthermore, we demonstrate that very low membrane fluidity is indeed capable of triggering large-scale lipid phase separation and protein segregation in intact, protein-crowded membranes of living cells; a process that coincides with the minimal level of fluidity capable of supporting growth. Importantly, the in vivo lipid phase separation is not associated with a breakdown of the membrane diffusion barrier function, thus explaining why the phase separation process induced by low fluidity is biologically reversible.
Identifiants
pubmed: 35037270
doi: 10.15252/embj.2021109800
pmc: PMC8886542
doi:
Substances chimiques
Membrane Lipids
0
Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e109800Subventions
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/S00257X/1
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/M011186/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/N013840/1
Pays : United Kingdom
Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2022 The Authors. Published under the terms of the CC BY 4.0 license.
Références
Nat Rev Microbiol. 2009 Sep;7(9):642-53
pubmed: 19680248
Proc Natl Acad Sci U S A. 2015 Sep 22;112(38):11971-6
pubmed: 26351677
Appl Environ Microbiol. 1997 Jun;63(6):2421-31
pubmed: 9172364
Eur J Biochem. 1981 Mar 16;115(1):175-81
pubmed: 6785086
Bacteriol Rev. 1977 Jun;41(2):391-418
pubmed: 329832
Biochim Biophys Acta. 2010 May;1798(5):1014-9
pubmed: 20096263
J Phys Chem B. 2019 Jul 11;123(27):5814-5821
pubmed: 31251616
Cold Spring Harb Perspect Biol. 2010 Jul;2(7):a002170
pubmed: 20519344
Biochim Biophys Acta. 1973 Jul 6;311(3):330-48
pubmed: 4729825
J Biol Chem. 2013 Aug 23;288(34):24465-79
pubmed: 23846684
J Bacteriol. 1996 Sep;178(18):5382-7
pubmed: 8808925
Nat Rev Microbiol. 2007 Apr;5(4):316-23
pubmed: 17334387
J Bacteriol. 2004 Oct;186(20):6681-8
pubmed: 15466018
Biosci Rep. 1987 Nov;7(11):823-37
pubmed: 3329533
J Bacteriol. 1997 Mar;179(6):2060-4
pubmed: 9068655
Annu Rev Phys Chem. 2021 Apr 20;72:51-72
pubmed: 33710910
FEBS Lett. 2010 May 3;584(9):1840-7
pubmed: 19837069
Biochim Biophys Acta. 2012 Apr;1818(4):984-94
pubmed: 21884678
Biochim Biophys Acta. 1992 Jun 22;1126(2):119-24
pubmed: 1627613
J Biol Chem. 2013 Sep 6;288(36):25880-25894
pubmed: 23864656
J Bacteriol. 1999 Apr;181(7):2059-66
pubmed: 10094682
Cold Spring Harb Perspect Biol. 2011 Apr 01;3(4):
pubmed: 21441593
Proc Natl Acad Sci U S A. 1999 Dec 7;96(25):14553-8
pubmed: 10588743
Biochim Biophys Acta. 2004 Nov 3;1666(1-2):62-87
pubmed: 15519309
Curr Protoc Mol Biol. 2007 Jul;Chapter 1:1.17.1-1.17.8
pubmed: 18265391
Methods Mol Biol. 2017;1520:159-174
pubmed: 27873252
Proc Natl Acad Sci U S A. 1999 Dec 21;96(26):14819-24
pubmed: 10611296
Biochim Biophys Acta. 2014 Jun;1838(6):1451-66
pubmed: 24189436
J Vis Exp. 2018 Jun 30;(136):
pubmed: 30010642
PLoS One. 2012;7(4):e35205
pubmed: 22514721
J Biochem. 1974 Sep;76(3):553-61
pubmed: 4612031
J Phys Chem Lett. 2017 Sep 7;8(17):4214-4217
pubmed: 28825491
Mol Microbiol. 2010 Jun;76(6):1514-26
pubmed: 20487275
Int J Mass Spectrom. 2009 Jun 1;283(1-3):178-184
pubmed: 20161304
Biophys J. 1990 Jun;57(6):1179-86
pubmed: 2393703
Biochemistry. 2004 Apr 20;43(15):4482-9
pubmed: 15078094
Nucleic Acids Res. 2002 Dec 15;30(24):5517-28
pubmed: 12490720
J Biol Chem. 2009 Dec 11;284(50):34880-8
pubmed: 19854834
Nature. 2014 Jan 16;505(7483):427-31
pubmed: 24362570
Nat Commun. 2020 Mar 12;11(1):1339
pubmed: 32165635
J Phys Chem B. 2011 Dec 15;115(49):14501-6
pubmed: 21988313
Proc Natl Acad Sci U S A. 1974 Feb;71(2):522-5
pubmed: 4360948
Metabolites. 2012 Oct 16;2(4):756-74
