• Please log in or register to access this feature.

Research Article

You have full text access to this OnlineOpen article

New secreted toxins and immunity proteins encoded within the Type VI secretion system gene cluster of Serratia marcescens

  1. Grant English1,†,
  2. Katharina Trunk1,†,
  3. Vincenzo A. Rao2,
  4. Velupillai Srikannathasan2,
  5. William N. Hunter2,
  6. Sarah J. Coulthurst1,*

Article first published online: 27 SEP 2012

DOI: 10.1111/mmi.12028

Issue

Molecular Microbiology

Molecular Microbiology

Volume 86, Issue 4, pages 921–936, November 2012

Additional Information

How to Cite

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. Molecular Microbiology, 86: 921–936. doi: 10.1111/mmi.12028

Author Information

  1. 1

    Division of Molecular Microbiology, College of Life Sciences, University of Dundee, Dundee, UK

  2. 2

    Division of Biological Chemistry and Drug Discovery, College of Life Sciences, University of Dundee, Dundee, UK

  1. †

    These authors contributed equally and are listed alphabetically.

*For correspondence. E-mail s.j.coulthurst@dundee.ac.uk; Tel. (+44) 1382 386208; Fax (+44) 1382 388216.

  1. †

    These authors contributed equally and are listed alphabetically.

Publication History

  1. Issue published online: 9 NOV 2012
  2. Article first published online: 27 SEP 2012
  3. Accepted manuscript online: 7 SEP 2012 06:52AM EST
  4. Manuscript Accepted: 3 SEP 2012

Funded by

  • Royal Society of Edinburgh
  • Medical Research Scotland. Grant Number: 382 FRG
  • Wellcome Trust. Grant Numbers: 082596, 083481
  • European Commission. Grant Number: FP7/2007-2013
  • Royal Society Project Grant

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article with Supporting Information (HTML) Get PDF (2312K)

