Chapter 10 : The Dynamic Structures of the Type IV Pilus

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The fundamental type IVa pilus (T4aP)-like architecture includes a retractable pilus fiber, a motor, an alignment subcomplex, and—in Gram-negative bacteria—an outer membrane secretin pore ( Fig. 1 ). The pilus is an extracellular polymer of pilins. Pilins subunits are stored in the inner membrane and the motor powers their polymerization (extension) and depolymerization (retraction) at the pilus base. The alignment subcomplex connects the secretin with the motor and controls pilus dynamics. Finally, the secretin pore allows the pilus to extend through the outer membrane. Since publication of previous T4aP reviews ( ), discoveries made using cryo-electron microscopy (cryo-EM), cryo-electron tomography (cryo-ET), X-ray crystallography, and nuclear magnetic resonance (NMR) have dramatically reshaped our understanding of T4P-like systems. Here we put these discoveries in context with the structure and function of the T4aP, using the T4aP system nomenclature.

Citation: McCallum M, Burrows L, Howell P. 2019. The Dynamic Structures of the Type IV Pilus, p 113-128. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0006-2018
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Figure 1

Subcomplexes of the T4aP. The protein structures portrayed reflect the full-length structure predictions and their predicted location in the T4aP. This figure is largely consistent with the previously published working model of the T4aP ( ). Due to limited information, there is uncertainty regarding the locations of PilF, TsaP, PilY1, and the minor pilins.

Citation: McCallum M, Burrows L, Howell P. 2019. The Dynamic Structures of the Type IV Pilus, p 113-128. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0006-2018
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Image of Figure 2
Figure 2

The structures of the type IV pilus. The four subcomplexes are split into four quadrants, which are further subdivided into individual proteins in boxes colored to correspond to Fig. 1 . In the linear domain architecture, domains are displayed to scale as blocks colored to indicate known structures (rainbow colors), segments with high-confidence structure predictions (gray), unknown structures (white), transmembrane segments (diagonal bars), hydrolyzed signal peptides (black), or predicted/known disorder (black line). The known or predicted domain name is written; if a domain has no name, it could not be predicted. In the black outlined cartoon structures, a black outline of the predicted ( ) full-length homology model is shown to scale for reference. Known structures are displayed as cartoons in rainbow colors corresponding to the colors shown in the linear domain architecture. A short description of the rainbow-colored cartoon structure and the PDB accession code are written in black font. Since the black outline is a structure prediction while the cartoons correspond to structures sometimes determined in other species, the black outline and cartoons may not fully match. Note that the PDB coordinate file for PilQ from (marked with an asterisk) was obtained from the authors of reference and used here with their permission; only the secretin and adjacent N1 domain (N5 in ) are shown here, as the other PilQ domains are divergent or atypical compared to those in . (The N1 domain is also named N2, N3, N4, or N5 in systems or species where the N1 domain is duplicated.) No black outline is shown for FimV, as high-confidence structure prediction was not possible for most of this component. Unexpectedly, most of TsaP was predicted ( ) with high confidence to be structurally similar to the protein with PDB code 3SLU. Gray boxes note interesting features of the protein or other relevant structures; structures in gray boxes are not to scale.

