The P. aeruginosa effector Tse5 forms membrane pores disrupting the membrane potential of intoxicated bacteria.

Pseudomonas aeruginosa / metabolism Membrane Potentials Bacterial Proteins / metabolism Type VI Secretion Systems / genetics

Journal

Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179

Informations de publication

Date de publication:
05 11 2022
Historique:
received: 25 11 2021
accepted: 20 10 2022
pubmed: 6 11 2022
medline: 9 11 2022
entrez: 6 11 2022
Statut: epublish

Résumé

The type VI secretion system (T6SS) of Pseudomonas aeruginosa injects effector proteins into neighbouring competitors and host cells, providing a fitness advantage that allows this opportunistic nosocomial pathogen to persist and prevail during the onset of infections. However, despite the high clinical relevance of P. aeruginosa, the identity and mode of action of most P. aeruginosa T6SS-dependent effectors remain to be discovered. Here, we report the molecular mechanism of Tse5-CT, the toxic auto-proteolytic product of the P. aeruginosa T6SS exported effector Tse5. Our results demonstrate that Tse5-CT is a pore-forming toxin that can transport ions across the membrane, causing membrane depolarisation and bacterial death. The membrane potential regulates a wide range of essential cellular functions; therefore, membrane depolarisation is an efficient strategy to compete with other microorganisms in polymicrobial environments.

Identifiants

DOI: 10.1038/s42003-022-04140-y PMID: 36335275 PMC: PMC9637101
pubmed: 36335275
doi: 10.1038/s42003-022-04140-y
pii: 10.1038/s42003-022-04140-y
pmc: PMC9637101
doi:

Substances chimiques

Bacterial Proteins 0
Type VI Secretion Systems 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1189

Informations de copyright

© 2022. The Author(s).

