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Chapter 1 : Electron Cryotomography of Bacterial Secretion Systems

Authors: Catherine M. Oikonomou, Grant J. Jensen
Content Type: Monograph
Publication Year: 2019

Category: Bacterial Pathogenesis

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Electron Cryotomography of Bacterial Secretion Systems, Page 1 of 2

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Abstract:

The envelope of bacterial cells consists of at least one—and often two—membranes, a cell wall, and possibly a surface layer. This envelope allows cells to differentiate themselves from their environment and handle the resulting osmotic pressure, but it also presents a significant obstacle. Anything a cell wishes to export, from a motility appendage to a plasmid, needs to be ushered across this barrier. To accomplish this, bacteria have evolved a battery of secretion systems. Secretion systems are often constructed from dozens of protein building blocks embedded in the cell’s envelope. The size, complexity, and location of these machines make them a particular challenge for structural characterization. High-resolution structure determination techniques such as X-ray crystallography and transmission electron microscopy (TEM)-based single-particle reconstruction (SPR) require objects to be purified from their cellular environment. This is problematic for membrane-associated proteins, which embed in the lipid bilayer by means of exposed hydrophobic patches. These patches can be protected during purification by adding detergents to the solvent, but often structural alterations still occur. Secretion systems are also unusually large targets and frequently lose peripheral or loosely-associated components during purification. In addition, they often cross two membranes and are avidly linked to the cell wall.

Citation: Oikonomou C, Jensen G. 2019. Electron Cryotomography of Bacterial Secretion Systems, p 1-12. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0019-2018
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Electron Cryotomography of Bacterial Secretion Systems
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Citation: Oikonomou C, Jensen G. 2019. Electron Cryotomography of Bacterial Secretion Systems, p 1-12. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0019-2018
/content/10.1128/9781683670285.chap1.fig1-1
Figure 1
T2SS. ECT revealed the structures of the T4aP in and , enabling high-resolution structures to be placed into the map to produce a hypothetical model of the machine. Further studies revealed structural convergence of the related T4bP in and T2SS in , with a similar periplasmic ring (arrows) formed by nonhomologous proteins in each system. Note in this and subsequent figures how bacterial secretion systems often locally distort the cell envelope . Images are reprinted from the following with permission: panel A left and middle, reference ; panel A right, reference ; panel B, reference ; and panel C, reference .
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Figure 1

T2SS. ECT revealed the structures of the T4aP in and , enabling high-resolution structures to be placed into the map to produce a hypothetical model of the machine. Further studies revealed structural convergence of the related T4bP in and T2SS in , with a similar periplasmic ring (arrows) formed by nonhomologous proteins in each system. Note in this and subsequent figures how bacterial secretion systems often locally distort the cell envelope . Images are reprinted from the following with permission: panel A left and middle, reference ; panel A right, reference ; panel B, reference ; and panel C, reference .

Citation: Oikonomou C, Jensen G. 2019. Electron Cryotomography of Bacterial Secretion Systems, p 1-12. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0019-2018
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Figure 2
T3SS. ECT and subtomogram averaging revealed the structures of diverse T3SSs, including the flagellar motors of many bacteria (three examples, from , , and ) and the injectisome from Typhimurium . Structures shown from left to right: EMD-3154, EMD-3155, and EBD-3150 from reference and EMD-2667 from reference .
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Figure 2

T3SS. ECT and subtomogram averaging revealed the structures of diverse T3SSs, including the flagellar motors of many bacteria (three examples, from , , and ) and the injectisome from Typhimurium . Structures shown from left to right: EMD-3154, EMD-3155, and EBD-3150 from reference and EMD-2667 from reference .

Citation: Oikonomou C, Jensen G. 2019. Electron Cryotomography of Bacterial Secretion Systems, p 1-12. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0019-2018
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Figure 3
T4SS. ECT revealed the structure of the Dot/Icm T4SS, including a central channel extending from the inner membrane, and enabled components to be placed in the map. It also revealed the similar structure of the T4SS (inset), as well as novel, related OM tubes. Images are reprinted from the following with permission: panel A, reference (but see also reference ); panel B, reference .
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Image of Figure 3
Figure 3

T4SS. ECT revealed the structure of the Dot/Icm T4SS, including a central channel extending from the inner membrane, and enabled components to be placed in the map. It also revealed the similar structure of the T4SS (inset), as well as novel, related OM tubes. Images are reprinted from the following with permission: panel A, reference (but see also reference ); panel B, reference .

