Effectiveness of Pseudomonas aeruginosa type VI secretion system relies on toxin potency and type IV pili-dependent interaction.
Journal
PLoS pathogens
ISSN: 1553-7374
Titre abrégé: PLoS Pathog
Pays: United States
ID NLM: 101238921
Informations de publication
Date de publication:
05 2023
05 2023
Historique:
received:
30
11
2022
accepted:
17
05
2023
revised:
20
06
2023
medline:
22
6
2023
pubmed:
30
5
2023
entrez:
30
5
2023
Statut:
epublish
Résumé
The type VI secretion system (T6SS) is an antibacterial weapon that is used by numerous Gram-negative bacteria to gain competitive advantage by injecting toxins into adjacent prey cells. Predicting the outcome of a T6SS-dependent competition is not only reliant on presence-absence of the system but instead involves a multiplicity of factors. Pseudomonas aeruginosa possesses 3 distinct T6SSs and a set of more than 20 toxic effectors with diverse functions including disruption of cell wall integrity, degradation of nucleic acids or metabolic impairment. We generated a comprehensive collection of mutants with various degrees of T6SS activity and/or sensitivity to each individual T6SS toxin. By imaging whole mixed bacterial macrocolonies, we then investigated how these P. aeruginosa strains gain a competitive edge in multiple attacker/prey combinations. We observed that the potency of single T6SS toxin varies significantly from one another as measured by monitoring the community structure, with some toxins acting better in synergy or requiring a higher payload. Remarkably the degree of intermixing between preys and attackers is also key to the competition outcome and is driven by the frequency of contact as well as the ability of the prey to move away from the attacker using type IV pili-dependent twitching motility. Finally, we implemented a computational model to better understand how changes in T6SS firing behaviours or cell-cell contacts lead to population level competitive advantages, thus providing conceptual insight applicable to all types of contact-based competition.
Identifiants
pubmed: 37253075
doi: 10.1371/journal.ppat.1011428
pii: PPATHOGENS-D-22-02073
pmc: PMC10281587
doi:
Substances chimiques
Type VI Secretion Systems
0
Bacterial Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1011428Subventions
Organisme : Medical Research Council
ID : MR/S02316X/1
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : 2133361
Pays : United Kingdom
Informations de copyright
Copyright: © 2023 Rudzite 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 have declared that no competing interests exist.
Références
Infect Immun. 2001 Sep;69(9):5794-804
pubmed: 11500457
Environ Microbiol. 2011 Jul;13(7):1666-81
pubmed: 21554516
Mol Cell. 2022 Sep 15;82(18):3484-3498.e11
pubmed: 36070765
Acta Crystallogr D Biol Crystallogr. 2014 Aug;70(Pt 8):2175-85
pubmed: 25084336
Proc Natl Acad Sci U S A. 2018 Dec 4;115(49):12519-12524
pubmed: 30455305
Curr Opin Gastroenterol. 2008 Jan;24(1):4-10
pubmed: 18043225
Mol Cell. 2013 Sep 12;51(5):584-93
pubmed: 23954347
Nat Rev Microbiol. 2006 Aug;4(8):597-607
pubmed: 16845430
Annu Rev Microbiol. 2022 Sep 8;76:413-433
pubmed: 35655342
mBio. 2021 Jun 29;12(3):e0026221
pubmed: 34061601
RNA Biol. 2021 Dec;18(12):2401-2416
