Acinetobacter type VI secretion system comprises a non-canonical membrane complex.


Journal

PLoS pathogens
ISSN: 1553-7374
Titre abrégé: PLoS Pathog
Pays: United States
ID NLM: 101238921

Informations de publication

Date de publication:
Sep 2023
Historique:
received: 13 04 2023
accepted: 14 09 2023
revised: 10 10 2023
pubmed: 28 9 2023
medline: 28 9 2023
entrez: 28 9 2023
Statut: epublish

Résumé

A. baumannii can rapidly acquire new resistance mechanisms and persist on abiotic surface, enabling the colonization of asymptomatic human host. In Acinetobacter the type VI secretion system (T6SS) is involved in twitching, surface motility and is used for interbacterial competition allowing the bacteria to uptake DNA. A. baumannii possesses a T6SS that has been well studied for its regulation and specific activity, but little is known concerning its assembly and architecture. The T6SS nanomachine is built from three architectural sub-complexes. Unlike the baseplate (BP) and the tail-tube complex (TTC), which are inherited from bacteriophages, the membrane complex (MC) originates from bacteria. The MC is the most external part of the T6SS and, as such, is subjected to evolution and adaptation. One unanswered question on the MC is how such a gigantesque molecular edifice is inserted and crosses the bacterial cell envelope. The A. baumannii MC lacks an essential component, the TssJ lipoprotein, which anchors the MC to the outer membrane. In this work, we studied how A. baumannii compensates the absence of a TssJ. We have characterized for the first time the A. baumannii's specific T6SS MC, its unique characteristic, its membrane localization, and assembly dynamics. We also defined its composition, demonstrating that its biogenesis employs three Acinetobacter-specific envelope-associated proteins that define an intricate network leading to the assembly of a five-proteins membrane super-complex. Our data suggest that A. baumannii has divided the function of TssJ by (1) co-opting a new protein TsmK that stabilizes the MC and by (2) evolving a new domain in TssM for homo-oligomerization, a prerequisite to build the T6SS channel. We believe that the atypical species-specific features we report in this study will have profound implication in our understanding of the assembly and evolutionary diversity of different T6SSs, that warrants future investigation.

Identifiants

pubmed: 37769028
doi: 10.1371/journal.ppat.1011687
pii: PPATHOGENS-D-23-00593
pmc: PMC10564176
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1011687

Informations de copyright

Copyright: © 2023 Kandolo et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

The authors declare no conflict of interest.

Références

Microbiology (Reading). 2007 Aug;153(Pt 8):2689-2699
pubmed: 17660433
Nat Microbiol. 2018 Nov;3(11):1304-1313
pubmed: 30275513
Mol Microbiol. 2018 Feb;107(4):455-471
pubmed: 29235173
mBio. 2016 Oct 11;7(5):
pubmed: 27729508
J Biol Chem. 2020 May 22;295(21):7501-7515
pubmed: 32317281
Methods Mol Biol. 2020;2112:29-42
pubmed: 32006276
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Proc Natl Acad Sci U S A. 2006 Jan 31;103(5):1528-33
pubmed: 16432199
PLoS One. 2013;8(3):e59388
pubmed: 23527179
Nucleic Acids Res. 2005 Apr 22;33(7):2302-9
pubmed: 15849316
BMC Bioinformatics. 2009 Dec 15;10:421
pubmed: 20003500
EMBO J. 2022 Jul 4;41(13):e108595
pubmed: 35634969
Virulence. 2021 Dec;12(1):2201-2213
pubmed: 34515614
Bioinformatics. 2006 Jul 1;22(13):1658-9
pubmed: 16731699
Bioinformatics. 2015 Mar 15;31(6):926-32
pubmed: 25398609
Nature. 2006 Nov 9;444(7116):226-9
pubmed: 17086202
Nucleic Acids Res. 2002 Jul 15;30(14):3059-66
pubmed: 12136088
Cell Rep. 2019 Nov 5;29(6):1633-1644.e4
pubmed: 31693901
EMBO Rep. 2017 Jan;18(1):138-149
pubmed: 27920034
J Biol Chem. 2014 Nov 21;289(47):33032-43
pubmed: 25305017
Proc Natl Acad Sci U S A. 2015 Oct 13;112(41):12693-8
pubmed: 26420866
PLoS Pathog. 2011 Nov;7(11):e1002386
pubmed: 22102820
Bioinformatics. 2003 Jan 22;19(2):311-2
pubmed: 12538265
PLoS Biol. 2022 Apr 7;20(4):e3001608
pubmed: 35389980
Science. 2012 Aug 17;337(6096):815
pubmed: 22767897
Virulence. 2010 Nov-Dec;1(6):535-40
pubmed: 21178498
Microbiol Mol Biol Rev. 2011 Sep;75(3):423-33, first page of table of contents
pubmed: 21885679
Nat Methods. 2022 Jun;19(6):679-682
pubmed: 35637307
Nature. 2009 Dec 24;462(7276):1011-5
pubmed: 19946264
EMBO J. 2019 May 15;38(10):
pubmed: 30877094
Proc Natl Acad Sci U S A. 2020 Jan 21;117(3):1496-1503
pubmed: 31896580
Nature. 2021 Aug;596(7873):583-589
pubmed: 34265844
EMBO Rep. 2017 Jul;18(7):1090-1099
pubmed: 28487352
Elife. 2017 Nov 01;6:
pubmed: 29091031
PLoS One. 2013;8(1):e55142
pubmed: 23365692
Biochim Biophys Acta. 2014 Aug;1843(8):1664-73
pubmed: 24681160
Nat Microbiol. 2016 Jun 20;1(7):16077
pubmed: 27572972
Protein Sci. 2021 Jan;30(1):70-82
pubmed: 32881101
Nat Methods. 2022 Dec;19(12):1634-1641
pubmed: 36344832
Trends Microbiol. 2020 May;28(5):372-386
pubmed: 32298615
Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6640-5
pubmed: 10829079
Proc Natl Acad Sci U S A. 2021 Feb 16;118(7):
pubmed: 33558227
J Bacteriol. 2020 Aug 10;202(17):
pubmed: 32571965
Nat Methods. 2007 Mar;4(3):251-6
pubmed: 17293868
mBio. 2021 Aug 31;12(4):e0134821
pubmed: 34372705
Microbiol Spectr. 2019 Jul;7(4):
pubmed: 31298206
Genome Res. 2004 Jun;14(6):1188-90
pubmed: 15173120
Nat Methods. 2021 Jan;18(1):100-106
pubmed: 33318659
Nat Microbiol. 2018 Dec;3(12):1404-1416
pubmed: 30323254
Proc Natl Acad Sci U S A. 2019 Nov 12;116(46):23292-23298
pubmed: 31659021
Curr Opin Microbiol. 2008 Feb;11(1):3-8
pubmed: 18289922
Nature. 2012 Feb 26;483(7388):182-6
pubmed: 22367545
Bioinformatics. 2009 May 1;25(9):1189-91
pubmed: 19151095
Nature. 2015 Jul 30;523(7562):555-60
pubmed: 26200339
Sci Rep. 2019 Jul 1;9(1):9438
pubmed: 31263148
Front Microbiol. 2019 Oct 30;10:2440
pubmed: 31736890
J Mol Biol. 2001 Jan 19;305(3):567-80
pubmed: 11152613
Cell Rep. 2015 Sep 29;12(12):2131-42
pubmed: 26387948
Environ Microbiol. 2013 Feb;15(2):471-86
pubmed: 22765374
Proc Natl Acad Sci U S A. 2015 Jul 28;112(30):9442-7
pubmed: 26170289
mBio. 2020 Jan 14;11(1):
pubmed: 31937641
mBio. 2022 Apr 26;13(2):e0308521
pubmed: 35404117
Nat Protoc. 2012 Jul 19;7(8):1511-22
pubmed: 22814390
Curr Opin Struct Biol. 2018 Apr;49:77-84
pubmed: 29414515
Appl Environ Microbiol. 2012 Aug;78(15):5440-3
pubmed: 22610439
Cell Rep. 2017 Dec 26;21(13):3927-3940
pubmed: 29281838
Proc Natl Acad Sci U S A. 2021 Oct 5;118(40):
pubmed: 34588306
Elife. 2021 Sep 09;10:
pubmed: 34498586
Proc Natl Acad Sci U S A. 2019 Jan 22;116(4):1378-1383
pubmed: 30626645