Citation: Oikonomou C, Jensen G. 2019. Electron Cryotomography of Bacterial Secretion Systems, p 1-12. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0019-2018
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Figure 4
T5SS. ECT revealed the stick-like form of the CDI T5SS (arrows) and helped elucidate its mechanism, in which half of CdiA extends out from the cell surface . Upon target binding, the remaining half of CdiA is exported to deliver the toxin to the target cell. Images reprinted with permission from reference .
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Figure 4

T5SS. ECT revealed the stick-like form of the CDI T5SS (arrows) and helped elucidate its mechanism, in which half of CdiA extends out from the cell surface . Upon target binding, the remaining half of CdiA is exported to deliver the toxin to the target cell. Images reprinted with permission from reference .

Citation: Oikonomou C, Jensen G. 2019. Electron Cryotomography of Bacterial Secretion Systems, p 1-12. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0019-2018
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Figure 5
T6SS. ECT revealed the contractile mechanism of the T6SS and its structure in . It also revealed higher-order arrays of T6SS in and a T6SS-related metamorphosis-associated contractile structure (MAC) in . Images are reprinted from the following with permission: panels A and B, reference ; panel D, reference .
10.1128/9781683670285/fig1-5_thmb.gif
10.1128/9781683670285/fig1-5.gif
Image of Figure 5
Figure 5

T6SS. ECT revealed the contractile mechanism of the T6SS and its structure in . It also revealed higher-order arrays of T6SS in and a T6SS-related metamorphosis-associated contractile structure (MAC) in . Images are reprinted from the following with permission: panels A and B, reference ; panel D, reference .

Citation: Oikonomou C, Jensen G. 2019. Electron Cryotomography of Bacterial Secretion Systems, p 1-12. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0019-2018
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References

