Abstract
Bacterial secretion systems play critical roles in communication with neighboring bacteria and in the modulation of host immune responses via the secretion of small proteins called effectors. Several secretion systems have been identified and these are denoted types I–VII. Of these, the type VI secretion system (T6SS) and its effectors were only recently elucidated. Most studies on the role and significance of the T6SS and its effectors have focused on human pathogens. In this review, type 6 effectors from plant-associated beneficial and pathogenic bacteria are discussed, including effectors from Agrobacterium tumefaciens, Dickeya dadanti, Rhizobium leguminosarum, Pectobacterium atroseptium, Ralstonia solanacearum, Pseudomonas syringae, Pseudomonas fluorescens, and Pseudomonas protegens. Type 6 effectors act in symbiosis, biofilm formation, virulence, and interbacterial competition. Understanding the impact of type 6 effectors on pathogenesis will contribute to the management of bacterial pathogens in crop plants by allowing the manipulation of intra and inter-specific interactions.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Agrios, G.N. 2008. Plant pathology. Amsterdam, Elsevier Academic Press, pp. 647–649.
Akira, S., Uematsu, S., and Takeuchi, O. 2006. Pathogen recognition and innate immunity. Cell. 124, 783–801.
Alvarez-Martinez, C.E. and Christie, P.J. 2009. Biological diversity of prokaryotic type IV secretion systems. Microbiol. Mol. Biol. Rev. 73, 775–808.
Aschtgen, M.S., Bernard, C.S., De Bentzmann, S., Lloubes, R., and Cascales, E. 2008. SciN is an outer membrane lipoprotein required for type VI secretion in enteroaggregative Escherichia coli. J. Bacteriol. 190, 7523–7531.
Barras, F., van Gijsegem, F., and Chatterjee, A.K. 1994. Extracellular enzymes and pathogenesis of soft-rot Erwinia. Annu. Rev. Phytopathol. 32, 201–234.
Bingle, L.E., Bailey, C.M., and Pallen, M.J. 2008. Type VI secretion: a beginner’s guide. Curr. Opin. Microbiol. 11, 1–6.
Bladergroen, M.R., Badelt, K., and Spaink, H.P. 2003. Infectionblocking genes of a symbiotic Rhizobium leguminosarum strain that are involved in temperature-dependent protein secretion. Mol. Plant Microbe Interact. 16, 53–64.
Blondel, C.J., Jimenez, J.C., Contreras, I., and Santiviago, C.A. 2009. Comparative genomic analysis uncovers 3 novel loci encoding type six secretion systems differentially distributed in Salmonella serotypes. BMC Genomics 10, 354.
Boyer, F., Fichant, G., Berthod, J., Vandenbrouck, Y., and Attree, I. 2009. Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources? BMC Genomics 10, 104.
Bröms, J.E., Ishikawa, T., Wai, S.N., and Sjöstedt, A. 2013. A functional VipA-VipB interaction is required for the type VI secretion system activity of Vibrio cholerae O1 strain A1552. BMC Microbiol. 13, 96.
Coleman, D. 2001. Cellular Microbiology. Bacteria-Host Interactions in Health and Disease. In Henderson, B., Wilson, M., McNab, R., et al (eds.) John Wiley and Sons, 1999. ISBN 0 471 98681 X. Molecular Pathology 4, 55.
Cunnac, S., Lindeberg, M., and Collmer, A. 2009. Pseudomonas syringae type III secretion system effectors: repertoires in search of functions. Curr. Opin. Microbiol. 12, 53–60.
Das, S. and Chaudhuri, K. 2003. Identification of a unique IAHP (IcmF associated homologous proteins) cluster in Vibrio cholera and other proteobacteria through in silico analysis. In Silico Biol. 3, 287–300.
Das, S., Chakrabortty, A., Banerjee, R., and Chaudhuri, K. 2002. Involvement of in vivo induced icmF gene of Vibrio cholera in motility, adherence to epithelial cells, and conjugation frequency. Biochem. Biophys. Res. Commun. 295, 922–928.
Davey, M. and O’Tool, G. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 64, 847–867.
Decoin, V., Barbey, C., Bergeau, D., Latour, X., Feuilloley, M.G., Orange, N., and Merieau, A. 2014. A type VI secretion system is involved in Pseudomonas fluorescens bacterial competition. PLoS One 9, e89411.
Dong, C., Zhang, H., Gao, Z.Q., Wang, W.J., She, Z., Liu, G.F., Shen, Y.Q., Su, X.D., and Dong, Y.H. 2013a. Structural insights into the inhibition of type VI effector Tae3 by its immunity protein Tai3. Biochem. J. 454, 59–68.
