title: Exploring the existence of lipid rafts in bacteria.
abstract: An interesting concept in the organization of cellular membranes is the proposed existence of lipid rafts. Membranes of eukaryotic cells organize signal transduction proteins into membrane rafts or lipid rafts that are enriched in particular lipids such as cholesterol and are important for the correct functionality of diverse cellular processes. The assembly of lipid rafts in eukaryotes has been considered a fundamental step during the evolution of cellular complexity, suggesting that bacteria and archaea were organisms too simple to require such a sophisticated organization of their cellular membranes. However, it was recently discovered that bacteria organize many signal transduction, protein secretion, and transport processes in functional membrane microdomains, which are equivalent to the lipid rafts of eukaryotic cells. This review contains the most significant advances during the last 4 years in understanding the structural and biological role of lipid rafts in bacteria. Furthermore, this review shows a detailed description of a number of molecular and genetic approaches related to the discovery of bacterial lipid rafts as well as an overview of the group of tentative lipid-protein and protein-protein interactions that give consistency to these sophisticated signaling platforms. Additional data suggesting that lipid rafts are widely distributed in bacteria are presented in this review. Therefore, we discuss the available techniques and optimized protocols for the purification and analysis of raft-associated proteins in various bacterial species to aid in the study of bacterial lipid rafts in other laboratories that could be interested in this topic. Overall, the discovery of lipid rafts in bacteria reveals a new level of sophistication in signal transduction and membrane organization that was unexpected for bacteria and shows that bacteria are more complex than previously appreciated.
authors: Department of Biology I, University of Munich (LMU), Planegg/Martinsried, Germany marc.bramkamp@lmu.de daniel.lopez@uni-wuerzburg.de.
authors: Marc
authors: M
authors: Bramkamp
authors: Research Center for Infectious Diseases ZINF, University of Würzburg, Würzburg, Germany marc.bramkamp@lmu.de daniel.lopez@uni-wuerzburg.de.
authors: Daniel
authors: D
authors: Lopez
mesh_terms: D001412:Bacillus subtilis / Q000737:chemistry / Q000378:metabolism / Q000648:ultrastructure; D001419:Bacteria / Q000378:metabolism* / Q000648:ultrastructure*; D001426:Bacterial Proteins / Q000302:isolation & purification / Q000378:metabolism; D053898:Biosynthetic Pathways; D002462:Cell Membrane / Q000378:metabolism; D008563:Membrane Lipids / Q000378:metabolism; D021962:Membrane Microdomains / Q000737:chemistry / Q000378:metabolism; D008565:Membrane Proteins / Q000302:isolation & purification / Q000378:metabolism; D008853:Microscopy; D021381:Protein Transport; D015398:Signal Transduction
chemical_list: D001426:Bacterial Proteins; D008563:Membrane Lipids; D008565:Membrane Proteins; C106354:flotillins
references: Cell. 2011 Mar 18;144(6):897-909
references: 21414482
references: Mol Microbiol. 1991 Jan;5(1):173-85
references: 1901616
references: J Nat Prod. 1997 Apr;60(4):397-8
references: 9134748
references: Nat Cell Biol. 2012 Jun;14(6):640-8
references: 22544065
references: Mol Microbiol. 2013 Sep;89(6):1084-98
references: 23869552
references: Mol Microbiol. 2006 Feb;59(4):1216-28
references: 16430695
references: Protein J. 2005 Feb;24(2):125-31
references: 16003954
references: J Bacteriol. 1995 Feb;177(3):861-3
references: 7836330
references: Biochemistry (Mosc). 2005 Feb;70(2):154-8
references: 15807653
references: Nature. 2005 Dec 1;438(7068):578-80
references: 16319876
references: Cell Host Microbe. 2010 Oct 21;8(4):331-42
references: 20951967
references: Proc Natl Acad Sci U S A. 2012 Aug 28;109(35):14236-40
references: 22893685
references: J Biol Chem. 2007 Jul 27;282(30):21573-7
references: 17442674
references: Microbiology. 1997 Mar;143 ( Pt 3):971-8
references: 9084181
references: J Bacteriol. 2009 Aug;191(16):5216-23