/content/book/10.1128/9781683670285.chap1
1. Oikonomou CM,, Jensen GJ . 2017. Cellular electron cryotomography: toward structural biology in situ. Annu Rev Biochem 86 : 873– 896.[CrossRef]
2. Rapisarda C,, Tassinari M,, Gubellini F,, Fronzes R . 2018. Using cryo-EM to investigate bacterial secretion systems. Annu Rev Microbiol 72 : 231– 254.[CrossRef]
3. Kooger R,, Szwedziak P,, Böck D,, Pilhofer M . 2018. CryoEM of bacterial secretion systems. Curr Opin Struct Biol 52 : 64– 70.[CrossRef]
4. Costa TR,, Felisberto-Rodrigues C,, Meir A,, Prevost MS,, Redzej A,, Trokter M,, Waksman G . 2015. Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat Rev Microbiol 13 : 343– 359.[CrossRef]
5. Gold VA,, Salzer R,, Averhoff B,, Kühlbrandt W . 2015. Structure of a type IV pilus machinery in the open and closed state. eLife 4 : e07380.[CrossRef]
6. Chang YW,, Rettberg LA,, Treuner-Lange A,, Iwasa J,, Søgaard-Andersen L,, Jensen GJ . 2016. Architecture of the type IVa pilus machine. Science 351 : aad2001.[CrossRef]
7. Abendroth J,, Murphy P,, Sandkvist M,, Bagdasarian M,, Hol WG . 2005. The X-ray structure of the type II secretion system complex formed by the N-terminal domain of EpsE and the cytoplasmic domain of EpsL of Vibrio cholerae. J Mol Biol 348 : 845– 855.[CrossRef]
8. Craig L,, Volkmann N,, Arvai AS,, Pique ME,, Yeager M,, Egelman EH,, Tainer JA . 2006. Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions. Mol Cell 23 : 651– 662.[CrossRef]
9. Balasingham SV,, Collins RF,, Assalkhou R,, Homberset H,, Frye SA,, Derrick JP,, Tønjum T . 2007. Interactions between the lipoprotein PilP and the secretin PilQ in Neisseria meningitidis. J Bacteriol 189 : 5716– 5727.[CrossRef]
10. Yamagata A,, Tainer JA . 2007. Hexameric structures of the archaeal secretion ATPase GspE and implications for a universal secretion mechanism. EMBO J 26 : 878– 890.[CrossRef][PubMed]
11. Satyshur KA,, Worzalla GA,, Meyer LS,, Heiniger EK,, Aukema KG,, Misic AM,, Forest KT . 2007. Crystal structures of the pilus retraction motor PilT suggest large domain movements and subunit cooperation drive motility. Structure 15 : 363– 376.[CrossRef][PubMed]
12. Ayers M,, Sampaleanu LM,, Tammam S,, Koo J,, Harvey H,, Howell PL,, Burrows LL . 2009. PilM/N/O/P proteins form an inner membrane complex that affects the stability of the Pseudomonas aeruginosa type IV pilus secretin. J Mol Biol 394 : 128– 142.[CrossRef][PubMed]
13. Abendroth J,, Mitchell DD,, Korotkov KV,, Johnson TL,, Kreger A,, Sandkvist M,, Hol WG . 2009. The three-dimensional structure of the cytoplasmic domains of EpsF from the type 2 secretion system of Vibrio cholerae. J Struct Biol 166 : 303– 315.[CrossRef][PubMed]
14. Bulyha I,, Schmidt C,, Lenz P,, Jakovljevic V,, Höne A,, Maier B,, Hoppert M,, Søgaard-Andersen L . 2009. Regulation of the type IV pili molecular machine by dynamic localization of two motor proteins. Mol Microbiol 74 : 691– 706.[CrossRef][PubMed]
15. Sampaleanu LM,, Bonanno JB,, Ayers M,, Koo J,, Tammam S,, Burley SK,, Almo SC,, Burrows LL,, Howell PL . 2009. Periplasmic domains of Pseudomonas aeruginosa PilN and PilO form a stable heterodimeric complex. J Mol Biol 394 : 143– 159.[CrossRef][PubMed]
16. Misic AM,, Satyshur KA,, Forest KT . 2010. P. aeruginosa PilT structures with and without nucleotide reveal a dynamic type IV pilus retraction motor. J Mol Biol 400 : 1011– 1021.[CrossRef][PubMed]
17. Karuppiah V,, Hassan D,, Saleem M,, Derrick JP . 2010. Structure and oligomerization of the PilC type IV pilus biogenesis protein from Thermus thermophilus. Proteins 78 : 2049– 2057.[PubMed]
18. Karuppiah V,, Derrick JP . 2011. Structure of the PilM-PilN inner membrane type IV pilus biogenesis complex from Thermus thermophilus. J Biol Chem 286 : 24434– 24442.[CrossRef][PubMed]
19. Korotkov KV,, Johnson TL,, Jobling MG,, Pruneda J,, Pardon E,, Héroux A,, Turley S,, Steyaert J,, Holmes RK,, Sandkvist M,, Hol WG . 2011. Structural and functional studies on the interaction of GspC and GspD in the type II secretion system. PLoS Pathog 7 : e1002228.[CrossRef][PubMed]