Références

Mol Microbiol. 2014 Jun;92(5):1092-112
pubmed: 24724564
Biochimie. 2009 Jun;91(6):718-33
pubmed: 19345719
Proc Natl Acad Sci U S A. 2018 Dec 4;115(49):12519-12524
pubmed: 30455305
Nat Commun. 2020 Apr 20;11(1):1865
pubmed: 32313027
Trends Microbiol. 2020 Apr;28(4):304-314
pubmed: 31952908
Biophys J. 2002 Apr;82(4):1985-94
pubmed: 11916856
Cell. 2015 Feb 26;160(5):952-962
pubmed: 25723169
Phys Rev Lett. 2009 Jun 26;102(25):256804
pubmed: 19659110
Proc Natl Acad Sci U S A. 1972 Dec;69(12):3561-6
pubmed: 4509315
Biochim Biophys Acta. 1975 Sep 16;406(1):97-107
pubmed: 1174576
Annu Rev Microbiol. 2020 Sep 8;74:497-520
pubmed: 32680451
Methods Cell Biol. 1991;34:61-75
pubmed: 1943817
Science. 2006 Jun 9;312(5779):1526-30
pubmed: 16763151
Nat Protoc. 2015 Jun;10(6):845-58
pubmed: 25950237
Nat Commun. 2019 May 30;10(1):2382
pubmed: 31147537
J Mol Biol. 2012 Nov 2;423(4):648-59
pubmed: 22858868
Proc Natl Acad Sci U S A. 1982 May;79(9):2827-31
pubmed: 6953432
Proc Natl Acad Sci U S A. 2013 Apr 23;110(17):7032-7
pubmed: 23572593
Nano Lett. 2018 Oct 10;18(10):6604-6610
pubmed: 30178677
Proc Natl Acad Sci U S A. 1987 Mar;84(5):1152-6
pubmed: 2434951
Science. 2012 Aug 17;337(6096):815
pubmed: 22767897
Biochemistry. 1995 Sep 12;34(36):11479-88
pubmed: 7547876
Bioelectrochemistry. 2021 Feb;137:107641
pubmed: 32889489
Cell Host Microbe. 2012 May 17;11(5):538-49
pubmed: 22607806
Biol Direct. 2012 Jun 25;7:18
pubmed: 22731697
Proc Natl Acad Sci U S A. 2020 Dec 15;:
pubmed: 33323487
J Biol Chem. 1994 Apr 29;269(17):12833-9
pubmed: 8175697
Chem Biodivers. 2007 Jun;4(6):1323-37
pubmed: 17589884
Nat Microbiol. 2018 Apr;3(4):440-446
pubmed: 29459733
Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15070-5
pubmed: 18812504
Nature. 1997 Jan 30;385(6615):461-4
pubmed: 9009197
PLoS Pathog. 2016 Jun 28;12(6):e1005735
pubmed: 27352036
J Bacteriol. 1987 Sep;169(9):4379-83
pubmed: 3040692
Elife. 2015 Feb 02;4:
pubmed: 25643398
J Biol Chem. 2013 Oct 18;288(42):30607-30613
pubmed: 24025333
Cell. 2015 Oct 22;163(3):607-19
pubmed: 26456113
Nat Rev Microbiol. 2016 Feb;14(2):77-92
pubmed: 26639780
Nat Rev Microbiol. 2004 Nov;2(11):898-907
pubmed: 15494746
Microbiol Mol Biol Rev. 2007 Mar;71(1):158-229
pubmed: 17347522
Curr Protoc Protein Sci. 2001 May;Appendix 3:Appendix 3F
pubmed: 18429073
Curr Opin Microbiol. 2009 Feb;12(1):11-7
pubmed: 19162533
Cell Host Microbe. 2009 Mar 19;5(3):234-43
pubmed: 19286133
Trends Biochem Sci. 2014 Nov;39(11):510-6
pubmed: 25440714
Environ Microbiol. 2017 Jan;19(1):345-360
pubmed: 27871130
Nature. 1989 Jan 5;337(6202):93-6
pubmed: 2909895
Philos Trans R Soc Lond B Biol Sci. 2015 Oct 5;370(1679):
pubmed: 26370934
Mol Microbiol. 2009 Jun;72(5):1111-25
pubmed: 19400797
J Biol Chem. 1996 Mar 22;271(12):6801-9
pubmed: 8636103
Biochim Biophys Acta. 1999 Dec 15;1462(1-2):109-40
pubmed: 10590305
J Mol Biol. 1999 Jan 29;285(4):1503-13
pubmed: 9917392
Nature. 2013 Sep 26;501(7468):547-50
pubmed: 23913273
Virulence. 2017 Oct 3;8(7):1189-1202
pubmed: 28060574
Mol Microbiol. 2014 May;92(3):529-42
pubmed: 24589350
Proteins. 2008 Mar;70(4):1488-97
pubmed: 17910056
BMC Genomics. 2009 Mar 12;10:104
pubmed: 19284603
Proc Natl Acad Sci U S A. 2007 Sep 25;104(39):15508-13
pubmed: 17873062
PLoS Genet. 2011 Aug;7(8):e1002217
pubmed: 21829394
J Bacteriol. 1986 Oct;168(1):228-36
pubmed: 3531169
J Biol Chem. 2011 Apr 8;286(14):12317-27
pubmed: 21325275
Mol Microbiol. 2004 Feb;51(3):711-20
pubmed: 14731273
Cell. 2013 Feb 14;152(4):884-94
pubmed: 23415234
Structure. 1997 Mar 15;5(3):443-58
pubmed: 9083117
Clin Microbiol Rev. 2012 Jan;25(1):193-213
pubmed: 22232376
Proc Natl Acad Sci U S A. 2008 Nov 18;105(46):17742-7
pubmed: 18988731
J Mol Biol. 2020 Feb 14;432(4):1279-1296
pubmed: 31870850
Cell Host Microbe. 2010 Jan 21;7(1):25-37
pubmed: 20114026
Curr Opin Microbiol. 2008 Feb;11(1):3-8
pubmed: 18289922
Nat Microbiol. 2017 Nov;2(11):1507-1512
pubmed: 28947741
Nat Commun. 2019 Dec 2;10(1):5484
pubmed: 31792213
J Bacteriol. 2010 Jan;192(1):155-68
pubmed: 19880608
Nat Biotechnol. 2006 Jul;24(7):823-31
pubmed: 16823375
J Bacteriol. 1987 Jul;169(7):3350-7
pubmed: 2439491
Science. 2013 Oct 11;342(6155):250-3
pubmed: 24115441
mBio. 2013 Jul 23;4(4):
pubmed: 23882014
Nature. 2015 Jul 30;523(7562):555-60
pubmed: 26200339
Biochim Biophys Acta. 1991 Feb 11;1062(1):94-102
pubmed: 1998715
Protein Expr Purif. 2013 Feb;87(2):129-35
pubmed: 23168094
Phys Rev Lett. 2000 Jul 3;85(1):202-5
pubmed: 10991194
J Biol Chem. 2014 Jun 20;289(25):17872-84
pubmed: 24794869
J Physiol. 1949 Mar 1;108(1):37-77
pubmed: 18128147
Trends Biotechnol. 2006 Aug;24(8):364-71
pubmed: 16820235
Nature. 2013 Aug 15;500(7462):350-353
pubmed: 23925114
Phys Rev Lett. 2010 Dec 31;105(26):260602
pubmed: 21231637
Nature. 2011 Jul 20;475(7356):343-7
pubmed: 21776080
PLoS Biol. 2018 Jan 17;16(1):e2004935
pubmed: 29342145
Microb Cell Fact. 2014 Nov 11;13:159
pubmed: 25384394
Front Cell Dev Biol. 2016 Apr 13;4:29
pubmed: 27148531
Structure. 1998 Jul 15;6(7):863-74
pubmed: 9687368
Trends Microbiol. 2016 Jan;24(1):51-62
pubmed: 26549582
PLoS Genet. 2015 Oct 13;11(10):e1005545
pubmed: 26460929
Methods Mol Biol. 2017;1615:129-142
pubmed: 28667608
EMBO J. 2018 Feb 15;37(4):
pubmed: 29255010
Virology. 2012 Oct 25;432(2):485-94
pubmed: 22832120
Cell Rep. 2017 Dec 26;21(13):3927-3940
pubmed: 29281838
Nanoscale. 2016 Jul 21;8(27):13422-8
pubmed: 27349445
Nat Microbiol. 2021 Sep;6(9):1199-1210
pubmed: 34413503
Biophys J. 2009 Jan;96(1):56-66
pubmed: 19134471
PLoS Pathog. 2013;9(12):e1003752
pubmed: 24348240
Proc Natl Acad Sci U S A. 2006 Jan 3;103(1):171-6
pubmed: 16373506
Biochim Biophys Acta Bioenerg. 2019 Jan;1860(1):22-29
pubmed: 30412693
Microbiology (Reading). 2008 Jun;154(Pt 6):1570-1583
pubmed: 18524912
Cell. 1990 Oct 19;63(2):269-79
pubmed: 2170023
Infect Immun. 2011 Jul;79(7):2941-9
pubmed: 21555399