Dong, T.G., Ho, B.T., Yoder-Himes, D.R., and Mekalanos, J.J. 2013b. Identification of T6SS-dependent effector and immunity proteins by Tn-seq in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 110, 2623–2628.
English, G., Trunk, K., Rao, V.A., Srikannathasan, V., Hunter, W.N., and Coulthurst, S.J. 2012. New secreted toxins and immunity proteins encoded within the Type VI secretion system gene cluster of Serratia marcescens. Mol. Microbiol. 86, 921–936.
Enos-Berlage, J.L., Guvener, Z.T., Keenan, C.E., and McCarter, L.L. 2005. Genetic determinants of biofilm development of opaque and translucent Vibrio parahaemolyticus. Mol. Microbiol. 55, 1160–1182.
Finlay, B. and Falkow, S. 1989. Common themes in microbial pathogenicity. Microbiol. Rev. 53, 210–230.
Fu, Y., Waldor, M.K., and Mekalanos, J.J. 2013. Tn-Seq analysis of Vibrio cholerae intestinal colonization reveals a role for T6SSmediated antibacterial activity in the host. Cell Host Microbe 14, 652–663.
Haapalainen, M., Mosorin, H., Dorati, F., Wu, R.F., Roine, E., Taira, S., Nissinen, R., Mattinen, L., Jackson, R., Pirhonen, M., and Lin, N.C. 2012. Hcp2, a secreted protein of the phytopathogen Pseudomonas syringae pv. tomato DC3000, is required for fitness for competition against bacteria and yeasts. J. Bacteriol. 194, 4810–4822.
Hauben, L., Moore, E.R.B., Vauterin, L., Steenackers, M., Mergaert, J., Verdonck, L., and Swings, J. 1998. Phylogenetic position of phytopathogens within the Enterobacteriaceae. Syst. Appl. Microbiol. 21, 384–397.
Ho, B.T., Basler, M., and Mekalanos, J.J. 2013. Type 6 secretion system-mediated immunity to type 4 secretion system-mediated gene transfer. Science 342, 250–253.
Ho, B.T., Dong, T.G., and Mekalanos, J.J. 2014. A view to a kill: the bacterial type VI secretion system. Cell Host Microbe 15, 9–21.
Hood, R.D., Singh, P., Hsu, F., Güvener, T., Carl, M.A., Trinidad, R.R., Silverman, J.M., Ohlson, B.B., Hicks, K.G., Plemel, R.L., et al 2010. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7, 25–37.
Hugouvieux-Cotte-Pattat, N. and Condemine, G. 1996. Regulation of pectinolysis in Erwinia chrysanthemi. Annu. Rev. Microbiol. 50, 213–258.
Jin, Q., Thilmony, R., Zwiesler-Vollick, J., and He, S.Y. 2003. Type III protein secretion in Pseudomonas syringae. Microbes Infect. 5, 301–310.
Jones, J.D. and Dangl, J.L. 2006. The plant immune system. Nature 444, 323–329.
Koskiniemi, S., Lamoureux, J.G., Nikolakakis, K.C., t’Kint de Roodenbeke, C., Kaplan, M.D., Low, D.A., and Hayes, C.S. 2013. Rhs proteins from diverse bacteria mediate intercellular competition. Proc. Natl. Acad. Sci. USA 110, 7032–7037.
Lim, J.A., Lee, D.H., and Heu, S. 2014. The interaction of human enteric pathogens with plants. Plant Pathol. J. 30, 109–116.
Lin, J.S., Wu, H.H., Hsu, P.H., Ma, L.S., Pang, Y.Y., Tsai, M.D., and Lai, E.M. 2014. Fha interaction with phosphothreonine of TssL activates type VI secretion in Agrobacterium tumefaciens. PLoS Pathog. 10, e1003991.
Lossi, N.S., Manoli, E., Förster, A., Dajani, R., Pape, T., Freemont, P., and Filloux, A. 2013. The HsiB1C1 (TssB-TssC) complex of the Pseudomonas aeruginosa type VI secretion system forms a bacteriophage tail sheathlike structure. J. Biol. Chem. 288, 7536–7548.
Ma, B., Hibbing, M.E., Kim, H.S., Reedy, R.M., Yedidia, I., Breuer, J., Breuer, J., Glasner, J.D., Perna, N.T., Kelman, A., et al 2007. Host range and molecular phylogenies of the soft rot enterobacterial genera Pectobacterium and Dickeya. Phytopathology 97, 1150–1163.