Auteurs

Ona Kandolo (O)

Laboratoire d'Ingénierie des Systèmes Macromoléculaires (LISM), Institut de Microbiologie, Bioénergies and Biotechnologie (IM2B), Aix-Marseille Université, Centre National de la Recherche Scientifique (CNRS)-UMR 7255, Marseille, France.

Yassine Cherrak (Y)

Laboratoire d'Ingénierie des Systèmes Macromoléculaires (LISM), Institut de Microbiologie, Bioénergies and Biotechnologie (IM2B), Aix-Marseille Université, Centre National de la Recherche Scientifique (CNRS)-UMR 7255, Marseille, France.

Isaac Filella-Merce (I)

Institut Pasteur, Structural Bioinformatics Unit, Department of Structural Biology and Chemistry, Paris, France.
Sorbonne Université, Collège doctoral, Paris, France.

Hugo Le Guenno (H)

Microscopy Core Facility, Aix Marseille Univ, CNRS, Institut de Microbiologie de la Méditerranée, Marseille Cedex 20, France.

Artemis Kosta (A)

Microscopy Core Facility, Aix Marseille Univ, CNRS, Institut de Microbiologie de la Méditerranée, Marseille Cedex 20, France.

Leon Espinosa (L)

Laboratoire de Chimie Bactérienne (LCB), Institut de Microbiologie, Bioénergies and Biotechnologie (IM2B), Aix-Marseille Université, Centre National de la Recherche Scientifique, Marseille, France.

Pierre Santucci (P)

Laboratoire d'Ingénierie des Systèmes Macromoléculaires (LISM), Institut de Microbiologie, Bioénergies and Biotechnologie (IM2B), Aix-Marseille Université, Centre National de la Recherche Scientifique (CNRS)-UMR 7255, Marseille, France.

Christophe Verthuy (C)

Proteomic Core Facility IMM, Marseille Protéomique (MaP), Aix Marseille Univ, Marseille Cedex 20, France.

Régine Lebrun (R)

Proteomic Core Facility IMM, Marseille Protéomique (MaP), Aix Marseille Univ, Marseille Cedex 20, France.

Michael Nilges (M)

Institut Pasteur, Structural Bioinformatics Unit, Department of Structural Biology and Chemistry, Paris, France.

Riccardo Pellarin (R)

Institut Pasteur, Structural Bioinformatics Unit, Department of Structural Biology and Chemistry, Paris, France.

Eric Durand (E)

Laboratoire d'Ingénierie des Systèmes Macromoléculaires (LISM), Institut de Microbiologie, Bioénergies and Biotechnologie (IM2B), Aix-Marseille Université, Centre National de la Recherche Scientifique (CNRS)-UMR 7255, Marseille, France.
Laboratoire d'Ingénierie des Systèmes Macromoléculaires (LISM), Institut de Microbiologie, Bioénergies and Biotechnologie (IM2B), Aix-Marseille Université, Institut National de la Santé et de la Recherche Médicale (INSERM), Marseille, France.

Classifications MeSH