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Research Paper

The phospholipase effector Tle1Vc promotes Vibrio cholerae virulence by killing competitors and impacting gene expression

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Article: 2241204 | Received 12 Apr 2023, Accepted 20 Jul 2023, Published online: 01 Aug 2023

References

  • Clemens JD, Nair GB, Ahmed T, Qadri F, Holmgren J. Cholera. Lancet. 2017 Sep 23;390(10101):1539–22. doi:10.1016/S0140-6736(17)30559-7.
  • Sack DA, Sack RB, Nair GB, Siddique AK. Cholera. Lancet. 2004 Jan 17;363(9404):223–233. doi:10.1016/S0140-6736(03)15328-7.
  • Faruque SM, Albert MJ, Mekalanos JJ. Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae. Microbiol Mol Biol Rev. 1998 Dec;62(4):1301–1314. doi:10.1128/MMBR.62.4.1301-1314.1998.
  • Fu Y, Waldor MK, Mekalanos JJ. Tn-Seq analysis of Vibrio cholerae intestinal colonization reveals a role for T6SS-mediated antibacterial activity in the host. Cell Host & Microbe. 2013 Dec 11;14(6):652–663. doi:10.1016/j.chom.2013.11.001.
  • Dong TG, Dong S, Catalano C, Moore R, Liang X, Mekalanos JJ. Generation of reactive oxygen species by lethal attacks from competing microbes. Proc Natl Acad Sci USA. 2015 Feb 17;112(7):2181–2186. doi:10.1073/pnas.1425007112.
  • Cherrak Y, Flaugnatti N, Durand E, Journet L, Cascales E. Structure and activity of the Type VI secretion system. Microbiol Spectr. 2019 Jul;7(4). doi:10.1128/microbiolspec.PSIB-0031-2019
  • Yu KW, Xue P, Fu Y, Yang L. T6SS mediated stress responses for bacterial environmental survival and host adaptation. Int J Mol Sci. 2021 Jan 6;22(2):478. doi:10.3390/ijms22020478.
  • Mougous JD, Cuff ME, Raunser S, Shen A, Zhou M, Gifford CA, Goodman AL, Joachimiak G, Ordoñez CL, Lory S, et al. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science. 2006 Jun 9;312(5779):1526–1530. doi:10.1126/science.1128393.
  • Pukatzki S, Ma AT, Sturtevant D, Krastins B, Sarracino D, Nelson WC, Heidelberg JF, Mekalanos JJ. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci USA. 2006 Jan 31;103(5):1528–1533. doi:10.1073/pnas.0510322103.
  • Boyer F, Fichant G, Berthod J, Vandenbrouck Y, Attree I. Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources? Bmc Genom. 2009 Mar 12;10(1):104. doi:10.1186/1471-2164-10-104.
  • Cherrak Y, Rapisarda C, Pellarin R, Bouvier G, Bardiaux B, Allain F, Malosse C, Rey M, Chamot-Rooke J, Cascales E, et al. Biogenesis and structure of a type VI secretion baseplate. Nature microbiol. 2018 Dec;3(12):1404–1416. doi:10.1038/s41564-018-0260-1.
  • Nguyen VS, Logger L, Spinelli S, Legrand P, Huyen Pham TT, Nhung Trinh TT, Cherrak Y, Zoued A, Desmyter A, Durand E, et al. Type VI secretion TssK baseplate protein exhibits structural similarity with phage receptor-binding proteins and evolved to bind the membrane complex. Nature microbiol. 2017 Jun 26;2(9):17103. doi:10.1038/nmicrobiol.2017.103.
  • Bonemann G, Pietrosiuk A, Mogk A. Tubules and donuts: a type VI secretion story. Mol Microbiol. 2010 May;76(4):815–821. doi:10.1111/j.1365-2958.2010.07171.x.
