Engineering the T6SS of Pseudomonas for targeted delivery of antibacterial and antifungal effectors

Hibbing ME, Fuqua C, Parsek MR, Peterson SB. Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol. 2010;8(1):15–25.

Article  Google Scholar 

Stubbendieck RM, Vargas-Bautista C, Straight PD. Bacterial Communities: Interactions to Scale. Front Microbiol. 2016;7:1234.

Article  MATH  Google Scholar 

Granato ET, Meiller-Legrand TA, Foster KR. The Evolution and Ecology of Bacterial Warfare. Curr Biol. 2019;29(11):R521–37.

Article  Google Scholar 

Niehaus L, Boland I, Liu M, Chen K, Fu D, Henckel C, et al. Microbial coexistence through chemical-mediated interactions. Nat Commun. 2019;10(1):2052.

Article  Google Scholar 

Peterson SB, Bertolli SK, Mougous JD. The Central Role of Interbacterial Antagonism in Bacterial Life. Curr Biol. 2020;30(19):R1203–14.

Article  Google Scholar 

Martin JF, Casqueiro J, Liras P. Secretion systems for secondary metabolites: how producer cells send out messages of intercellular communication. Curr Opin Microbiol. 2005;8(3):282–93.

Article  Google Scholar 

Blasey N, Rehrmann D, Riebisch AK, Muhlen S. Targeting bacterial pathogenesis by inhibiting virulence-associated Type III and Type IV secretion systems. Front Cell Infect Microbiol. 2022;12:1065561.

Article  Google Scholar 

Fronzes R, Christie PJ, Waksman G. The structural biology of type IV secretion systems. Nat Rev Microbiol. 2009;7(10):703–14.

Article  MATH  Google Scholar 

Lasica AM, Ksiazek M, Madej M, Potempa J. The Type IX Secretion System (T9SS): Highlights and Recent Insights into Its Structure and Function. Front Cell Infect Microbiol. 2017;7:215.

Article  MATH  Google Scholar 

Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W, Mougous JD. Type VI secretion delivers bacteriolytic effectors to target cells. Nature. 2011;475(7356):343–7.

Article  Google Scholar 

Mougous JD, Cuff ME, Raunser S, Shen A, Zhou M, Gifford CA, et al. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science. 2006;312(5779):1526–30.

Article  Google Scholar 

Pukatzki S, Ma AT, Sturtevant D, Krastins B, Sarracino D, Nelson WC, et al. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci U S A. 2006;103(5):1528–33.

Article  Google Scholar 

Hood RD, Peterson SB, Mougous JD. From Striking Out to Striking Gold: Discovering that Type VI Secretion Targets Bacteria. Cell Host Microbe. 2017;21(3):286–9.

Article  Google Scholar 

Basler M, Pilhofer M, Henderson GP, Jensen GJ, Mekalanos JJ. Type VI secretion requires a dynamic contractile phage tail-like structure. Nature. 2012;483(7388):182–6.

Article  Google Scholar 

Silverman JM, Brunet YR, Cascales E, Mougous JD. Structure and regulation of the type VI secretion system. Annu Rev Microbiol. 2012;66:453–72.

Article  Google Scholar 

Cianfanelli FR, Alcoforado Diniz J, Guo M, De Cesare V, Trost M, Coulthurst SJ. VgrG and PAAR Proteins Define Distinct Versions of a Functional Type VI Secretion System. PLoS Pathog. 2016;12(6): e1005735.

Article  Google Scholar 

Cianfanelli FR, Monlezun L, Coulthurst SJ. Aim, Load, Fire: The Type VI Secretion System, a Bacterial Nanoweapon. Trends Microbiol. 2016;24(1):51–62.

Article  Google Scholar 

Trunk K, Peltier J, Liu YC, Dill BD, Walker L, Gow NAR, et al. The type VI secretion system deploys antifungal effectors against microbial competitors. Nat Microbiol. 2018;3(8):920–31.