Ma, L.S., Hachani, A., Lin, J.S., Filloux, A., and Lai, E.M. 2014. Agrobacterium tumefaciens deploys a superfamily of type VI secretion DNase effectors as weapons for interbacterial competition in planta. Cell Host Microbe 16, 94–104.
Mattinen, L., Nissinen, R., TeroRiipi, T., Kalkkinen, N., and Pirhonen, M. 2007. Host-extract induced changes in the secretome of the plant pathogenic bacterium Pectobacterium atrosepticum. Proteomics 7, 3527–3537.
Mattinen, L., Somervuo, P., Nykyri, P., Nissinen, R., Kouvonen, P., Corthals, G., Auvinen, P., Aittamaa, M., Valkonen, J.P.T., and Pirhonen, M. 2008. Microarray profiling of host-extract induced genes and characterization of the type VI secretion cluster in the potato pathogen Pectobacterium atrosepticum. Microbiol. 154, 2387–2396.
Morris, C.E. and Monier, J.M. 2003. The ecological significance of biofilm formation by plant-associated bacteria. Annu. Rev. Phytopathol. 41, 429–453.
Morris, C.E., Monteil, C.L., and Berge, O. 2013. The life history of Pseudomonas syringae: linking agriculture to earth system processes. Annu. Rev. Phytopathol. 51, 85–104.
Mougous, J.D., Cuff, M.E., Raunser, S., Shen, A., Zhou, M., Gifford, C.A., Goodman, A.L., Joachimiak, G., Ordoñez, C.L., Lory, S., et al 2006. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312, 1526–1530.
Nester, E.W. 2015. Agrobacterium: nature’s genetic engineer. Front. Plant Sci. 5, 730.
Nivaskumar, M. and Francetic, O. 2014. Type II secretion system: a magic beanstalk or a protein escalator. Biochim. Biophys. Acta. 1843, 1568–1577.
Pukatzki, S., Ma, A.T., Revel, A.T., Sturtevant, D., and Mekalanos, J.J. 2007. Type VI secretion system translocates a phage tail spikelike protein into target cells where it cross-links actin. Proc. Natl. Acad. Sci. USA 104, 15508–15513.
Pukatzki, S., Ma, A.T., Sturtevant, D., Krastins, B., Sarracino, D., Nelson, W.C., Heidelberg, J.F., and Mekalanos, J.J. 2006. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc. Natl. Acad. Sci. USA 103, 1528–1533.
Roest, H.P., Mulders, I.H., Spaink, H.P., Wijffelman, C.A., and Lugtenberg, B.J. 1997. A Rhizobium leguminosarum biovar trifolii locus not localized on the sym plasmid hinders effective nodulation on plants of the pea cross-inoculation group. Mol. Plant Microbe Interact. 7, 938–941.
Russell, A.B., Hood, R.D., Bui, N.K., LeRoux, M., Vollmer, W., and Mougous, J.D. 2011. Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475, 343–347.
Russell, A.B., Peterson, S.B., and Mougous, J.D. 2014. Type VI secretion system effectors: poisons with a purpose. Nat. Rev. Microbiol. 12, 137–148.
Ryu, C.M. 2013. Promoting plant protection by root-associated microbes. Plant Pathol. J. 29, 123–124.
Ryu, C.M., Choi, H.K., Lee, C.H., Murphy, J.F., Lee, J.K., and Kloepper, J.W. 2013. Modulation of quorum sensing in acylhomoserine lactone-producing or-degrading tobacco plants leads to alteration of induced systemic resistance elicited by the rhizobacterium Serratia marcescens 90–166. Plant Pathol. J. 29, 182–192.
Sarris, P.F., Skandalis, N., Kokkinidis, M., and Panopoulos, N.J. 2010. In silico analysis reveals multiple putative type VI secretion systems and effector proteins in Pseudomonas syringae pathovars. Mol. Plant Pathol. 11, 795–804.
Sauer, K., Camper, A.K., Ehrlich, G.D., Costerton, J.W., and Davies, D.G. 2002. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 184, 1140–1154.
Schechter, L.M., Vencato, M., Jordan, K.L., Schneider, S.E., Schneider, D.J., and Collmer, A. 2006. Multiple approaches to a complete inventory of Pseudomonas syringae pv. tomato DC3000 type III secretion system effector proteins. Mol. Plant Microbe Interact. 19, 1180–1192.
