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Structural studies of T4S systems by electron microscopy

  • Received: 20 March 2015 Accepted: 21 May 2015 Published: 15 June 2015
  • Type IV secretion (T4S) systems are large dynamic nanomachines that transport DNA and/or proteins through the membranes of bacteria. Analysis of T4S system architecture is an extremely challenging task taking into account their multi protein organisation and lack of overall global symmetry. Nonetheless the last decade demonstrated an amazing progress achieved by X-ray crystallography and cryo-electron microscopy. In this review we present a structural analysis of this dynamic complex based on recent advances in biochemical, biophysical and structural studies.

    Citation: Adam Redzej, Gabriel Waksman, Elena V Orlova. Structural studies of T4S systems by electron microscopy[J]. AIMS Biophysics, 2015, 2(2): 184-199. doi: 10.3934/biophy.2015.2.184

    Related Papers:

  • Type IV secretion (T4S) systems are large dynamic nanomachines that transport DNA and/or proteins through the membranes of bacteria. Analysis of T4S system architecture is an extremely challenging task taking into account their multi protein organisation and lack of overall global symmetry. Nonetheless the last decade demonstrated an amazing progress achieved by X-ray crystallography and cryo-electron microscopy. In this review we present a structural analysis of this dynamic complex based on recent advances in biochemical, biophysical and structural studies.