references: 19502399
references: J Biophotonics. 2010 Jul;3(7):446-54
references: 20148419
references: Mol Microbiol. 2006 Feb;59(4):1229-38
references: 16430696
references: Geobiology. 2009 Dec;7(5):524-32
references: 19811542
references: Biophys J. 1997 Jun;72(6):2413-29
references: 9168019
references: Int J Mol Sci. 2013 Feb 18;14(2):4050-65
references: 23429192
references: EMBO J. 2011 Dec 14;30(24):4931-41
references: 21964069
references: J Appl Microbiol. 2010 Jun;108(6):1889-902
references: 19878522
references: Science. 1972 Feb 18;175(4023):720-31
references: 4333397
references: Nat Immunol. 2006 Nov;7(11):1139-42
references: 17053798
references: J Bacteriol. 2012 Sep;194(17):4652-61
references: 22753055
references: Science. 2008 Mar 7;319(5868):1391-4
references: 18276850
references: Proc Natl Acad Sci U S A. 2008 May 6;105(18):6725-9
references: 18436644
references: Cell Mol Life Sci. 2006 Feb;63(3):343-57
references: 16389450
references: Genes Dev. 2005 Sep 15;19(18):2236-44
references: 16166384
references: J Mol Evol. 2009 Dec;69(6):657-67
references: 20012272
references: BMC Microbiol. 2011;11:13
references: 21241511
references: Nat Rev Microbiol. 2014 Jan;12(1):9-22
references: 24336182
references: J Biol Chem. 1991 Dec 25;266(36):24596-600
references: 1837025
references: J Bacteriol. 2008 Jun;190(11):3808-16
references: 18375558
references: Biofactors. 1999;10(2-3):99-104
references: 10609869
references: Curr Protoc Immunol. 2002 Nov;Chapter 11:Unit 11.10
references: 18432868
references: Microbiology. 2009 Apr;155(Pt 4):1122-32
references: 19332814
references: FEMS Microbiol Lett. 2005 Feb 1;243(1):59-64
references: 15668001
references: Mol Microbiol. 2013 Sep;89(6):1069-83
references: 23855774
references: J Bacteriol. 1995 Jun;177(12):3601-5
references: 7768874
references: Proc Natl Acad Sci U S A. 2003 Jun 24;100(13):7913-8
references: 12799465
references: J Bacteriol. 1970 Jul;103(1):191-8
references: 5423369
references: Traffic. 2008 Jun;9(6):893-909
references: 18397183
references: Mol Cell Biol. 1999 May;19(5):3435-42
references: 10207067
references: Environ Microbiol. 2007 Sep;9(9):2175-88
references: 17686016
references: Mol Microbiol. 2001 Jul;41(1):59-71
references: 11454200
references: J Bacteriol. 2000 Aug;182(15):4319-27
references: 10894743
references: Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):9879-84
references: 9707569
references: Virol J. 2011;8:479
references: 22023811
references: Trends Microbiol. 2005 Jan;13(1):20-6
references: 15639628
references: Biochem J. 2004 Mar 1;378(Pt 2):509-18
references: 14599293
references: J Mol Evol. 2002 Feb;54(2):235-45
references: 11821916
references: Annu Rev Genet. 1995;29:477-508
references: 8825484
references: J Bacteriol. 2004 Mar;186(5):1475-83
references: 14973018
references: Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11621-6
references: 11572999
references: Mol Microbiol. 2007 Jun;64(6):1419-22
references: 17555431
references: Proc Natl Acad Sci U S A. 2009 Sep 29;106(39):16645-50
references: 19805351
references: BMC Evol Biol. 2009;9:10
references: 19138386
references: Cold Spring Harb Perspect Biol. 2010 Jun;2(6):a003442
references: 20516135
references: J Bacteriol. 2007 Feb;189(3):801-6
references: 17142392
references: Nature. 1959 Dec 12;184(Suppl 24):1891-2
references: 13818963
references: Trends Cell Biol. 2010 Jan;20(1):6-13
references: 19896850
references: Arch Microbiol. 1982 Dec;133(2):100-2
references: 6762170
references: PLoS Biol. 2013;11(5):e1001565
references: 23700385
references: Methods Mol Biol. 2007;398:21-8
references: 18214371
references: Nat Rev Mol Cell Biol. 2010 Oct;11(10):688-99
references: 20861879
references: Mol Membr Biol. 1995 Jan-Mar;12(1):113-9
references: 7767369
references: J Bacteriol. 2011 Dec;193(23):6712-23
references: 21965564
references: Methods Enzymol. 2010;471:229-51
references: 20946851
references: Trends Cell Biol. 2007 Aug;17(8):394-402
references: 17766116
references: Traffic. 2005 Sep;6(9):725-40
references: 16101677
references: FEMS Microbiol Rev. 2009 Jan;33(1):152-63
references: 19054118
references: J Bacteriol. 2012 Mar;194(5):993-1001