Citation: McCallum M, Burrows L, Howell P. 2019. The Dynamic Structures of the Type IV Pilus, p 113-128. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0006-2018
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1. Craig L,, Li J . 2008. Type IV pili: paradoxes in form and function. Curr Opin Struct Biol 18 : 267 277.[CrossRef][PubMed]
2. Leighton TL,, Buensuceso RN,, Howell PL,, Burrows LL . 2015. Biogenesis of Pseudomonas aeruginosa type IV pili and regulation of their function. Environ Microbiol 17 : 4148 4163.[CrossRef][PubMed]
3. Ayers M,, Howell PL,, Burrows LL . 2010. Architecture of the type II secretion and type IV pilus machineries. Future Microbiol 5 : 1203 1218.[CrossRef][PubMed]
4. Hospenthal MK,, Costa TRD,, Waksman G . 2017. A comprehensive guide to pilus biogenesis in Gram-negative bacteria. Nat Rev Microbiol 15 : 365 379.[CrossRef][PubMed]
5. Nguyen Y,, Jackson SG,, Aidoo F,, Junop M,, Burrows LL . 2010. Structural characterization of novel Pseudomonas aeruginosa type IV pilins. J Mol Biol 395 : 491 503.[CrossRef][PubMed]
6. Craig L,, Taylor RK,, Pique ME,, Adair BD,, Arvai AS,, Singh M,, Lloyd SJ,, Shin DS,, Getzoff ED,, Yeager M,, Forest KT,, Tainer JA . 2003. Type IV pilin structure and assembly: X-ray and EM analyses of Vibrio cholerae toxin-coregulated pilus and Pseudomonas aeruginosa PAK pilin. Mol Cell 11 : 1139 1150.[CrossRef]
7. 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][PubMed]
8. Piepenbrink KH,, Lillehoj E,, Harding CM,, Labonte JW,, Zuo X,, Rapp CA,, Munson RS Jr,, Goldblum SE,, Feldman MF,, Gray JJ,, Sundberg EJ . 2016. Structural diversity in the type IV pili of multidrug-resistant Acinetobacter. J Biol Chem 291 : 22924 22935.[CrossRef][PubMed]
9. Piepenbrink KH,, Maldarelli GA,, Martinez de la Peña CF,, Dingle TC,, Mulvey GL,, Lee A,, von Rosenvinge E,, Armstrong GD,, Donnenberg MS,, Sundberg EJ . 2015. Structural and evolutionary analyses show unique stabilization strategies in the type IV pili of Clostridium difficile. Structure 23 : 385 396.[CrossRef][PubMed]
10. Hartung S,, Arvai AS,, Wood T,, Kolappan S,, Shin DS,, Craig L,, Tainer JA . 2011. Ultrahigh resolution and full-length pilin structures with insights for filament assembly, pathogenic functions, and vaccine potential. J Biol Chem 286 : 44254 44265.[CrossRef][PubMed]
11. Kao DJ,, Churchill ME,, Irvin RT,, Hodges RS . 2007. Animal protection and structural studies of a consensus sequence vaccine targeting the receptor binding domain of the type IV pilus of Pseudomonas aeruginosa. J Mol Biol 374 : 426 442.[CrossRef][PubMed]
12. Hazes B,, Sastry PA,, Hayakawa K,, Read RJ,, Irvin RT . 2000. Crystal structure of Pseudomonas aeruginosa PAK pilin suggests a main-chain-dominated mode of receptor binding. J Mol Biol 299 : 1005 1017.[CrossRef][PubMed]
13. Parge HE,, Forest KT,, Hickey MJ,, Christensen DA,, Getzoff ED,, Tainer JA . 1995. Structure of the fibre-forming protein pilin at 2.6 A resolution. Nature 378 : 32 38.[CrossRef][PubMed]
14. Audette GF,, Irvin RT,, Hazes B . 2004. Crystallographic analysis of the Pseudomonas aeruginosa strain K122-4 monomeric pilin reveals a conserved receptor-binding architecture. Biochemistry 43 : 11427 11435.[CrossRef][PubMed]
15. Gorgel M,, Ulstrup JJ,, Bøggild A,, Jones NC,, Hoffmann SV,, Nissen P,, Boesen T . 2015. High-resolution structure of a type IV pilin from the metal-reducing bacterium Shewanella oneidensis. BMC Struct Biol 15 : 4.[CrossRef][PubMed]
16. Karuppiah V,, Thistlethwaite A,, Derrick JP . 2016. Structures of type IV pilins from Thermus thermophilus demonstrate similarities with type II secretion system pseudopilins. J Struct Biol 196 : 375 384.[CrossRef][PubMed]
17. Dunlop KV,, Irvin RT,, Hazes B . 2005. Pros and cons of cryocrystallography: should we also collect a room-temperature data set? Acta Crystallogr D Biol Crystallogr 61 : 80 87.[CrossRef][PubMed]
18. Forest KT,, Dunham SA,, Koomey M,, Tainer JA . 1999. Crystallographic structure reveals phosphorylated pilin from Neisseria: phosphoserine sites modify type IV pilus surface chemistry and fibre morphology. Mol Microbiol 31 : 743 752.[CrossRef][PubMed]
19. Reardon PN,, Mueller KT . 2013. Structure of the type IVa major pilin from the electrically conductive bacterial nanowires of Geobacter sulfurreducens. J Biol Chem 288 : 29260 29266.[CrossRef][PubMed]