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    [1] Alvarez-Martinez CE, Christie PJ (2009) Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73: 775-808.
    [2] Filloux A (2004) The underlying mechanisms of type II protein secretion. Biochim Biophys Acta 1694: 163-179. doi: 10.1016/j.bbamcr.2004.05.003
    [3] Cornelis GR, Van Gijsegem F (2000) Assembly and function of type III secretory systems. Annu Rev Microbiol 54: 735-774. doi: 10.1146/annurev.micro.54.1.735
    [4] Henderson IR, Navarro-Garcia F, Desvaux M, et al. (2004) Type V protein secretion pathway: the autotransporter story. Microbiol Mol Biol Rev 68: 692-744. doi: 10.1128/MMBR.68.4.692-744.2004
    [5] Cascales E (2008) The type VI secretion toolkit. EMBO Rep 9: 735-741. doi: 10.1038/embor.2008.131
    [6] Abdallah AM, Gey van Pittius NC, Champion PA, et al. (2007) Type VII secretion--mycobacteria show the way. Nat Rev Microbiol 5: 883-891. doi: 10.1038/nrmicro1773
    [7] Backert S, Meyer TF (2006) Type IV secretion systems and their effectors in bacterial pathogenesis. Curr Opin Microbiol 9: 207-217. doi: 10.1016/j.mib.2006.02.008
    [8] de Jong MF, Sun YH, den Hartigh AB, et al. (2008) Identification of VceA and VceC, two members of the VjbR regulon that are translocated into macrophages by the Brucella type IV secretion system. Mol Microbiol 70: 1378-1396. doi: 10.1111/j.1365-2958.2008.06487.x
    [9] Ninio S, Roy CR (2007) Effector proteins translocated by Legionella pneumophila: strength in numbers. Trends Microbiol 15: 372-380. doi: 10.1016/j.tim.2007.06.006
    [10] O'Callaghan D, Cazevieille C, Allardet-Servent A, et al. (1999) A homologue of the Agrobacterium tumefaciens VirB and Bordetella pertussis Ptl type IV secretion systems is essential for intracellular survival of Brucella suis. Mol Microbiol 33: 1210-1220.
    [11] Lederberg J, Tatum EL (1953) Sex in bacteria; genetic studies, 1945-1952. Science 118: 169-175. doi: 10.1126/science.118.3059.169
    [12] Hofreuter D, Karnholz A, Haas R (2003) Topology and membrane interaction of Helicobacter pylori ComB proteins involved in natural transformation competence. Int J Med Microbiol 293: 153-165. doi: 10.1078/1438-4221-00258
    [13] Ramsey ME, Woodhams KL, Dillard JP (2011) The Gonococcal Genetic Island and Type IV Secretion in the Pathogenic Neisseria. Front Microbiol 2: 61.
    [14] Lessl M, Lanka E (1994) Common mechanisms in bacterial conjugation and Ti-mediated T-DNA transfer to plant cells. Cell 77: 321-324. doi: 10.1016/0092-8674(94)90146-5
    [15] Christie PJ, Cascales E (2005) Structural and dynamic properties of bacterial type IV secretion systems (review). Mol Membr Biol 22: 51-61. doi: 10.1080/09687860500063316
    [16] Trokter M, Felisberto-Rodrigues C, Christie PJ, et al. (2014) Recent advances in the structural and molecular biology of type IV secretion systems. Curr Opin Struct Biol 27: 16-23. doi: 10.1016/j.sbi.2014.02.006
    [17] Pansegrau W, Lanka E (1996) Enzymology of DNA transfer by conjugative mechanisms. Prog Nucleic Acid Res Mol Biol 54: 197-251. doi: 10.1016/S0079-6603(08)60364-5
    [18] Fronzes R, Christie PJ, Waksman G (2009) The structural biology of type IV secretion systems. Nat Rev Microbiol 7: 703-714. doi: 10.1038/nrmicro2218
    [19] Schmidt-Eisenlohr H, Domke N, Angerer C, et al. (1999) Vir proteins stabilize VirB5 and mediate its association with the T pilus of Agrobacterium tumefaciens. J Bacteriol 181: 7485-7492.
    [20] Schmidt-Eisenlohr H, Domke N, Baron C (1999) TraC of IncN plasmid pKM101 associates with membranes and extracellular high-molecular-weight structures in Escherichia coli. J Bacteriol 181: 5563-5571.
    [21] Christie PJ, Atmakuri K, Krishnamoorthy V, et al. (2005) Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu Rev Microbiol 59: 451-485. doi: 10.1146/annurev.micro.58.030603.123630
    [22] Eisenbrandt R, Kalkum M, Lai EM, et al. (1999) Conjugative pili of IncP plasmids, and the Ti plasmid T pilus are composed of cyclic subunits. J Biol Chem 274: 22548-22555. doi: 10.1074/jbc.274.32.22548
    [23] Yuan Q, Carle A, Gao C, et al. (2005) Identification of the VirB4-VirB8-VirB5-VirB2 pilus assembly sequence of type IV secretion systems. J Biol Chem 280: 26349-26359. doi: 10.1074/jbc.M502347200
    [24] Kerr JE, Christie PJ (2010) Evidence for VirB4-mediated dislocation of membrane-integrated VirB2 pilin during biogenesis of the Agrobacterium VirB/VirD4 type IV secretion system. J Bacteriol 192: 4923-4934. doi: 10.1128/JB.00557-10
    [25] Yeo HJ, Yuan Q, Beck MR, et al. (2003) Structural and functional characterization of the VirB5 protein from the type IV secretion system encoded by the conjugative plasmid pKM101. Proc Natl Acad Sci U S A 100: 15947-15952. doi: 10.1073/pnas.2535211100
    [26] Fronzes R, Schafer E, Wang L, et al. (2009) Structure of a type IV secretion system core complex. Science 323: 266-268. doi: 10.1126/science.1166101
    [27] Low HH, Gubellini F, Rivera-Calzada A, et al. (2014) Structure of a type IV secretion system. Nature 508: 550-553. doi: 10.1038/nature13081
    [28] Mossey P, Hudacek A, Das A (2010) Agrobacterium tumefaciens type IV secretion protein VirB3 is an inner membrane protein and requires VirB4, VirB7, and VirB8 for stabilization. J Bacteriol 192: 2830-2838. doi: 10.1128/JB.01331-09
    [29] Jakubowski SJ, Krishnamoorthy V, Cascales E, et al. (2004) Agrobacterium tumefaciens VirB6 domains direct the ordered export of a DNA substrate through a type IV secretion System. J Mol Biol 341: 961-977. doi: 10.1016/j.jmb.2004.06.052
    [30] Judd PK, Mahli D, Das A (2005) Molecular characterization of the Agrobacterium tumefaciens DNA transfer protein VirB6. Microbiology 151: 3483-3492. doi: 10.1099/mic.0.28337-0