  • Kapitein N, Bonemann G, Pietrosiuk A, Seyffer F, Hausser I, Locker JK, Mogk A. ClpV recycles VipA/VipB tubules and prevents non-productive tubule formation to ensure efficient type VI protein secretion. Mol Microbiol. 2013 Mar;87(5):1013–1028. doi:10.1111/mmi.12147.
  • Brackmann M, Wang J, Basler M. Type VI secretion system sheath inter-subunit interactions modulate its contraction. EMBO Rep. 2018 Feb;19(2):225–233. doi:10.15252/embr.201744416.
  • Nguyen VS, Douzi B, Durand E, Roussel A, Cascales E, Cambillau C. Towards a complete structural deciphering of Type VI secretion system. Curr Opin Struct Biol. 2018 Apr;49:77–84. doi:10.1016/j.sbi.2018.01.007.
  • Ma J, Pan Z, Huang J, Sun M, Lu C, Yao H. The Hcp proteins fused with diverse extended-toxin domains represent a novel pattern of antibacterial effectors in type VI secretion systems. Virulence. 2017 Oct 3;8(7):1189–1202. doi:10.1080/21505594.2017.1279374.
  • Jurenas D, Journet L. Activity, delivery, and diversity of Type VI secretion effectors. Mol Microbiol. 2021 Mar;115(3):383–394. doi:10.1111/mmi.14648.
  • Russell AB, LeRoux M, Hathazi K, Agnello DM, Ishikawa T, Wiggins PA, Wai SN, Mougous JD. Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature. 2013 Apr 25;496(7446):508–512. doi:10.1038/nature12074.
  • Egan F, Reen FJ, O’Gara F. Tle distribution and diversity in metagenomic datasets reveal niche specialization. Environ Microbiol Rep. 2015 Apr;7(2):194–203. doi:10.1111/1758-2229.12222.
  • Ma S, Dong Y, Wang N, Liu J, Lu C, Liu Y. Identification of a new effector-immunity pair of Aeromonas hydrophila type VI secretion system. Vet Res. 2020 May 24;51(1):71. doi:10.1186/s13567-020-00794-w.
  • Kamal F, Liang X, Manera K, Pei T-T, Kim H, Lam LG, Pun A, Hersch SJ, Dong TG. Differential cellular response to translocated toxic effectors and physical penetration by the Type VI secretion system. Cell Rep. 2020 Jun 16;31(11):107766. doi:10.1016/j.celrep.2020.107766.
  • Crisan CV, Chande AT, Williams K, Raghuram V, Rishishwar L, Steinbach G, Watve SS, Yunker P, Jordan IK, Hammer BK, et al. Analysis of Vibrio cholerae genomes identifies new type VI secretion system gene clusters. Genome Biol. 2019 Aug 12;20(1):163. doi:10.1186/s13059-019-1765-5.
  • Flaugnatti N, Le TT, Canaan S, Aschtgen M-S, Nguyen VS, Blangy S, Kellenberger C, Roussel A, Cambillau C, Cascales E, et al. A phospholipase A1 antibacterial Type VI secretion effector interacts directly with the C-terminal domain of the VgrG spike protein for delivery. Mol Microbiol. 2016 Mar;99(6):1099–1118. doi:10.1111/mmi.13292.
  • Hu H, Zhang H, Gao Z, Wang D, Liu G, Xu J, Lan K, Dong Y. Structure of the type VI secretion phospholipase effector Tle1 provides insight into its hydrolysis and membrane targeting. Acta Crystallogr D Biol Crystallogr. 2014 Aug;70(8):2175–2185. doi:10.1107/S1399004714012899.
  • Tam VC, Serruto D, Dziejman M, Brieher, W., Mekalanos, J J. A type III secretion system in Vibrio cholerae translocates a formin/spire hybrid-like actin nucleator to promote intestinal colonization. Cell Host & Microbe. 2007 Apr 19;1(2):95–107. doi:10.1016/j.chom.2007.03.005.