Article  Google Scholar 

Molina-Santiago C, Pearson JR, Navarro Y, Berlanga-Clavero MV, Caraballo-Rodriguez AM, Petras D, et al. The extracellular matrix protects Bacillus subtilis colonies from Pseudomonas invasion and modulates plant co-colonization. Nat Commun. 2019;10(1):1919.

Article  Google Scholar 

Perez-Lorente AI, Molina-Santiago C, de Vicente A, Romero D. Sporulation Activated via sigma(W) Protects Bacillus from a Tse1 Peptidoglycan Hydrolase Type VI Secretion System Effector. Microbiol Spectr. 2023;11(2): e0504522.

Article  Google Scholar 

Ren A, Jia M, Liu J, Zhou T, Wu L, Dong T, et al. Acquisition of T6SS Effector TseL Contributes to the Emerging of Novel Epidemic Strains of Pseudomonas aeruginosa. Microbiol Spectr. 2023;11(1): e0330822.

Article  Google Scholar 

Allsopp LP, Bernal P. Killing in the name of: T6SS structure and effector diversity. Microbiology (Reading). 2023;169(7).

Bondage DD, Lin J-S, Ma L-S, Kuo C-H, Lai E-M. VgrG C terminus confers the type VI effector transport specificity and is required for binding with PAAR and adaptor–effector complex. 2016;113(27):E3931-E40.

Flaugnatti N, Le TTH, Canaan S, Aschtgen M-S, Nguyen VS, Blangy S, et al. A phospholipase A1 antibacterial Type VI secretion effector interacts directly with the C-terminal domain of the VgrG spike protein for delivery. 2016;99(6):1099–118.

Shneider MM, Buth SA, Ho BT, Basler M, Mekalanos JJ, Leiman PG. PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature. 2013;500(7462):350–3.

Article  Google Scholar 

Alcoforado Diniz J, Liu YC, Coulthurst SJ. Molecular weaponry: diverse effectors delivered by the Type VI secretion system. Cell Microbiol. 2015;17(12):1742–51.

Article  Google Scholar 

Durand E, Nguyen VS, Zoued A, Logger L, Pehau-Arnaudet G, Aschtgen MS, et al. Biogenesis and structure of a type VI secretion membrane core complex. Nature. 2015;523(7562):555–60.

Article  Google Scholar 

Jana B, Fridman CM, Bosis E, Salomon D. A modular effector with a DNase domain and a marker for T6SS substrates. Nat Commun. 2019;10(1):3595.

Article  Google Scholar 

Wood TE, Howard SA, Wettstadt S, Filloux A. PAAR proteins act as the “sorting hat” of the type VI secretion system. Microbiology (Reading). 2019;165(11):1203–18.

Article  Google Scholar 

Liang X, Pei TT, Li H, Zheng HY, Luo H, Cui Y, et al. VgrG-dependent effectors and chaperones modulate the assembly of the type VI secretion system. PLoS Pathog. 2021;17(12): e1010116.

Article  Google Scholar 

Pukatzki S, Ma AT, Revel AT, Sturtevant D, Mekalanos JJ. Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci U S A. 2007;104(39):15508–13.

Article  Google Scholar 

Wettstadt S, Lai EM, Filloux A. Solving the Puzzle: Connecting a Heterologous Agrobacterium tumefaciens T6SS Effector to a Pseudomonas aeruginosa Spike Complex. Front Cell Infect Microbiol. 2020;10:291.

Article  Google Scholar 

Flaugnatti N, Le TT, Canaan S, Aschtgen MS, Nguyen VS, Blangy S, 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;99(6):1099–118.

Article  Google Scholar 

Ma LS, Hachani A, Lin JS, Filloux A, Lai EM. Agrobacterium tumefaciens deploys a superfamily of type VI secretion DNase effectors as weapons for interbacterial competition in planta. Cell Host Microbe. 2014;16(1):94–104.