20. Tammam S,, Sampaleanu LM,, Koo J,, Sundaram P,, Ayers M,, Chong PA,, Forman-Kay JD,, Burrows LL,, Howell PL . 2011. Characterization of the PilN, PilO and PilP type IVa pilus subcomplex. Mol Microbiol 82 : 1496– 1514.[CrossRef][PubMed]
21. Gu S,, Kelly G,, Wang X,, Frenkiel T,, Shevchik VE,, Pickersgill RW . 2012. Solution structure of homology region (HR) domain of type II secretion system. J Biol Chem 287 : 9072– 9080.[CrossRef][PubMed]
22. Georgiadou M,, Castagnini M,, Karimova G,, Ladant D,, Pelicic V . 2012. Large-scale study of the interactions between proteins involved in type IV pilus biology in Neisseria meningitidis: characterization of a subcomplex involved in pilus assembly. Mol Microbiol 84 : 857– 873.[CrossRef][PubMed]
23. Karuppiah V,, Collins RF,, Thistlethwaite A,, Gao Y,, Derrick JP . 2013. Structure and assembly of an inner membrane platform for initiation of type IV pilus biogenesis. Proc Natl Acad Sci U S A 110 : E4638– E4647.[CrossRef][PubMed]
24. Li C,, Wallace RA,, Black WP,, Li YZ,, Yang Z . 2013. Type IV pilus proteins form an integrated structure extending from the cytoplasm to the outer membrane. PLoS One 8 : e70144.[CrossRef][PubMed]
25. Lu C,, Turley S,, Marionni ST,, Park YJ,, Lee KK,, Patrick M,, Shah R,, Sandkvist M,, Bush MF,, Hol WG . 2013. Hexamers of the type II secretion ATPase GspE from Vibrio cholerae with increased ATPase activity. Structure 21 : 1707– 1717.[CrossRef][PubMed]
26. Tammam S,, Sampaleanu LM,, Koo J,, Manoharan K,, Daubaras M,, Burrows LL,, Howell PL . 2013. PilMNOPQ from the Pseudomonas aeruginosa type IV pilus system form a transenvelope protein interaction network that interacts with PilA. J Bacteriol 195 : 2126– 2135.[CrossRef][PubMed]
27. Friedrich C,, Bulyha I,, Søgaard-Andersen L . 2014. Outside-in assembly pathway of the type IV pilus system in Myxococcus xanthus. J Bacteriol 196 : 378– 390.[CrossRef][PubMed]
28. Siewering K,, Jain S,, Friedrich C,, Webber-Birungi MT,, Semchonok DA,, Binzen I,, Wagner A,, Huntley S,, Kahnt J,, Klingl A,, Boekema EJ,, Søgaard-Andersen L,, van der Does C . 2014. Peptidoglycan-binding protein TsaP functions in surface assembly of type IV pili. Proc Natl Acad Sci U S A 111 : E953– E961.[CrossRef][PubMed]
29. Chang YW,, Kjær A,, Ortega DR,, Kovacikova G,, Sutherland JA,, Rettberg LA,, Taylor RK,, Jensen GJ . 2017. Architecture of the Vibrio cholerae toxin-coregulated pilus machine revealed by electron cryotomography. Nat Microbiol 2 : 16269.[CrossRef][PubMed]
30. Thomassin JL,, Santos Moreno J,, Guilvout I,, Tran Van Nhieu G,, Francetic O . 2017. The trans-envelope architecture and function of the type 2 secretion system: new insights raising new questions. Mol Microbiol 105 : 211– 226.[CrossRef][PubMed]
31. Ghosal D,, Kim KW,, Zheng H,, Kaplan M,, Vogel JP,, Cianciotto NP,, Jensen GJ . 2019. In vivo structure of the Legionella type II secretion system by electron cryotomography. bioRxiv.[CrossRef]
32. Murphy GE,, Leadbetter JR,, Jensen GJ . 2006. In situ structure of the complete Treponema primitia flagellar motor. Nature 442 : 1062– 1064.[CrossRef][PubMed]
33. Berg HC . 2003. The rotary motor of bacterial flagella. Annu Rev Biochem 72 : 19– 54.[CrossRef][PubMed]
34. Macnab RM . 2003. How bacteria assemble flagella. Annu Rev Microbiol 57 : 77– 100.[CrossRef][PubMed]
35. DePamphilis ML,, Adler J . 1971. Fine structure and isolation of the hook-basal body complex of flagella from Escherichia coli and Bacillus subtilis. J Bacteriol 105 : 384– 395.[PubMed]
36. Stallmeyer MJ,, Aizawa S,, Macnab RM,, DeRosier DJ . 1989. Image reconstruction of the flagellar basal body of Salmonella typhimurium. J Mol Biol 205 : 519– 528.[CrossRef]
37. Francis NR,, Sosinsky GE,, Thomas D,, DeRosier DJ . 1994. Isolation, characterization and structure of bacterial flagellar motors containing the switch complex. J Mol Biol 235 : 1261– 1270.[CrossRef][PubMed]