  • Liu M, Zhao MY, Wang H, Wang Z-H, Wang Z, Liu Y, Li Y-P, Dong T, Fu Y. Pesticin-like effector VgrG3 cp targeting peptidoglycan delivered by the Type VI secretion system contributes to Vibrio cholerae interbacterial competition. Microbiol Spectr. 2023 Jan 10;11(1):e0426722. doi:10.1128/spectrum.04267-22.
  • Philippe N, Alcaraz JP, Coursange E, Geiselmann J, Schneider D. Improvement of pCVD442, a suicide plasmid for gene allele exchange in bacteria. Plasmid. 2004 May;51(3):246–255. doi:10.1016/j.plasmid.2004.02.003.
  • Metcalf WW, Jiang W, Daniels LL, Kim S-K, Haldimann A, Wanner BL. Conditionally replicative and conjugative plasmids CarryinglacZα for cloning, mutagenesis, and allele replacement in bacteria. Plasmid. 1996 Jan;35(1):1–13. doi:10.1006/plas.1996.0001.
  • Choi KH, Schweizer HP. An improved method for rapid generation of unmarked Pseudomonas aeruginosa deletion mutants. BMC Microbiol. 2005 May 23;5(1):30. doi:10.1186/1471-2180-5-30.
  • Guzman LM, Belin D, Carson MJ, Beckwith J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol. 1995 Jul;177(14):4121–4130. doi:10.1128/jb.177.14.4121-4130.1995.
  • Liang X, Kamal F, Pei TT, Xu P, Mekalanos JJ, Dong TG. An onboard checking mechanism ensures effector delivery of the type VI secretion system in Vibrio cholerae. Proc Natl Acad Sci USA. 2019 Nov 12;116(46):23292–23298. doi:10.1073/pnas.1914202116.
  • Khan SR, Gaines J, Roop RM 2nd, Farrand SK. Broad-host-range expression vectors with tightly regulated promoters and their use to examine the influence of TraR and TraM expression on Ti plasmid quorum sensing. Appl Environ Microbiol. 2008 Aug;74(16):5053–5062. doi:10.1128/AEM.01098-08.
  • von Tigerstrom RG, Stelmaschuk S, Tigerstrom RGV. The use of Tween 20 in a sensitive turbidimetric assay of lipolytic enzymes. Can J Microbiol. 1989 Apr;35(4):511–514. doi:10.1139/m89-079.
  • Zottig X, Meddeb-Mouelhi F, Beauregard M. Development of a high-throughput liquid state assay for lipase activity using natural substrates and rhodamine B. Anal Biochem. 2016 Mar 1;496:25–29. doi:10.1016/j.ab.2015.11.020.
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 2001 Dec;25(4):402–408. doi:10.1006/meth.2001.1262.
  • Quereda JJ, Meza-Torres J, Cossart P, Pizarro-Cerdá J. Listeriolysin S: A bacteriocin from epidemic Listeria monocytogenes strains that targets the gut microbiota. Gut Microbes. 2017;8(4):384–391. doi:10.1080/19490976.2017.1290759.
  • Liu M, Hao G, Li Z, Zhou Y, Garcia-Sillas R, Li J, Wang H, Kan B, Zhu J, et al. CitAB two-component system-regulated citrate utilization contributes to Vibrio cholerae competitiveness with the gut microbiota. Infect Immun. 2019 Mar;87(3). doi:10.1128/IAI.00746-18.
  • Drebes Dorr NC, Blokesch M. Interbacterial competition and anti-predatory behaviour of environmental Vibrio cholerae strains. Environ Microbiol. 2020 Oct;22(10):4485–4504. doi:10.1111/1462-2920.15224.
  • Unterweger D, Miyata ST, Bachmann V, Brooks TM, Mullins T, Kostiuk B, Provenzano D, Pukatzki S. The Vibrio cholerae type VI secretion system employs diverse effector modules for intraspecific competition. Nat Commun. 2014 Apr 1;5(1):3549. doi:10.1038/ncomms4549.