References

  • Aubert, D.F., Flannagan, R.S., and Valvano, M.A. (2008) A novel sensor kinase-response regulator hybrid controls biofilm formation and type VI secretion system activity in Burkholderia cenocepacia. Infect Immun 76: 1979–1991.
  • Basler, M., Pilhofer, M., Henderson, G.P., Jensen, G.J., and Mekalanos, J.J. (2012) Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483: 182–186.
  • Bonemann, G., Pietrosiuk, A., and Mogk, A. (2010) Tubules and donuts: a type VI secretion story. Mol Microbiol 76: 815–821.
    Direct Link:
  • Burtnick, M.N., Brett, P.J., Harding, S.V., Ngugi, S.A., Ribot, W.J., Chantratita, N., et al. (2011) The cluster 1 type VI secretion system is a major virulence determinant in Burkholderia pseudomallei. Infect Immun 79: 1512–1525.
  • Cascales, E. (2008) The type VI secretion toolkit. EMBO Rep 9: 735–741.
  • Cascales, E., and Cambillau, C. (2012) Structural biology of type VI secretion systems. Philos Trans R Soc Lond B Biol Sci 367: 1102–1111.
  • Choi, S.H., Lee, J.E., Park, S.J., Kim, M.N., Choo, E.J., Kwak, Y.G., et al. (2007) Prevalence, microbiology, and clinical characteristics of extended-spectrum beta-lactamase-producing Enterobacter spp., Serratia marcescens, Citrobacter freundii, and Morganella morganii in Korea. Eur J Clin Microbiol Infect Dis 26: 557–561.
  • Chou, S., Bui, N.K., Russell, A.B., Lexa, K.W., Gardiner, T.E., Leroux, M., Vollmer, W., and Mougous, J.D. (2012) Structure of a peptidoglycan amidase effector targeted to Gram-negative bacteria by the Type VI secretion system. Cell Rep 1: 656–664.
  • Cruickshank, D.W. (1999) Remarks about protein structure precision. Acta Crystallogr D Biol Crystallogr 55: 583–601.
    Direct Link:
  • Dawson, A., Fyfe, P.K., and Hunter, W.N. (2008) Specificity and reactivity in menaquinone biosynthesis: the structure of Escherichia coli MenD (2-succinyl-5-enolpyruvyl-6-hydroxy-3-cyclohexadiene-1-carboxylate synthase). J Mol Biol 384: 1353–1368.
  • Ding, J., Wang, W., Feng, H., Zhang, Y., and Wang, D.C. (2012) Structural insights into the Pseudomonas aeruginosa type VI virulence effector Tse1 bacteriolysis and self-protection mechanisms. J Biol Chem 287: 26911–26920.
  • Filloux, A., Hachani, A., and Bleves, S. (2008) The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology 154: 1570–1583.
  • Gerlach, R.G., and Hensel, M. (2007) Protein secretion systems and adhesins: the molecular armory of Gram-negative pathogens. Int J Med Microbiol 297: 401–415.
  • Hood, R.D., Singh, P., Hsu, F., Guvener, T., Carl, M.A., Trinidad, R.R., et al. (2010) A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7: 25–37.
  • Jani, A.J., and Cotter, P.A. (2010) Type VI secretion: not just for pathogenesis anymore. Cell Host Microbe 8: 2–6.
  • Kelley, L.A., and Sternberg, M.J. (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363–371.
  • Krissinel, E., and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774–797.
  • Laskowski, R.A., Watson, J.D., and Thornton, J.M. (2005) ProFunc: a server for predicting protein function from 3D structure. Nucleic Acids Res 33: W89–W93.
  • Leiman, P.G., Basler, M., Ramagopal, U.A., Bonanno, J.B., Sauder, J.M., Pukatzki, S., et al. (2009) Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc Natl Acad Sci USA 106: 4154–4159.
  • Li, M., Le Trong, I., Carl, M.A., Larson, E.T., Chou, S., De Leon, J.A., et al. (2012) Structural basis for type VI secretion effector recognition by a cognate immunity protein. PLoS Pathog 8: e1002613.
  • Lockhart, S.R., Abramson, M.A., Beekmann, S.E., Gallagher, G., Riedel, S., Diekema, D.J., et al. (2007) Antimicrobial resistance among Gram-negative bacilli causing infections in intensive care unit patients in the United States between 1993 and 2004. J Clin Microbiol 45: 3352–3359.
  • MacIntyre, D.L., Miyata, S.T., Kitaoka, M., and Pukatzki, S. (2010) The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proc Natl Acad Sci USA 107: 19520–19524.
  • Micossi, E., Hunter, W.N., and Leonard, G.A. (2002) De novo phasing of two crystal forms of tryparedoxin II using the anomalous scattering from S atoms: a combination of small signal and medium resolution reveals this to be a general tool for solving protein crystal structures. Acta Crystallogr D Biol Crystallogr 58: 21–28.
    Direct Link:
  • Mulder, D.T., Cooper, C.A., and Coombes, B.K. (2012) Type VI secretion system-associated gene clusters contribute to pathogenesis of Salmonella enterica serovar Typhimurium. Infect Immun 80: 1996–2007.
  • Murdoch, S.L., Trunk, K., English, G., Fritsch, M.J., Pourkarimi, E., and Coulthurst, S.J. (2011) The opportunistic pathogen Serratia marcescens utilizes type VI secretion to target bacterial competitors. J Bacteriol 193: 6057–6069.
  • de Pace, F., Nakazato, G., Pacheco, A., de Paiva, J.B., Sperandio, V., and da Silveira, W.D. (2010) The type VI secretion system plays a role in type 1 fimbria expression and pathogenesis of an avian pathogenic Escherichia coli strain. Infect Immun 78: 4990–4998.
  • Petersen, T.N., Brunak, S., von Heijne, G., and Nielsen, H. (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785–786.
  • Petty, N.K., Foulds, I.J., Pradel, E., Ewbank, J.J., and Salmond, G.P. (2006) A generalized transducing phage (phiIF3) for the genomically sequenced Serratia marcescens strain Db11: a tool for functional genomics of an opportunistic human pathogen. Microbiology 152: 1701–1708.
  • Pukatzki, S., Ma, A.T., Revel, A.T., Sturtevant, D., and Mekalanos, J.J. (2007) Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci USA 104: 15508–15513.
  • Pukatzki, S., McAuley, S.B., and Miyata, S.T. (2009) The type VI secretion system: translocation of effectors and effector-domains. Curr Opin Microbiol 12: 11–17.
  • Rickman, C., Meunier, F.A., Binz, T., and Davletov, B. (2004) High affinity interaction of syntaxin and SNAP-25 on the plasma membrane is abolished by botulinum toxin E. J Biol Chem 279: 644–651.
  • Rosales-Reyes, R., Skeldon, A.M., Aubert, D.F., and Valvano, M.A. (2012) The Type VI secretion system of Burkholderia cenocepacia affects multiple Rho family GTPases disrupting the actin cytoskeleton and the assembly of NADPH oxidase complex in macrophages. Cell Microbiol 14: 255–273.
    Direct Link:
  • 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., Singh, P., Brittnacher, M., Bui, N.K., Hood, R.D., Carl, M.A., et al. (2012) A widespread bacterial type VI secretion effector superfamily identified using a heuristic approach. Cell Host Microbe 11: 538–549.
  • Sambrook, J., and Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  • Schwarz, S., West, T.E., Boyer, F., Chiang, W.C., Carl, M.A., Hood, R.D., et al. (2010) Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog 6: e1001068.
  • Suarez, G., Sierra, J.C., Erova, T.E., Sha, J., Horneman, A.J., and Chopra, A.K. (2010) A type VI secretion system effector protein, VgrG1, from Aeromonas hydrophila that induces host cell toxicity by ADP ribosylation of actin. J Bacteriol 192: 155–168.
  • Wiseman, T., Williston, S., Brandts, J.F., and Lin, L.N. (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal Biochem 179: 131–137.
  • Yamaguchi, Y., and Inouye, M. (2011) Regulation of growth and death in Escherichia coli by toxin-antitoxin systems. Nat Rev Microbiol 9: 779–790.
  • Zheng, J., and Leung, K.Y. (2007) Dissection of a type VI secretion system in Edwardsiella tarda. Mol Microbiol 66: 1192–1206.
    Direct Link:
  • Zou, T., Yao, X., Qin, B., Zhang, M., Cai, L., Shang, W., et al. (2012) Crystal structure of Pseudomonas aeruginosa Tsi2 reveals a stably folded superhelical antitoxin. J Mol Biol 417: 351–361.
View Full Article with Supporting Information (HTML) Get PDF (2312K)