references: 22178969
references: Front Plant Sci. 2013 Dec 12;4:503
references: 24376453
references: J Bacteriol. 2012 Mar;194(5):1253-4
references: 22328753
references: FEBS Lett. 1976 Dec 31;72(2):323-6
references: 16386050
references: Mol Microbiol. 2008 Jun;68(5):1315-27
references: 18430139
references: Annu Rev Microbiol. 1987;41:301-33
references: 3120639
references: Nucleic Acids Res. 2012 Jan;40(Database issue):D302-5
references: 22053084
references: Curr Opin Microbiol. 2004 Dec;7(6):579-86
references: 15556029
references: PLoS One. 2014;9(1):e84455
references: 24409299
references: Microbiol Rev. 1984 Sep;48(3):181-98
references: 6387426
references: Science. 2011 May 6;332(6030):680-6
references: 21551057
references: F1000 Biol Rep. 2010;2:31
references: 20606718
references: J Cell Sci. 2005 Mar 15;118(Pt 6):1099-102
references: 15764592
references: Mol Microbiol. 2012 Oct;86(2):457-71
references: 22882210
references: J Neurobiol. 1998 Dec;37(4):502-23
references: 9858255
references: J Cell Sci. 2011 Dec 1;124(Pt 23):3933-40
references: 22194304
references: Biochim Biophys Acta. 2009 Oct;1788(10):2084-91
references: 19371718
references: FEMS Microbiol Lett. 2000 Feb 15;183(2):295-9
references: 10675600
references: Mol Microbiol. 2011 Jun;80(5):1155-68
references: 21477127
references: Annu Rev Microbiol. 2005;59:211-31
references: 15910274
references: Proc Natl Acad Sci U S A. 2011 Nov 8;108(45):E1045-51
references: 21873238
references: Nat Rev Mol Cell Biol. 2008 Feb;9(2):112-24
references: 18216768
references: MBio. 2013;4(6):e00719-13
references: 24222488
references: Environ Microbiol. 2009 May;11(5):1208-23
references: 19128318
references: Appl Environ Microbiol. 2011 Jun;77(12):3905-15
references: 21531832
references: Mol Biol Cell. 2013 Sep;24(18):2765-8
references: 24030510
references: Nature. 1997 Jun 5;387(6633):569-72
references: 9177342
references: Annu Rev Microbiol. 2003;57:203-24
references: 14527277
references: J Bacteriol. 2013 Jun;195(12):2747-54
references: 23564171
references: Mol Microbiol. 2013 Dec;90(6):1201-15
references: 24164455
references: Biochim Biophys Acta. 2011 Jan;1808(1):298-306
references: 20937246
references: Res Microbiol. 2010 Nov;161(9):783-90
references: 20863890
references: Chem Biol. 2014 Nov 20;21(11):1557-63
references: 25308276
references: EMBO J. 1996 Nov 15;15(22):6122-31
references: 8947034
references: Biochem Soc Symp. 2005;(72):109-18
references: 15649135
references: PLoS Pathog. 2013;9(5):e1003353
references: 23696733
references: J Lipid Res. 2002 Jan;43(1):132-40
references: 11792732
references: Structure. 2011 Nov 9;19(11):1543-8
references: 22078554
references: Mol Microbiol. 2006 Sep;61(5):1110-7
references: 16925550
references: Mol Microbiol. 2005 Feb;55(3):739-49
references: 15661000
references: J Antimicrob Chemother. 2008 Apr;61(4):774-85
references: 18263570
references: Eur J Cell Biol. 2007 Sep;86(9):525-32
references: 17482313
references: Prog Lipid Res. 2013 Jul;52(3):249-76
references: 23500459
references: Clin Microbiol Rev. 2010 Jul;23(3):616-87
references: 20610826
references: Proc Natl Acad Sci U S A. 1997 May 27;94(11):5544-9
references: 9159109
references: Mol Microbiol. 2000 Nov;38(3):535-42
references: 11069677
references: Nat Commun. 2014;5:3442
references: 24603761
references: J Biol Chem. 1997 May 23;272(21):13793-802
references: 9153235
references: Development. 1997 Jan;124(2):577-87
references: 9053333
references: Cold Spring Harb Perspect Biol. 2011 Oct;3(10):a004697
references: 21628426
references: FEBS Lett. 2001 Oct 26;507(2):187-90
references: 11684095
references: Clin Microbiol Infect. 2009 Apr;15(4):325-34
references: 19416304
references: J Bacteriol. 2009 Feb;191(3):851-61
references: 19028897
references: Trends Microbiol. 2004 Dec;12(12):569-76
references: 15539117
references: Nat Rev Neurosci. 2007 Feb;8(2):128-40
references: 17195035
references: J Cell Sci. 2004 Dec 1;117(Pt 25):5955-64
references: 15564373
references: J Bacteriol. 2014 Oct;196(19):3386-98
references: 25002539
references: Trends Biochem Sci. 1999 Nov;24(11):425-7
references: 10542406