    [31] Thorstenson YR, Zambryski PC (1994) The essential virulence protein VirB8 localizes to the inner membrane of Agrobacterium tumefaciens. J Bacteriol 176: 1711-1717.
    [32] Sivanesan D, Baron C (2011) The dimer interface of Agrobacterium tumefaciens VirB8 is important for type IV secretion system function, stability, and association of VirB2 with the core complex. J Bacteriol 193: 2097-2106. doi: 10.1128/JB.00907-10
    [33] Terradot L, Bayliss R, Oomen C, et al. (2005) Structures of two core subunits of the bacterial type IV secretion system, VirB8 from Brucella suis and ComB10 from Helicobacter pylori. Proc Natl Acad Sci U S A 102: 4596-4601. doi: 10.1073/pnas.0408927102
    [34] Bailey S, Ward D, Middleton R, et al. (2006) Agrobacterium tumefaciens VirB8 structure reveals potential protein-protein interaction sites. Proc Natl Acad Sci U S A 103: 2582-2587. doi: 10.1073/pnas.0511216103
    [35] Ripoll-Rozada J, Zunzunegui S, de la Cruz F, et al. (2013) Functional interactions of VirB11 traffic ATPases with VirB4 and VirD4 molecular motors in type IV secretion systems. J Bacteriol 195: 4195-4201. doi: 10.1128/JB.00437-13
    [36] Wallden K, Williams R, Yan J, et al. (2012) Structure of the VirB4 ATPase, alone and bound to the core complex of a type IV secretion system. Proc Natl Acad Sci U S A 109: 11348-11353. doi: 10.1073/pnas.1201428109
    [37] Pena A, Matilla I, Martin-Benito J, et al. (2012) The hexameric structure of a conjugative VirB4 protein ATPase provides new insights for a functional and phylogenetic relationship with DNA translocases. J Biol Chem 287: 39925-39932. doi: 10.1074/jbc.M112.413849
    [38] Durand E, Waksman G, Receveur-Brechot V (2011) Structural insights into the membrane-extracted dimeric form of the ATPase TraB from the Escherichia coli pKM101 conjugation system. BMC Struct Biol 11: 4. doi: 10.1186/1472-6807-11-4
    [39] Yeo HJ, Savvides SN, Herr AB, et al. (2000) Crystal structure of the hexameric traffic ATPase of the Helicobacter pylori type IV secretion system. Mol Cell 6: 1461-1472. doi: 10.1016/S1097-2765(00)00142-8
    [40] Savvides SN, Yeo HJ, Beck MR, et al. (2003) VirB11 ATPases are dynamic hexameric assemblies: new insights into bacterial type IV secretion. EMBO J 22: 1969-1980. doi: 10.1093/emboj/cdg223
    [41] Llosa M, de la Cruz F (2005) Bacterial conjugation: a potential tool for genomic engineering. Res Microbiol 156: 1-6. doi: 10.1016/j.resmic.2004.07.008
    [42] Schroder G, Krause S, Zechner EL, et al. (2002) TraG-like proteins of DNA transfer systems and of the Helicobacter pylori type IV secretion system: inner membrane gate for exported substrates? J Bacteriol 184: 2767-2779. doi: 10.1128/JB.184.10.2767-2779.2002
    [43] Gomis-Ruth FX, Moncalian G, Perez-Luque R, et al. (2001) The bacterial conjugation protein TrwB resembles ring helicases and F1-ATPase. Nature 409: 637-641. doi: 10.1038/35054586
    [44] Orlova EV, Saibil HR (2011) Structural analysis of macromolecular assemblies by electron microscopy. Chem Rev 111: 7710-7748. doi: 10.1021/cr100353t
    [45] De Carlo S, Harris JR (2011) Negative staining and cryo-negative staining of macromolecules and viruses for TEM. Micron 42: 117-131. doi: 10.1016/j.micron.2010.06.003
    [46] Dubochet J (2012) Cryo-EM--the first thirty years. J Microsc 245: 221-224. doi: 10.1111/j.1365-2818.2011.03569.x
    [47] Rivera-Calzada A, Fronzes R, Savva CG, et al. (2013) Structure of a bacterial type IV secretion core complex at subnanometre resolution. EMBO J 32: 1195-1204. doi: 10.1038/emboj.2013.58
    [48] Jakubowski SJ, Kerr JE, Garza I, et al. (2009) Agrobacterium VirB10 domain requirements for type IV secretion and T pilus biogenesis. Mol Microbiol 71: 779-794. doi: 10.1111/j.1365-2958.2008.06565.x
    [49] Christie PJ (1997) Agrobacterium tumefaciens T-complex transport apparatus: a paradigm for a new family of multifunctional transporters in eubacteria. J Bacteriol 179: 3085-3094.
    [50] Cascales E, Christie PJ (2004) Agrobacterium VirB10, an ATP energy sensor required for type IV secretion. Proc Natl Acad Sci U S A 101: 17228-17233. doi: 10.1073/pnas.0405843101
    [51] Banta LM, Kerr JE, Cascales E, et al. (2011) An Agrobacterium VirB10 mutation conferring a type IV secretion system gating defect. J Bacteriol 193: 2566-2574. doi: 10.1128/JB.00038-11
    [52] Zechner EL, Lang S, Schildbach JF (2012) Assembly and mechanisms of bacterial type IV secretion machines. Philos Trans R Soc Lond B Biol Sci 367: 1073-1087. doi: 10.1098/rstb.2011.0207
    [53] Cascales E, Christie PJ (2004) Definition of a bacterial type IV secretion pathway for a DNA substrate. Science 304: 1170-1173. doi: 10.1126/science.1095211
    [54] Schraidt O, Marlovits TC (2011) Three-dimensional model of Salmonella's needle complex at subnanometer resolution. Science 331: 1192-1195. doi: 10.1126/science.1199358
    [55] Kudryashev M, Wang RY, Brackmann M, et al. (2015) Structure of the Type VI Secretion System Contractile Sheath. Cell 160: 952-962. doi: 10.1016/j.cell.2015.01.037
    [56] Clemens DL, Ge P, Lee BY, et al. (2015) Atomic Structure of T6SS Reveals Interlaced Array Essential to Function. Cell 160: 940-951. doi: 10.1016/j.cell.2015.02.005
    [57] McMullan G, Faruqi AR, Henderson R, et al. (2009) Experimental observation of the improvement in MTF from backthinning a CMOS direct electron detector. Ultramicroscopy 109: 1144-1147. doi: 10.1016/j.ultramic.2009.05.005
    [58] Li X, Mooney P, Zheng S, et al. (2013) Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat Methods 10: 584-590. doi: 10.1038/nmeth.2472
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