Structural biology of type VI secretion systems

Type VI secretion systems (T6SSs) are transenvelope complexes specialized in the transport of proteins or domains directly into target cells. These systems are versatile as they can target either eukaryotic host cells and therefore modulate the bacteria–host interaction and pathogenesis or bacterial cells and therefore facilitate access to a specific niche. These molecular machines comprise at least 13 proteins. Although recent years have witnessed advances in the role and function of these secretion systems, little is known about how these complexes assemble in the cell envelope. Interestingly, the current information converges to the idea that T6SSs are composed of two subassemblies, one resembling the contractile bacteriophage tail, whereas the other subunits are embedded in the inner and outer membranes and anchor the bacteriophage-like structure to the cell envelope. In this review, we summarize recent structural information on individual T6SS components emphasizing the fact that T6SSs are composite systems, adapting subunits from various origins.

[1]  D. Eide,et al.  Zinc-responsive coactivator recruitment by the yeast Zap1 transcription factor , 2012, MicrobiologyOpen.

[2]  L. Journet,et al.  The C-tail anchored TssL subunit, an essential protein of the enteroaggregative Escherichia coli Sci-1 Type VI secretion system, is inserted by YidC , 2012, MicrobiologyOpen.

[3]  K. Hueffer,et al.  The biochemical properties of the Francisella pathogenicity island (FPI)-encoded proteins IglA, IglB, IglC, PdpB and DotU suggest roles in type VI secretion. , 2011, Microbiology.

[4]  P. Freemont,et al.  Structure–function analysis of HsiF, a gp25-like component of the type VI secretion system, in Pseudomonas aeruginosa , 2011, Microbiology.

[5]  W. Hunter,et al.  The structure of Serratia marcescens Lip, a membrane-bound component of the type VI secretion system , 2011, Acta crystallographica. Section D, Biological crystallography.

[6]  C. Cambillau,et al.  Towards a Structural Comprehension of Bacterial Type VI Secretion Systems: Characterization of the TssJ-TssM Complex of an Escherichia coli Pathovar , 2011, PLoS pathogens.

[7]  A. Dessen,et al.  Structural characterization and membrane localization of ExsB from the type III secretion system (T3SS) of Pseudomonas aeruginosa. , 2011, Journal of molecular biology.

[8]  Katharina Trunk,et al.  The Opportunistic Pathogen Serratia marcescens Utilizes Type VI Secretion To Target Bacterial Competitors , 2011, Journal of bacteriology.

[9]  Christian Cambillau,et al.  A Common Evolutionary Origin for Tailed-Bacteriophage Functional Modules and Bacterial Machineries , 2011, Microbiology and Molecular Reviews.

[10]  Waldemar Vollmer,et al.  Type VI secretion delivers bacteriolytic effectors to target cells , 2011, Nature.

[11]  H. Zentgraf,et al.  Molecular Basis for the Unique Role of the AAA+ Chaperone ClpV in Type VI Protein Secretion* , 2011, The Journal of Biological Chemistry.

[12]  A. Records The type VI secretion system: a multipurpose delivery system with a phage-like machinery. , 2011, Molecular plant-microbe interactions : MPMI.

[13]  D. Veesler,et al.  The Opening of the SPP1 Bacteriophage Tail, a Prevalent Mechanism in Gram-positive-infecting Siphophages* , 2011, The Journal of Biological Chemistry.

[14]  A. Joachimiak,et al.  Crystal structure of secretory protein Hcp3 from Pseudomonas aeruginosa , 2011, Journal of Structural and Functional Genomics.

[15]  H. Nagai,et al.  Type IVB Secretion Systems of Legionella and Other Gram-Negative Bacteria , 2011, Front. Microbio..

[16]  A. Filloux,et al.  Type VI Secretion System in Pseudomonas aeruginosa , 2011, The Journal of Biological Chemistry.

[17]  K. Leung,et al.  Type VI secretion regulation: crosstalk and intracellular communication. , 2011, Current opinion in microbiology.

[18]  M. Rossmann,et al.  Morphogenesis of the T4 tail and tail fibers , 2010, Virology Journal.

[19]  J. Mougous,et al.  What is type VI secretion doing in all those bugs? , 2010, Trends in microbiology.

[20]  Mark S. Thomas,et al.  Anchoring the type VI secretion system to the peptidoglycan: TssL, TagL, TagP... what else? , 2010, Virulence.

[21]  S. Pukatzki,et al.  The Vibrio cholerae type VI secretion system displays antimicrobial properties , 2010, Proceedings of the National Academy of Sciences.

[22]  Ka Yin Leung,et al.  Structural Basis for the Secretion of EvpC: A Key Type VI Secretion System Protein from Edwardsiella tarda , 2010, PloS one.

[23]  D. Veesler,et al.  Crystal Structure of Bacteriophage SPP1 Distal Tail Protein (gp19.1) , 2010, The Journal of Biological Chemistry.

[24]  M. Valvano,et al.  BcsKC Is an Essential Protein for the Type VI Secretion System Activity in Burkholderia cenocepacia That Forms an Outer Membrane Complex with BcsLB* , 2010, The Journal of Biological Chemistry.

[25]  T. West,et al.  Burkholderia Type VI Secretion Systems Have Distinct Roles in Eukaryotic and Bacterial Cell Interactions , 2010, PLoS pathogens.

[26]  P. Cotter,et al.  Type VI secretion: not just for pathogenesis anymore. , 2010, Cell host & microbe.

[27]  E. Cascales,et al.  Nooks and Crannies in Type VI Secretion Regulation , 2010, Journal of bacteriology.

[28]  A. Mogk,et al.  Tubules and donuts: a type VI secretion story , 2010, Molecular microbiology.