Schell, M.A., Ulrich, R.L., Ribot, W.J., Brueggemann, E.E., Hines, H.B., Chen, D., Lipscomb, L., Kim, H.S., Mrázek, J., Nierman, W.C., and Deshazer, D. 2007. Type VI secretion is a major virulence determinant in Burkholderia mallei. Mol. Microbiol. 64, 1466–1485.
Schumacher, J., Waite, C.J., Bennett, M.H., Perez, M.F., Shethi, K., and Buck, M. 2014. Differential secretome analysis of Pseudomonas syringae pv. tomato using gel-free MS proteomics. Front. Plant Sci. 5, 242.
Schwarz, S., Hood, R.D., and Mougous, J.D. 2010. What is type VI secretion doing in all those bugs? Trends Microbiol. 18, 531–537.
Shao, H., James, D., Lamont, R.J., and Demuth, D.R. 2007. Differential interaction of Aggregatibacter (Actinobacillus) actinomycetemcomitans LsrB and RbsB proteins with autoinducer 2. J. Bacteriol. 189, 5559–5565.
Shneider, M.M., Buth, S.A., Ho, B.T., Basler, M., Mekalanos, J.J., and Leiman, P.G. 2013. PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 500, 350–353.
Silverman, J.M., Brunet, Y.R., Cascales, E., and Mougous, J.D. 2012. Structure and regulation of the type VI secretion system. Annu. Rev. Microbiol. 66, 453–472.
Southey-Pillig, C.J., Davies, D.G., and Sauer, K. 2005. Characterization of temporal protein production in Pseudomonas aeruginosa biofilms. J. Bacteriol. 187, 8114–8126.
Thomson, S.V., Hildebrand, D.C., and Schroth, M.N. 1981. Identification and nutritional differentiation of the Erwinia sugarbeet pathogen from members of Erwinia carotovora and Erwinia chrysanthemi. Phytopathology 71, 1037–1042.
Um, H.Y., Kong, H.G., Lee, H.J., Choi, H.K., Park, E.J., Kim, S.T., Murugiyan, S., Chung, E., Kang, K.Y., and Lee, S.W. 2013. Altered gene expression and intracellular changes of the viable but nonculturable state in Ralstonia solanacearum by copper treatment. Plant Pathol. J. 29, 374–385.
Whitman, W.B., Coleman, D.C., and Wiebe, W.J. 1998. Prokaryotes: The unseen majority. Proc. Natl. Acad. Sci. USA 95, 6578–6583.
Whitney, J.C., Chou, S., Russell, A.B., Biboy, J., Gardiner, T.E., Ferrin, M.A., Brittnacher, M., Vollmer, W., and Mougous, J.D. 2013. Identification, structure, and function of a novel type VI secretion peptidoglycan glycoside hydrolase effector-immunity pair. J. Biol. Chem. 288, 26616–26624.
Wu, H.Y., Chung, P.C., Shih, H.W., Wen, S.R., and Lai, E.M. 2008. Secretome analysis uncovers an Hcp-family protein secreted via a type VI secretion system in Agrobacterium tumefaciens. J. Bacteriol. 190, 2841–2850.
Wu, C.F., Lin, J.S., Shaw, G.C., and Lai, E.M. 2012. Acid-induced type VI secretion system is regulated by ExoR-ChvG/ChvI signaling cascade in Agrobacterium tumefaciens. PLoS Pathog. 8, e1002938.
Xin, X.F. and He, S.Y. 2013. Pseudomonas syringae pv. tomato DC3000: a model pathogen for probing disease susceptibility and hormone signaling in plants. Annu. Rev. Phytopathol. 51, 473–498.
Yao, J. and Allen, C. 2007. The plant pathogen Ralstonia solanacearum needs aerotaxis for normal biofilm formation and interactions with its tomato host. J. Bacteriol. 189, 6415–6524.
Zhang, L., Xu, J., Xu, J., Zhang, H., He, L., and Feng, J. 2014. TssB is essential for virulence and required for type VI secretion system in Ralstonia solanacearum. Microb. Pathog. 74, 1–7.
Zhang, H., Zhang, H., Gao, Z.Q., Wang, W.J., Liu, G.F., Xu, J.H., Su, X.D., and Dong, Y.H. 2013. Structure of the type VI effector-immunity complex (Tae4-Tai4) provides novel insights into the inhibition mechanism of the effector by its immunity protein. J. Biol. Chem. 288, 5928–5939.3
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ryu, CM. Against friend and foe: Type 6 effectors in plant-associated bacteria. J Microbiol. 53, 201–208 (2015). https://doi.org/10.1007/s12275-015-5055-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12275-015-5055-y