38. Thomas DR,, Morgan DG,, DeRosier DJ . 1999. Rotational symmetry of the C ring and a mechanism for the flagellar rotary motor. Proc Natl Acad Sci U S A 96 : 10134– 10139.[CrossRef][PubMed]
39. Suzuki H,, Yonekura K,, Namba K . 2004. Structure of the rotor of the bacterial flagellar motor revealed by electron cryomicroscopy and single-particle image analysis. J Mol Biol 337 : 105– 113.[CrossRef][PubMed]
40. Thomas DR,, Francis NR,, Xu C,, DeRosier DJ . 2006. The three-dimensional structure of the flagellar rotor from a clockwise-locked mutant of Salmonella enterica serovar Typhimurium. J Bacteriol 188 : 7039– 7048.[CrossRef][PubMed]
41. Liu J,, Lin T,, Botkin DJ,, McCrum E,, Winkler H,, Norris SJ . 2009. Intact flagellar motor of Borrelia burgdorferi revealed by cryo-electron tomography: evidence for stator ring curvature and rotor/C-ring assembly flexion. J Bacteriol 191 : 5026– 5036.[CrossRef][PubMed]
42. Kudryashev M,, Cyrklaff M,, Wallich R,, Baumeister W,, Frischknecht F . 2010. Distinct in situ structures of the Borrelia flagellar motor. J Struct Biol 169 : 54– 61.[CrossRef][PubMed]
43. Abrusci P,, Vergara-Irigaray M,, Johnson S,, Beeby MD,, Hendrixson DR,, Roversi P,, Friede ME,, Deane JE,, Jensen GJ,, Tang CM,, Lea SM . 2013. Architecture of the major component of the type III secretion system export apparatus. Nat Struct Mol Biol 20 : 99– 104.[CrossRef][PubMed]
44. Chen S,, Beeby M,, Murphy GE,, Leadbetter JR,, Hendrixson DR,, Briegel A,, Li Z,, Shi J,, Tocheva EI,, Müller A,, Dobro MJ,, Jensen GJ . 2011. Structural diversity of bacterial flagellar motors. EMBO J 30 : 2972– 2981.[CrossRef][PubMed]
45. Beeby M,, Ribardo DA,, Brennan CA,, Ruby EG,, Jensen GJ,, Hendrixson DR . 2016. Diverse high-torque bacterial flagellar motors assemble wider stator rings using a conserved protein scaffold. Proc Natl Acad Sci U S A 113 : E1917– E1926.[CrossRef][PubMed]
46. Qin Z,, Lin WT,, Zhu S,, Franco AT,, Liu J . 2017. Imaging the motility and chemotaxis machineries in Helicobacter pylori by cryo-electron tomography. J Bacteriol 199 : e00695-16.[PubMed]
47. Chaban B,, Coleman I,, Beeby M . 2018. Evolution of higher torque in Campylobacter-type bacterial flagellar motors. Sci Rep 8 : 97.[CrossRef][PubMed]
48. Kaplan M,, Ghosal D,, Subramanian P,, Oikonomou CM,, Kjaer A,, Pirbadian S,, Ortega DR,, Briegel A,, El-Naggar MY,, Jensen GJ . 2019. The presence and absence of periplasmic rings in bacterial flagellar motors correlates with stator type. eLife 8 : e43487.[CrossRef][PubMed]
49. Zhu S,, Nishikino T,, Hu B,, Kojima S,, Homma M,, Liu J . 2017. Molecular architecture of the sheathed polar flagellum in Vibrio alginolyticus. Proc Natl Acad Sci U S A 114 : 10966– 10971.[CrossRef][PubMed]
50. Galán JE,, Lara-Tejero M,, Marlovits TC,, Wagner S . 2014. Bacterial type III secretion systems: specialized nanomachines for protein delivery into target cells. Annu Rev Microbiol 68 : 415– 438.[CrossRef][PubMed]
51. Diepold A,, Armitage JP . 2015. Type III secretion systems: the bacterial flagellum and the injectisome. Philos Trans R Soc Lond B Biol Sci 370 : 20150020.[CrossRef][PubMed]
52. Hu B,, Morado DR,, Margolin W,, Rohde JR,, Arizmendi O,, Picking WL,, Picking WD,, Liu J . 2015. Visualization of the type III secretion sorting platform of Shigella flexneri. Proc Natl Acad Sci U S A 112 : 1047– 1052.[CrossRef][PubMed]
53. Hu B,, Lara-Tejero M,, Kong Q,, Galan JE,, Liu J . 2017. In situ molecular architecture of the Salmonella type III secretion machine. Cell 168 : 1065– 1074.e1010.[PubMed]
54. Wagner S,, Königsmaier L,, Lara-Tejero M,, Lefebre M,, Marlovits TC,, Galán JE . 2010. Organization and coordinated assembly of the type III secretion export apparatus. Proc Natl Acad Sci U S A 107 : 17745– 17750.[CrossRef][PubMed]
55. Park D,, Lara-Tejero M,, Waxham MN,, Li W,, Hu B,, Galán JE,, Liu J . 2018. Visualization of the type III secretion mediated Salmonella-host cell interface using cryo-electron tomography. eLife 7 : e39514.[CrossRef][PubMed]