references: FEMS Microbiol Lett. 2006 Feb;255(2):215-24
references: 16448498
references: J Cell Biol. 2010 Jul 26;190(2):165-75
references: 20643879
references: J Biol Chem. 2012 Mar 2;287(10):7265-78
references: 22232557
references: Genes Dev. 2010 Sep 1;24(17):1893-902
references: 20713508
references: J Lipid Res. 2008 Aug;49(8):1607-20
references: 18077827
references: Nat Rev Mol Cell Biol. 2000 Oct;1(1):31-9
references: 11413487
references: Mol Membr Biol. 2006 Jan-Feb;23(1):41-8
references: 16611579
references: Biochemistry. 1988 Aug 23;27(17):6197-202
references: 3064805
references: Proc Natl Acad Sci U S A. 2010 Feb 2;107(5):2230-4
references: 20080671
references: J Cell Biol. 2006 Sep 11;174(6):851-62
references: 16954349
references: FEMS Microbiol Lett. 2000 Aug 1;189(1):93-5
references: 10913872
references: Biochim Biophys Acta. 2011 Mar;1808(3):634-41
references: 21126508
references: J Biomol NMR. 2008 Sep;42(1):69-76
references: 18696230
references: J Biol Chem. 2005 Sep 16;280(37):32493-8
references: 16020541
references: Biophys J. 2003 Oct;85(4):2406-16
references: 14507704
references: J Cell Biochem. 1988 Jan;36(1):51-8
references: 3277985
references: Exp Cell Res. 2009 Oct 15;315(17):2871-8
references: 19632223
references: Microbiology. 2009 Jun;155(Pt 6):1786-99
references: 19383680
references: J Bacteriol. 1987 May;169(5):2223-30
references: 2437099
references: Cell Signal. 2009 Aug;21(8):1287-97
references: 19318123
references: Acta Biochim Pol. 2012;59(1):109-14
references: 22428142
references: Can J Microbiol. 2001 Jun;47(6):535-40
references: 11467729
references: PLoS Biol. 2011 Apr;9(4):e1001041
references: 21483721
references: ISME J. 2009 Mar;3(3):352-63
references: 19037261
references: J Biol Chem. 2011 Nov 25;286(47):40631-7
references: 21965671
references: Clin Infect Dis. 2001 Oct 15;33(8):1352-7
references: 11565076
references: Science. 2012 Aug 31;337(6098):1047-9
references: 22936764
references: Langmuir. 2013 Jun 25;29(25):7922-30
references: 23713788
references: Nature. 1998 May 7;393(6680):85-8
references: 9590695
references: Science. 2010 Jan 1;327(5961):46-50
references: 20044567
references: J Bacteriol. 2003 Feb;185(3):973-82
references: 12533473
references: Mol Microbiol. 2013 Jun;88(6):1205-17
references: 23651456
references: Curr Protein Pept Sci. 2011 Dec;12(8):725-35
references: 22329548
references: Cell Mol Life Sci. 2005 Oct;62(19-20):2228-40
references: 16091845
references: Acta Crystallogr Sect F Struct Biol Cryst Commun. 2013 Jan 1;69(Pt 1):77-9
references: 23295493
references: FEMS Microbiol Rev. 2010 Mar;34(2):134-49
references: 20030732
references: Mol Microbiol. 2001 Dec;42(5):1199-209
references: 11886552
references: Biochem J. 2007 Apr 15;403(2):313-22
references: 17206938
references: Cold Spring Harb Perspect Biol. 2010 Jul;2(7):a000398
references: 20519345
references: Biol Cell. 2007 Mar;99(3):129-40
references: 17064251
references: Cell. 2003 Nov 14;115(4):377-88
references: 14622593
references: Proc Natl Acad Sci U S A. 2009 Jan 6;106(1):280-5
references: 19114652
references: Cold Spring Harb Perspect Med. 2012 Nov;2(11). pii: a010009. doi: 10.1101/cshperspect.a010009
references: 23125201
references: J Biol Chem. 2002 Dec 13;277(50):48834-41
references: 12370178
references: Proc Natl Acad Sci U S A. 1993 Jan 1;90(1):80-4
references: 8419946
references: Proc Natl Acad Sci U S A. 2010 Dec 21;107(51):22050-4
references: 21131568
references: Proc Natl Acad Sci U S A. 2012 Mar 13;109(11):4104-9
references: 22378651
references: Trends Neurosci. 2002 Aug;25(8):412-7
references: 12127758
references: Mol Microbiol. 2006 Apr;60(2):448-57
references: 16573693
references: J Bacteriol. 2000 Feb;182(4):1172-5
references: 10648548
references: Peptides. 2001 Oct;22(10):1519-27
references: 11587781
references: Nucleic Acids Res. 2002 Jan 1;30(1):62-5
references: 11752255
references: J Neurochem. 2011 Mar;116(5):708-13
references: 21214550
references: J Mol Biol. 2002 Feb 22;316(3):443-57
references: 11866510
references: Genes Dev. 1993 Feb;7(2):283-94
references: 8436298
references: Nat Chem Biol. 2012 Sep;8(9):743-4
references: 22907090