  • Dong TG, Ho BT, Yoder-Himes DR, Mekalanos JJ. Identification of T6SS-dependent effector and immunity proteins by Tn-seq in Vibrio cholerae. Proc Natl Acad Sci USA. 2013 Feb 12;110(7):2623–2628. doi:10.1073/pnas.1222783110.
  • Miyata ST, Kitaoka M, Brooks TM, McAuley SB, Pukatzki S. Vibrio cholerae requires the type VI secretion system virulence factor VasX to kill Dictyostelium discoideum. Infect Immun. 2011 Jul;79(7):2941–2949. doi:10.1128/IAI.01266-10.
  • Basler M, Ho BT, Mekalanos JJ. Tit-for-tat: type VI secretion system counterattack during bacterial cell-cell interactions. Cell. 2013 Feb 14;152(4):884–894. doi:10.1016/j.cell.2013.01.042.
  • Taylor RK, Miller VL, Furlong DB, Mekalanos JJ. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc Natl Acad Sci USA. 1987 May;84(9):2833–2837. doi:10.1073/pnas.84.9.2833.
  • Wang P, Dong JF, Li RQ, Li L, Zou Q-H. Roles of the Hcp family proteins in the pathogenicity of Salmonella typhimurium 14028s. Virulence. 2020 Dec;11(1):1716–1726. doi:10.1080/21505594.2020.1854538.
  • Li Y, Chen L, Zhang P, Bhagirath AY, Duan K. ClpV3 of the H3-Type VI secretion system (H3-T6SS) affects multiple virulence factors in Pseudomonas aeruginosa. Front Microbiol. 2020;11:1096. doi:10.3389/fmicb.2020.01096.
  • Zhang LQ, Xu JS, Xu J, Zhang H, He L, Feng J. TssB is essential for virulence and required for Type VI secretion system in Ralstonia solanacearum. Microb Pathog. 2014 Sep;74:1–7. doi:10.1016/j.micpath.2014.06.006.
  • Klose KE, Mekalanos JJ. Differential regulation of multiple flagellins in Vibrio cholerae. J Bacteriol. 1998 Jan;180(2):303–316. doi:10.1128/JB.180.2.303-316.1998.
  • Prouty MG, Correa NE, Klose KE. The novel sigma54- and sigma28-dependent flagellar gene transcription hierarchy of Vibrio cholerae. Mol Microbiol. 2001 Mar;39(6):1595–1609. doi:10.1046/j.1365-2958.2001.02348.x.
  • Echazarreta MA, Klose KE. Vibrio flagellar synthesis. Front Cell Infect Microbiol. 2019;9:131. doi:10.3389/fcimb.2019.00131.
  • Echazarreta MA, Kepple JL, Yen LH, Chen Y, Klose KE. A critical region in the FlaA flagellin facilitates filament formation of the Vibrio cholerae flagellum. J Bacteriol. 2018 Aug 1;200(15). doi:10.1128/JB.00029-18.
  • Song L, Pan J, Yang Y, Zhang Z, Cui R, Jia S, Wang Z, Yang C, Xu L, Dong TG, et al. Contact-independent killing mediated by a T6SS effector with intrinsic cell-entry properties. Nat Commun. 2021 Jan 18;12(1):423. doi:10.1038/s41467-020-20726-8.
  • Sana TG, Flaugnatti N, Lugo KA, Lam LH, Jacobson A, Baylot V, Durand E, Journet L, Cascales E, Monack DM. Salmonella Typhimurium utilizes a T6SS-mediated antibacterial weapon to establish in the host gut. Proc Natl Acad Sci USA. 2016 Aug 23;113(34):E5044–51. doi:10.1073/pnas.1608858113.
  • LaCourse KD, Peterson SB, Kulasekara HD, Radey MC, Kim J, Mougous JD. Conditional toxicity and synergy drive diversity among antibacterial effectors. Nature microbiol. 2018 Apr;3(4):440–446. doi:10.1038/s41564-018-0113-y.