pubmed: 33866926
Annu Rev Microbiol. 2012;66:493-520
pubmed: 22746331
EMBO J. 2019 Sep 16;38(18):e100825
pubmed: 31403721
Annu Rev Microbiol. 2002;56:187-209
pubmed: 12142477
J Cell Sci. 2019 Apr 3;132(7):
pubmed: 30944157
Proc Natl Acad Sci U S A. 2014 Dec 16;111(50):18013-8
pubmed: 25468980
Microbiome. 2018 Apr 25;6(1):78
pubmed: 29695294
Nat Microbiol. 2018 Aug;3(8):920-931
pubmed: 30038307
Science. 2006 Jun 9;312(5779):1526-30
pubmed: 16763151
Curr Opin Microbiol. 2018 Feb;41:15-20
pubmed: 29166621
Cell Host Microbe. 2014 Jan 15;15(1):9-21
pubmed: 24332978
Mol Microbiol. 2009 May;72(3):612-32
pubmed: 19426209
Nucleic Acids Res. 2018 Jul 27;46(13):6823-6840
pubmed: 29718466
Sci Rep. 2017 Sep 22;7(1):12151
pubmed: 28939833
FEMS Microbiol Lett. 1999 May 1;174(1):9-17
pubmed: 10234817
Dev Biol. 2005 Feb 1;278(1):255-63
pubmed: 15649477
Front Mol Biosci. 2022 Apr 26;9:866854
pubmed: 35558562
Anim Nutr. 2022 Mar 24;9:335-344
pubmed: 35600541
J Bacteriol. 1990 Nov;172(11):6557-67
pubmed: 2172216
Nat Microbiol. 2018 May;3(5):632-640
pubmed: 29632369
Curr Biol. 2019 Jun 3;29(11):R521-R537
pubmed: 31163166
ISME J. 2022 Jun;16(6):1512-1522
pubmed: 35121821
Proc Natl Acad Sci U S A. 2014 Jun 24;111(25):9271-6
pubmed: 24927539
Trends Microbiol. 2015 Dec;23(12):775-788
pubmed: 26497940
Annu Rev Phytopathol. 2022 Aug 26;60:337-356
pubmed: 35584884
Res Microbiol. 2001 Apr-May;152(3-4):311-21
pubmed: 11421278
mBio. 2015 Jun 02;6(3):e00712
pubmed: 26037124
Microbiol Spectr. 2019 Mar;7(2):
pubmed: 30825301
Sci Adv. 2018 Nov 21;4(11):eaau0695
pubmed: 30474057
Nat Microbiol. 2018 Apr;3(4):440-446
pubmed: 29459733
Front Microbiol. 2018 Oct 29;9:2578
pubmed: 30420847
J Am Chem Soc. 2013 Apr 3;135(13):4950-3
pubmed: 23510438
Sci Rep. 2017 Mar 22;7:45133
pubmed: 28327641
Nat Commun. 2015 Mar 06;6:6453
pubmed: 25743609
ISME J. 2017 Sep;11(9):2112-2123
pubmed: 28534878
Cell. 2015 Oct 22;163(3):607-19
pubmed: 26456113
Microbiol Mol Biol Rev. 2012 Mar;76(1):46-65
pubmed: 22390972
Nat Commun. 2020 Oct 26;11(1):5395
pubmed: 33106492
Nat Microbiol. 2021 Feb;6(2):151-156
pubmed: 33398098
Proc Natl Acad Sci U S A. 2017 Jul 18;114(29):7707-7712
pubmed: 28673999
Structure. 2016 Feb 2;24(2):277-84
pubmed: 26749446
Microbiol Mol Biol Rev. 2007 Mar;71(1):158-229
pubmed: 17347522
Proc Natl Acad Sci U S A. 2018 Jul 17;115(29):7593-7598
pubmed: 29967163
Nucleic Acids Res. 2022 Jan 11;50(1):227-243
pubmed: 34928327
Curr Opin Microbiol. 2016 Feb;29:81-93
pubmed: 26722980
Microbiology (Reading). 2019 Nov;165(11):1203-1218
pubmed: 31380737
PLoS Pathog. 2009 Nov;5(11):e1000668
pubmed: 19936057
Philos Trans R Soc Lond B Biol Sci. 2015 Oct 5;370(1679):
pubmed: 26370934
mBio. 2017 Mar 28;8(2):
pubmed: 28351921
Science. 2005 Aug 19;309(5738):1245-8
pubmed: 16109881
Environ Microbiol. 2011 Dec;13(12):3128-38
pubmed: 21955777
Phys Rev Lett. 1992 Sep 28;69(13):2013-2016
pubmed: 10046374
Nature. 2019 Nov;575(7784):674-678
pubmed: 31695193
FEMS Microbiol Rev. 2013 May;37(3):384-406
pubmed: 23480449
Mol Microbiol. 2014 May;92(3):529-42
pubmed: 24589350
Nat Commun. 2021 Oct 1;12(1):5751
pubmed: 34599171
FEBS J. 2021 Oct;288(19):5755-5767
pubmed: 33838074
Mol Microbiol. 2016 Mar;99(6):1099-118
pubmed: 26714038