pubmed: 24957761
Sci Rep. 2017 Mar 09;7:44332
pubmed: 28276520
Proc Natl Acad Sci U S A. 2011 Jan 25;108(4):1343-8
pubmed: 21205902
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Biochim Biophys Acta. 1999 Jun 9;1419(1):97-104
pubmed: 10366675
Nat Rev Mol Cell Biol. 2018 May;19(5):281-296
pubmed: 29410529
J Exp Zool. 1993 Mar 15;265(4):432-7
pubmed: 8463792
Nat Commun. 2017 Oct 31;8(1):1219
pubmed: 29089556
J Bacteriol. 1962 Dec;84(6):1260-7
pubmed: 16561982
J Biol Chem. 1973 Feb 25;248(4):1188-95
pubmed: 4568811
Science. 2018 Dec 7;362(6419):1186-1189
pubmed: 30361388
Biochemistry. 1987 Jun 30;26(13):4036-44
pubmed: 3651434
Hum Reprod. 2005 Dec;20(12):3385-9
pubmed: 16055458
J Biol Chem. 1996 Mar 22;271(12):6801-9
pubmed: 8636103
Ann N Y Acad Sci. 1967 Jul 28;143(1):115-29
pubmed: 4228218
Front Microbiol. 2015 Aug 05;6:813
pubmed: 26300876
Eur J Biochem. 1998 Jan 15;251(1-2):122-32
pubmed: 9492276
J Biol Chem. 1971 Sep 10;246(17):5264-72
pubmed: 4999353
J Vis Exp. 2011 Jul 28;(53):
pubmed: 21841760
Proc Natl Acad Sci U S A. 1977 Feb;74(2):452-6
pubmed: 322126
Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6640-5
pubmed: 10829079
Biochim Biophys Acta. 1982 Jan 22;684(2):195-9
pubmed: 7055561
Annu Rev Biophys Biomol Struct. 2007;36:107-30
pubmed: 17263662
J Phys Chem B. 2011 Nov 10;115(44):12778-84
pubmed: 21962215
Proc Natl Acad Sci U S A. 2002 Jun 25;99(13):8701-6
pubmed: 12060714
Semin Cell Dev Biol. 2007 Oct;18(5):573-82
pubmed: 17942350
BMC Biol. 2018 Sep 3;16(1):97
pubmed: 30173665
Proc Natl Acad Sci U S A. 2010 Jul 6;107(27):12281-6
pubmed: 20566861
Proc Natl Acad Sci U S A. 2017 Dec 19;114(51):13394-13399
pubmed: 29196526
Annu Rev Biophys. 2010;39:207-26
pubmed: 20192775
Annu Rev Biochem. 2015;84:631-57
pubmed: 25839341
Anal Biochem. 1976 Mar;71(1):209-13
pubmed: 179440
Proc Natl Acad Sci U S A. 2007 Feb 27;104(9):3165-70
pubmed: 17360623
J Am Chem Soc. 2009 Sep 9;131(35):12650-6
pubmed: 19673517
J Bacteriol. 1974 Mar;117(3):971-7
pubmed: 4591962
Q Rev Biophys. 1975 May;8(2):185-235
pubmed: 1103214
Prog Lipid Res. 2013 Jul;52(3):249-76
pubmed: 23500459
Biochim Biophys Acta Biomembr. 2017 Apr;1859(4):509-528
pubmed: 27823927
Annu Rev Physiol. 1995;57:19-42
pubmed: 7778864
EMBO J. 2022 Mar 1;41(5):e109800
pubmed: 35037270
Nat Commun. 2017 Jul 14;8:15976
pubmed: 28706306
Dev Cell. 2012 Nov 13;23(5):886-95
pubmed: 23153485
Proc Natl Acad Sci U S A. 2008 Oct 7;105(40):15376-81
pubmed: 18832162
Curr Opin Cell Biol. 2018 Aug;53:44-51
pubmed: 29787971
J Cell Biol. 2013 Jul 8;202(1):35-44
pubmed: 23836928
Biophys J. 2017 Sep 19;113(6):1212-1222
pubmed: 28552311
J Biol Chem. 1992 Jun 15;267(17):12370-4
pubmed: 1376323
Science. 2010 Jan 1;327(5961):46-50
pubmed: 20044567
Nat Rev Microbiol. 2011 Dec 28;10(2):123-36
pubmed: 22203377
Biophys J. 2010 Feb 17;98(4):552-9
pubmed: 20159151
Cell Metab. 2018 Jan 9;27(1):167-179.e7
pubmed: 29103922
J Phys Chem B. 2018 Jul 12;122(27):6954-6965
pubmed: 29767519
Front Cell Dev Biol. 2016 Apr 13;4:29
pubmed: 27148531
Annu Rev Microbiol. 2017 Sep 8;71:519-538
pubmed: 28697671
J Mol Biol. 2016 Dec 4;428(24 Pt A):4776-4791
pubmed: 27534816
J Bacteriol. 1999 Sep;181(17):5341-9
pubmed: 10464205
Anal Biochem. 1987 Nov 1;166(2):368-79
pubmed: 2449095
Chem Phys Lipids. 1993 Sep;64(1-3):99-116
pubmed: 8242843
Nat Commun. 2020 Feb 6;11(1):756
pubmed: 32029718
Biophys J. 2016 Mar 8;110(5):1139-49
pubmed: 26958890
Bio Protoc. 2018 Oct 20;8(20):e3063
pubmed: 34532528
Nat Commun. 2014 Mar 07;5:3442
pubmed: 24603761
J Bacteriol. 1973 Oct;116(1):285-9
pubmed: 4583215