Auteurs

Amaia González-Magaña (A)

Fundación Biofísica Bizkaia/Biofisika Bizkaia Fundazioa (FBB) and Departamento de Bioquímica y Biología Molecular, Instituto Biofisika (CSIC, UPV/EHU), University of the Basque Country, 48940, Leioa, Spain.

Jon Altuna (J)

Fundación Biofísica Bizkaia/Biofisika Bizkaia Fundazioa (FBB) and Departamento de Bioquímica y Biología Molecular, Instituto Biofisika (CSIC, UPV/EHU), University of the Basque Country, 48940, Leioa, Spain.

María Queralt-Martín (M)

Laboratory of Molecular Biophysics, Department of Physics, University Jaume I, 12071, Castellón, Spain.
ORCID: 0000-0002-0644-6746

Eneko Largo (E)

Fundación Biofísica Bizkaia/Biofisika Bizkaia Fundazioa (FBB) and Departamento de Bioquímica y Biología Molecular, Instituto Biofisika (CSIC, UPV/EHU), University of the Basque Country, 48940, Leioa, Spain.
Departamento de Inmunología, Microbiología y Parasitología, University of the Basque Country, 48940, Leioa, Spain.
ORCID: 0000-0003-4400-3521

Carmen Velázquez (C)

Fundación Biofísica Bizkaia/Biofisika Bizkaia Fundazioa (FBB) and Departamento de Bioquímica y Biología Molecular, Instituto Biofisika (CSIC, UPV/EHU), University of the Basque Country, 48940, Leioa, Spain.

Itxaso Montánchez (I)

Departamento de Inmunología, Microbiología y Parasitología, University of the Basque Country, 48940, Leioa, Spain.

Patricia Bernal (P)

Departamento de Microbiología, Facultad de Biología, Universidad de Sevilla, 41012, Sevilla, Spain.
ORCID: 0000-0002-6228-0496

Antonio Alcaraz (A)

Laboratory of Molecular Biophysics, Department of Physics, University Jaume I, 12071, Castellón, Spain.
ORCID: 0000-0002-7830-3189

David Albesa-Jové (D)

Fundación Biofísica Bizkaia/Biofisika Bizkaia Fundazioa (FBB) and Departamento de Bioquímica y Biología Molecular, Instituto Biofisika (CSIC, UPV/EHU), University of the Basque Country, 48940, Leioa, Spain. david.albesa@ehu.eus.
Ikerbasque, Basque Foundation for Science, 48013, Bilbao, Spain. david.albesa@ehu.eus.
ORCID: 0000-0003-2904-8203

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Classifications MeSH

Recherchemedicale.com › Bactéries › Proteobacteria › Gammaproteobacteria › Pseudomonadaceae › Pseudomonas › Pseudomonas aeruginosa › The P. aeruginosa effector Tse5 forms membrane...
Recherchemedicale.com › Phénomènes physiologiques de l'appareil locomoteur et du système nerveux › Phénomènes physiologiques du système nerveux › Potentiels de membrane › The P. aeruginosa effector Tse5 forms membrane...
Recherchemedicale.com › Acides aminés, peptides et protéines › Protéines › Protéines bactériennes › The P. aeruginosa effector Tse5 forms membrane...
Recherchemedicale.com › Structures macromoléculaires › Complexes multiprotéiques › Systèmes de translocation des protéines › Systèmes bactériens de sécrétion › Systèmes de sécrétion de type VI › The P. aeruginosa effector Tse5 forms membrane...