Proc Natl Acad Sci U S A. 2021 Feb 16;118(7):
pubmed: 33558227
Proc Natl Acad Sci U S A. 2011 Jun 28;108 Suppl 2:10839-46
pubmed: 21690380
Nature. 2019 Nov;575(7781):224-228
pubmed: 31666699
J Biol Chem. 2011 Apr 8;286(14):12317-27
pubmed: 21325275
Microbiology (Reading). 2005 Mar;151(Pt 3):985-997
pubmed: 15758243
Proc Natl Acad Sci U S A. 2014 Apr 1;111(13):4964-9
pubmed: 24639530
Cell. 2013 Feb 14;152(4):884-94
pubmed: 23415234
Cell Rep. 2019 Oct 1;29(1):187-201.e7
pubmed: 31577948
FEMS Microbiol Lett. 2017 Aug 1;364(14):
pubmed: 28854668
Cell Host Microbe. 2010 Jan 21;7(1):25-37
pubmed: 20114026
Nature. 2013 Apr 25;496(7446):508-12
pubmed: 23552891
Nature. 2012 Feb 26;483(7388):182-6
pubmed: 22367545
Mol Microbiol. 2020 Aug;114(2):308-321
pubmed: 32279364
Cell Host Microbe. 2017 Jun 14;21(6):769-776.e3
pubmed: 28618272
Sci Rep. 2019 Sep 6;9(1):12859
pubmed: 31492943
Front Microbiol. 2019 Jun 05;10:1218
pubmed: 31231326
Proc Natl Acad Sci U S A. 2010 Mar 2;107(9):4365-70
pubmed: 20150509
J Bacteriol. 2014 Feb;196(4):800-10
pubmed: 24317402
Microbiology (Reading). 2022 Apr;168(4):
pubmed: 35467500
Elife. 2015 Sep 24;4:
pubmed: 26402455
Mol Microbiol. 2001 Jan;39(2):291-303
pubmed: 11136451
Curr Biol. 2019 Jun 3;29(11):R545-R550
pubmed: 31163168
mBio. 2021 Jan 12;12(1):
pubmed: 33436426
Microbiol Res. 2021 Apr;245:126690
pubmed: 33460987
Mol Microbiol. 2010 Jun;76(6):1427-43
pubmed: 20398205
Dev Cell. 2004 Nov;7(5):745-54
pubmed: 15525535
Front Microbiol. 2019 Jul 31;10:1718
pubmed: 31417515
PLoS Pathog. 2019 Dec 2;15(12):e1008198
pubmed: 31790504
Nat Microbiol. 2016 Oct 10;2:16183
pubmed: 27723728
J Biol Chem. 2014 Jun 20;289(25):17872-84
pubmed: 24794869
Nature. 2011 Jul 20;475(7356):343-7
pubmed: 21776080
Elife. 2021 Jul 07;10:
pubmed: 34232858
Curr Top Med Chem. 2001 May;1(1):7-30
pubmed: 11895294
PLoS Pathog. 2012;8(4):e1002613
pubmed: 22511866
J Bacteriol. 2018 May 9;200(11):
pubmed: 29463606
Antimicrob Agents Chemother. 2006 May;50(5):1780-7
pubmed: 16641450
Science. 1999 May 21;284(5418):1318-22
pubmed: 10334980
Trends Microbiol. 2016 Jan;24(1):51-62
pubmed: 26549582
Biochemistry. 2015 Feb 10;54(5):1208-18
pubmed: 25565226
Microbiol Spectr. 2022 Feb 23;10(1):e0194421
pubmed: 35171019
Nat Rev Microbiol. 2020 Mar;18(3):152-163
pubmed: 31748738
FEBS Lett. 1992 Jul 20;306(2-3):119-24
pubmed: 1633865
Appl Microbiol Biotechnol. 2020 Jan;104(1):33-49
pubmed: 31768614
Nat Commun. 2017 Mar 28;8:14888
pubmed: 28348410
ISME J. 2017 Apr;11(4):972-987
pubmed: 28045455
ISME J. 2014 Oct;8(10):2069-79
pubmed: 24694715
PLoS Biol. 2020 May 26;18(5):e3000720
pubmed: 32453732
Nat Rev Microbiol. 2014 Feb;12(2):137-48
pubmed: 24384601
Nat Microbiol. 2021 Sep;6(9):1199-1210
pubmed: 34413503
Curr Biol. 2019 Nov 4;29(21):3622-3634.e5
pubmed: 31630946
Cell Host Microbe. 2014 May 14;15(5):600-10
pubmed: 24832454
Acta Crystallogr D Biol Crystallogr. 2014 Dec 1;70(Pt 12):3233-43
pubmed: 25478841
Nat Commun. 2018 Jun 7;9(1):2219
pubmed: 29880803
Microbiology (Reading). 2008 Jun;154(Pt 6):1570-1583
pubmed: 18524912
ACS Synth Biol. 2012 Aug 17;1(8):345-52
pubmed: 23651288
Acta Crystallogr F Struct Biol Commun. 2020 May 1;76(Pt 5):222-227
pubmed: 32356524
J Struct Biol. 2020 Dec 1;212(3):107651
pubmed: 33096229