56. Ide T,, Laarmann S,, Greune L,, Schillers H,, Oberleithner H,, Schmidt MA . 2001. Characterization of translocation pores inserted into plasma membranes by type III-secreted Esp proteins of enteropathogenic Escherichia coli. Cell Microbiol 3 : 669– 679.[CrossRef][PubMed]
57. Low HH,, Gubellini F,, Rivera-Calzada A,, Braun N,, Connery S,, Dujeancourt A,, Lu F,, Redzej A,, Fronzes R,, Orlova EV,, Waksman G . 2014. Structure of a type IV secretion system. Nature 508 : 550– 553.[CrossRef][PubMed]
58. Frick-Cheng AE,, Pyburn TM,, Voss BJ,, McDonald WH,, Ohi MD,, Cover TL . 2016. Molecular and structural analysis of the Helicobacter pylori cag type IV secretion system core complex. mBio 7 : e02001-15.[CrossRef][PubMed]
59. Chetrit D,, Hu B,, Christie PJ,, Roy CR,, Liu J . 2018. A unique cytoplasmic ATPase complex defines the Legionella pneumophila type IV secretion channel. Nat Microbiol 3 : 678– 686.[CrossRef][PubMed]
60. Ghosal D,, Chang YW,, Jeong KC,, Vogel JP,, Jensen GJ . 2018. Molecular architecture of the Legionella Dot/Icm type IV secretion system. bioRxiv.[CrossRef]
61. Chang YW,, Shaffer CL,, Rettberg LA,, Ghosal D,, Jensen GJ . 2018. In vivo structures of the Helicobacter pylori cag type IV secretion system. Cell Rep 23 : 673– 681.[CrossRef][PubMed]
62. Ensminger AW . 2016. Legionella pneumophila, armed to the hilt: justifying the largest arsenal of effectors in the bacterial world. Curr Opin Microbiol 29 : 74– 80.[CrossRef][PubMed]
63. Aoki SK,, Pamma R,, Hernday AD,, Bickham JE,, Braaten BA,, Low DA . 2005. Contact-dependent inhibition of growth in Escherichia coli. Science 309 : 1245– 1248.[CrossRef][PubMed]
64. Aoki SK,, Malinverni JC,, Jacoby K,, Thomas B,, Pamma R,, Trinh BN,, Remers S,, Webb J,, Braaten BA,, Silhavy TJ,, Low DA . 2008. Contact-dependent growth inhibition requires the essential outer membrane protein BamA (YaeT) as the receptor and the inner membrane transport protein AcrB. Mol Microbiol 70 : 323– 340.[CrossRef][PubMed]
65. Ruhe ZC,, Nguyen JY,, Xiong J,, Koskiniemi S,, Beck CM,, Perkins BR,, Low DA,, Hayes CS . 2017. CdiA effectors use modular receptor-binding domains to recognize target bacteria. mBio 8 : e00290-17.[CrossRef][PubMed]
66. Ruhe ZC,, Subramanian P,, Song K,, Nguyen JY,, Stevens TA,, Low DA,, Jensen GJ,, Hayes CS . 2018. Programmed secretion arrest and receptor-triggered toxin export during antibacterial contact-dependent growth inhibition. Cell 175 : 921– 933.e14.[CrossRef][PubMed]
67. MacIntyre DL,, Miyata ST,, Kitaoka M,, Pukatzki S . 2010. The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proc Natl Acad Sci U S A 107 : 19520– 19524.[CrossRef][PubMed]
68. Basler M,, Pilhofer M,, Henderson GP,, Jensen GJ,, Mekalanos JJ . 2012. Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483 : 182– 186.[CrossRef][PubMed]
69. Bönemann G,, Pietrosiuk A,, Mogk A . 2010. Tubules and donuts: a type VI secretion story. Mol Microbiol 76 : 815– 821.[CrossRef][PubMed]
70. Chang YW,, Rettberg LA,, Ortega DR,, Jensen GJ . 2017. In vivo structures of an intact type VI secretion system revealed by electron cryotomography. EMBO Rep 18 : 1090– 1099.[CrossRef][PubMed]
71. Rapisarda C,, Cherrak Y,, Kooger R,, Schmidt V,, Pellarin R,, Logger L,, Cascales E,, Pilhofer M,, Durand E,, Fronzes R . 2018. In situ and high-resolution cryo-EM structure of the type VI secretion membrane complex. bioRxiv.[CrossRef]
72. Shikuma NJ,, Pilhofer M,, Weiss GL,, Hadfield MG,, Jensen GJ,, Newman DK . 2014. Marine tubeworm metamorphosis induced by arrays of bacterial phage tail-like structures. Science 343 : 529– 533.[CrossRef][PubMed]
73. Medeiros JM,, Böck D,, Pilhofer M . 2018. Imaging bacteria inside their host by cryo-focused ion beam milling and electron cryotomography. Curr Opin Microbiol 43 : 62– 68.[CrossRef][PubMed]
74. Böck D,, Medeiros JM,, Tsao HF,, Penz T,, Weiss GL,, Aistleitner K,, Horn M,, Pilhofer M . 2017. In situ architecture, function, and evolution of a contractile injection system. Science 357 : 713– 717.[CrossRef][PubMed]

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