  • Liu L, Ye M, Li X, Li J, Deng Z, Yao Y-F, Ou H-Y. Identification and characterization of an antibacterial Type VI secretion system in the carbapenem-resistant strain Klebsiella pneumoniae HS11286. Front Cell Infect Microbiol. 2017;7:442. doi:10.3389/fcimb.2017.00442.
  • Lery LM, Frangeul L, Tomas A, Passet V, Almeida AS, Bialek-Davenet S, Barbe V, Bengoechea JA, Sansonetti P, Brisse S, et al. Comparative analysis of Klebsiella pneumoniae genomes identifies a phospholipase D family protein as a novel virulence factor. BMC Biol. 2014 May 29;12(1):41. doi:10.1186/1741-7007-12-41.
  • Tang MX, Pei TT, Xiang Q, Wang Z-H, Luo H, Wang X-Y, Fu Y, Dong T. Abiotic factors modulate interspecies competition mediated by the type VI secretion system effectors in Vibrio cholerae. Isme J. 2022 Jul;16(7):1765–1775. doi:10.1038/s41396-022-01228-5.
  • Kostiuk B, Santoriello FJ, Diaz-Satizabal L, Bisaro F, Lee K-J, Dhody AN, Provenzano D, Unterweger D, Pukatzki S. Author Correction: Type VI secretion system mutations reduced competitive fitness of classical Vibrio cholerae biotype. Nat Commun. 2022 Feb 11;13(1):916. doi:10.1038/s41467-022-28572-6.
  • Sha J, Rosenzweig JA, Kozlova EV, Wang S, Erova TE, Kirtley ML, van Lier CJ, Chopra AK. Evaluation of the roles played by Hcp and VgrG type 6 secretion system effectors in Aeromonas hydrophila SSU pathogenesis. Microbiology. 2013 Jun;159(Pt 6):1120–1135. doi:10.1099/mic.0.063495-0.
  • Ho BT, Fu Y, Dong TG, Mekalanos JJ. Vibrio cholerae type 6 secretion system effector trafficking in target bacterial cells. Proc Natl Acad Sci USA. 2017 Aug 29;114(35):9427–9432. doi:10.1073/pnas.1711219114.
  • Sporing I, Felgner S, Preusse M, Eckweiler D, Rohde M, Häussler S, Weiss S, Erhardt M, et al. Regulation of flagellum biosynthesis in response to cell envelope stress in Salmonella enterica Serovar Typhimurium. mBio. 2018 May 1;9 (3).10.1128/mBio.00736-17
  • Palmer AD, Slauch JM, O’Toole G. Envelope stress and regulation of the Salmonella pathogenicity Island 1 Type III secretion system. J Bacteriol. 2020 Aug 10;202(17). doi:10.1128/JB.00272-20.
  • Nishino K, Honda T, Yamaguchi A. Genome-wide analyses of Escherichia coli gene expression responsive to the BaeSR two-component regulatory system. J Bacteriol. 2005 Mar;187(5):1763–1772. doi:10.1128/JB.187.5.1763-1772.2005.
  • Hersch SJ, Watanabe N, Stietz MS, Manera K, Kamal F, Burkinshaw B, Lam L, Pun A, Li M, Savchenko A, et al. Envelope stress responses defend against type six secretion system attacks independently of immunity proteins. Nature microbiol. 2020 May;5(5):706–714. doi:10.1038/s41564-020-0672-6.
  • Logan SL, Thomas J, Yan JY, Baker RP, Shields DS, Xavier JB, Hammer BK, Parthasarathy R. The Vibrio cholerae type VI secretion system can modulate host intestinal mechanics to displace gut bacterial symbionts. Proc Natl Acad Sci USA. 2018 Apr 17;115(16):E3779–E3787. doi:10.1073/pnas.1720133115.