Article  Google Scholar 

Kamal F, Liang X, Manera K, Pei TT, Kim H, Lam LG, et al. Differential Cellular Response to Translocated Toxic Effectors and Physical Penetration by the Type VI Secretion System. Cell Rep. 2020;31(11): 107766.

Article  Google Scholar 

Jana B, Keppel K, Salomon D. Engineering a customizable antibacterial T6SS-based platform in Vibrio natriegens. EMBO Rep. 2021;22(11): e53681.

Article  Google Scholar 

Hersch SJ, Lam L, Dong TG. Engineered Type Six Secretion Systems Deliver Active Exogenous Effectors and Cre Recombinase. mBio. 2021;12(4):e0111521.

Ting SY, Martinez-Garcia E, Huang S, Bertolli SK, Kelly KA, Cutler KJ, et al. Targeted Depletion of Bacteria from Mixed Populations by Programmable Adhesion with Antagonistic Competitor Cells. Cell Host Microbe. 2020;28(2):313–21 e6.

Bernal P, Llamas MA, Filloux A. Type VI secretion systems in plant-associated bacteria. Environ Microbiol. 2018;20(1):1–15.

Article  Google Scholar 

de Lorenzo V, Perez-Pantoja D, Nikel PI. Pseudomonas putida KT2440: the long journey of a soil-dweller to become a synthetic biology chassis. J Bacteriol. 2024;206(7): e0013624.

Article  Google Scholar 

Weimer A, Kohlstedt M, Volke DC, Nikel PI, Wittmann C. Industrial biotechnology of Pseudomonas putida: advances and prospects. Appl Microbiol Biotechnol. 2020;104(18):7745–66.

Article  Google Scholar 

Martínez-García E, Fraile S, Algar E, Aparicio T, Velázquez E, Calles B, et al. SEVA 4.0: an update of the Standard European Vector Architecture database for advanced analysis and programming of bacterial phenotypes. Nucleic Acids Research. 2022;51(D1):D1558-D67.

Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA 3rd, Smith HO. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods. 2009;6(5):343–5.

Article  Google Scholar 

Choi KH, Kumar A, Schweizer HP. A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J Microbiol Methods. 2006;64(3):391–7.

Article  Google Scholar 

Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9(7):676–82.

Article  Google Scholar 

Jiang F, Wang X, Wang B, Chen L, Zhao Z, Waterfield NR, et al. The Pseudomonas aeruginosa Type VI Secretion PGAP1-like Effector Induces Host Autophagy by Activating Endoplasmic Reticulum Stress. Cell Rep. 2016;16(6):1502–9.

Article  Google Scholar 

Abramson J, Adler J, Dunger J, Evans R, Green T, Pritzel A, et al. Accurate structure prediction of biomolecular interactions with AlphaFold 3. Nature. 2024;630(8016):493–500.

Article  Google Scholar 

Álvarez-Salmoral D, Borza R, Xie R, Joosten RP, Hekkelman ML, Perrakis A. AlphaBridge: tools for the analysis of predicted macromolecular complexes. bioRxiv. 2024:2024.10.23.619601.

Guerra RM, Maleno FD, Figueras MJ, Pujol-Bajador I, Fernandez-Bravo A. Potential Pathogenicity of Aeromonas spp. Recovered in River Water, Soil, and Vegetation from a Natural Recreational Area. Pathogens. 2022;11(11).

Richards JK, Xiao CL, Jurick WM, 2nd. Botrytis spp.: A Contemporary Perspective and Synthesis of Recent Scientific Developments of a Widespread Genus that Threatens Global Food Security. Phytopathology. 2021;111(3):432–6.

DEAN R, VAN KAN JAL, PRETORIUS ZA, HAMMOND-KOSACK KE, DI PIETRO A, SPANU PD, et al. The Top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology. 2012;13(4):414–30.

Comments (0)

No login
gif