[29]  G. Sciara,et al.  Structure of lactococcal phage p2 baseplate and its mechanism of activation , 2010, Proceedings of the National Academy of Sciences.

[30]  R. Lloubès,et al.  The SciZ protein anchors the enteroaggregative Escherichia coli Type VI secretion system to the cell wall , 2010, Molecular microbiology.

[31]  D. Goodlett,et al.  A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. , 2010, Cell host & microbe.

[32]  P. Leiman,et al.  The baseplate wedges of bacteriophage T4 spontaneously assemble into hubless baseplate-like structure in vitro. , 2010, Journal of molecular biology.

[33]  J. Sha,et al.  A Type VI Secretion System Effector Protein, VgrG1, from Aeromonas hydrophila That Induces Host Cell Toxicity by ADP Ribosylation of Actin , 2009, Journal of bacteriology.

[34]  E. Lai,et al.  An IcmF Family Protein, ImpLM, Is an Integral Inner Membrane Protein Interacting with ImpKL, and Its Walker A Motif Is Required for Type VI Secretion System-Mediated Hcp Secretion in Agrobacterium tumefaciens , 2009, Journal of bacteriology.

[35]  Michael G Rossmann,et al.  The tail sheath structure of bacteriophage T4: a molecular machine for infecting bacteria , 2009, EMBO Journal.

[36]  J. Mekalanos,et al.  Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. , 2009, Cell host & microbe.

[37]  A. Davidson,et al.  The phage λ major tail protein structure reveals a common evolution for long-tailed phages and the type VI bacterial secretion system , 2009, Proceedings of the National Academy of Sciences.

[38]  S. Kanamaru Structural similarity of tailed phages and pathogenic bacterial secretion systems , 2009, Proceedings of the National Academy of Sciences.

[39]  J. M. Sauder,et al.  Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin , 2009, Proceedings of the National Academy of Sciences.

[40]  Frédéric Boyer,et al.  Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources? , 2009, BMC Genomics.

[41]  Alexander V. Diemand,et al.  Remodelling of VipA/VipB tubules by ClpV‐mediated threading is crucial for type VI protein secretion , 2009, The EMBO journal.

[42]  A. Sjöstedt,et al.  A Conserved α-Helix Essential for a Type VI Secretion-Like System of Francisella tularensis , 2009, Journal of bacteriology.

[43]  S. Pukatzki,et al.  The type VI secretion system: translocation of effectors and effector-domains. , 2009, Current opinion in microbiology.

[44]  R. Lloubès,et al.  SciN Is an Outer Membrane Lipoprotein Required for Type VI Secretion in Enteroaggregative Escherichia coli , 2008, Journal of bacteriology.

[45]  E. Cascales,et al.  The type VI secretion toolkit , 2008, EMBO reports.

[46]  Sophie Bleves,et al.  The bacterial type VI secretion machine: yet another player for protein transport across membranes. , 2008, Microbiology.

[47]  Yifan Cheng,et al.  In vitro self-assembly of tailorable nanotubes from a simple protein building block , 2008, Proceedings of the National Academy of Sciences.

[48]  Christopher M. Bailey,et al.  Type VI secretion: a beginner's guide. , 2008, Current opinion in microbiology.

[49]  K. Leung,et al.  Dissection of a type VI secretion system in Edwardsiella tarda , 2007, Molecular microbiology.

[50]  D. Waugh,et al.  New protein fold revealed by a 1.65 Å resolution crystal structure of Francisella tularensis pathogenicity island protein IglC , 2007, Protein science : a publication of the Protein Society.

[51]  Andrew T. Revel,et al.  Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin , 2007, Proceedings of the National Academy of Sciences.

[52]  Mark S. Thomas,et al.  In vivo expression technology identifies a type VI secretion system locus in Burkholderia pseudomallei that is induced upon invasion of macrophages. , 2007, Microbiology.

[53]  L. Lian,et al.  The solution structure of a domain from the Neisseria meningitidis lipoprotein PilP reveals a new beta-sandwich fold. , 2006, Journal of molecular biology.

[54]  Stephen Lory,et al.  A Virulence Locus of Pseudomonas aeruginosa Encodes a Protein Secretion Apparatus , 2006, Science.

[55]  W. Nelson,et al.  Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[56]  E. Yamashita,et al.  Structure of the central hub of bacteriophage Mu baseplate determined by X-ray crystallography of gp44. , 2005, Journal of molecular biology.

[57]  Fumio Arisaka,et al.  The tail structure of bacteriophage T4 and its mechanism of contraction , 2005, Nature Structural &Molecular Biology.

[58]  Conrad C. Huang,et al.  UCSF Chimera—A visualization system for exploratory research and analysis , 2004, J. Comput. Chem..

[59]  Fumio Arisaka,et al.  The bacteriophage T4 DNA injection machine. , 2004, Current opinion in structural biology.

[60]  Fumio Arisaka,et al.  Three-dimensional structure of bacteriophage T4 baseplate , 2003, Nature Structural Biology.

[61]  Fumio Arisaka,et al.  Structure of the cell-puncturing device of bacteriophage T4 , 2002, Nature.

[62]  K. Bieńkowska-Szewczyk,et al.  Identification of T4 gene 25 product, a component of the tail baseplate, as a 15K lysozyme , 1986, Molecular and General Genetics MGG.

[63]  Keya Chaudhuri,et al.  Identification of a unique IAHP (IcmF associated homologous proteins) cluster in Vibrio cholerae and other proteobacteria through in silico analysis , 2003, Silico Biol..

[64]  W. Delano The PyMOL Molecular Graphics System , 2002 .