20. Nguyen Y,, Boulton S,, McNicholl ET,, Akimoto M,, Harvey H,, Aidoo F,, Melacini G,, Burrows LL . 2018. A highly dynamic loop of the Pseudomonas aeruginosa PA14 type IV pilin is essential for pilus assembly. ACS Infect Dis 4 : 936 943.[CrossRef][PubMed]
21. Keizer DW,, Slupsky CM,, Kalisiak M,, Campbell AP,, Crump MP,, Sastry PA,, Hazes B,, Irvin RT,, Sykes BD . 2001. Structure of a pilin monomer from Pseudomonas aeruginosa: implications for the assembly of pili. J Biol Chem 276 : 24186 24193.[CrossRef][PubMed]
22. Hegge FT,, Hitchen PG,, Aas FE,, Kristiansen H,, Løvold C,, Egge-Jacobsen W,, Panico M,, Leong WY,, Bull V,, Virji M,, Morris HR,, Dell A,, Koomey M . 2004. Unique modifications with phosphocholine and phosphoethanolamine define alternate antigenic forms of Neisseria gonorrhoeae type IV pili. Proc Natl Acad Sci USA 101 : 10798 10803.[CrossRef][PubMed]
23. Jennings MP,, Jen FE,, Roddam LF,, Apicella MA,, Edwards JL . 2011. Neisseria gonorrhoeae pilin glycan contributes to CR3 activation during challenge of primary cervical epithelial cells. Cell Microbiol 13 : 885 896.[CrossRef][PubMed]
24. Harvey H,, Bondy-Denomy J,, Marquis H,, Sztanko KM,, Davidson AR,, Burrows LL . 2018. Pseudomonas aeruginosa defends against phages through type IV pilus glycosylation. Nat Microbiol 3 : 47 52.[CrossRef][PubMed]
25. Gault J,, Ferber M,, Machata S,, Imhaus AF,, Malosse C,, Charles-Orszag A,, Millien C,, Bouvier G,, Bardiaux B,, Péhau-Arnaudet G,, Klinge K,, Podglajen I,, Ploy MC,, Seifert HS,, Nilges M,, Chamot-Rooke J,, Duménil G . 2015. Neisseria meningitidis type IV pili composed of sequence invariable pilins are masked by multisite glycosylation. PLoS Pathog 11 : e1005162.[CrossRef][PubMed]
26. Tan RM,, Kuang Z,, Hao Y,, Lee F,, Lee T,, Lee RJ,, Lau GW . 2015. Type IV pilus glycosylation mediates resistance of Pseudomonas aeruginosa to opsonic activities of the pulmonary surfactant protein A. Infect Immun 83 : 1339 1346.[CrossRef][PubMed]
27. Kus JV,, Kelly J,, Tessier L,, Harvey H,, Cvitkovitch DG,, Burrows LL . 2008. Modification of Pseudomonas aeruginosa Pa5196 type IV pilins at multiple sites with d-Ara f by a novel GT-C family arabinosyltransferase, TfpW. J Bacteriol 190 : 7464 7478.[CrossRef][PubMed]
28. LaPointe CF,, Taylor RK . 2000. The type 4 prepilin peptidases comprise a novel family of aspartic acid proteases. J Biol Chem 275 : 1502 1510.[CrossRef]
29. Kolappan S,, Coureuil M,, Yu X,, Nassif X,, Egelman EH,, Craig L . 2016. Structure of the Neisseria meningitidis type IV pilus. Nat Commun 7 : 13015.[CrossRef][PubMed]
30. Wang F,, Coureuil M,, Osinski T,, Orlova A,, Altindal T,, Gesbert G,, Nassif X,, Egelman EH,, Craig L . 2017. Cryoelectron microscopy reconstructions of the Pseudomonas aeruginosa and Neisseria gonorrhoeae type IV pili at sub-nanometer resolution. Structure 25 : 1423 1435.e4.[CrossRef][PubMed]
31. Folkhard W,, Marvin DA,, Watts TH,, Paranchych W . 1981. Structure of polar pili from Pseudomonas aeruginosa strains K and O. J Mol Biol 149 : 79 93.[CrossRef]
32. Egelman EH . 2017. Cryo-EM of bacterial pili and archaeal flagellar filaments. Curr Opin Struct Biol 46 : 31 37.[CrossRef][PubMed]
33. Watts TH,, Scraba DG,, Paranchych W . 1982. Formation of 9-nm filaments from pilin monomers obtained by octyl-glucoside dissociation of Pseudomonas aeruginosa pili. J Bacteriol 151 : 1508 1513.[PubMed]
34. Ingber DE,, Wang N,, Stamenovic D . 2014. Tensegrity, cellular biophysics, and the mechanics of living systems. Rep Prog Phys 77 : 046603.[CrossRef][PubMed]
35. Ellison CK,, Dalia TN,, Vidal Ceballos A,, Wang JC,, Biais N,, Brun YV,, Dalia AB . 2018. Retraction of DNA-bound type IV competence pili initiates DNA uptake during natural transformation in Vibrio cholerae. Nat Microbiol 3 : 773 780.[CrossRef][PubMed]
36. de Haan HW . 2016. Modeling and simulating the dynamics of type IV pili extension of Pseudomonas aeruginosa. Biophys J 111 : 2263 2273.[CrossRef][PubMed]
37. Piepenbrink KH,, Maldarelli GA,, de la Peña CF,, Mulvey GL,, Snyder GA,, De Masi L,, von Rosenvinge EC,, Günther S,, Armstrong GD,, Donnenberg MS,, Sundberg EJ . 2014. Structure of Clostridium difficile PilJ exhibits unprecedented divergence from known type IV pilins. J Biol Chem 289 : 4334 4345.[CrossRef][PubMed]
38. Berry JL,, Xu Y,, Ward PN,, Lea SM,, Matthews SJ,, Pelicic V . 2016. A comparative structure/function analysis of two type IV pilin DNA receptors defines a novel mode of DNA binding. Structure 24 : 926 934.[CrossRef][PubMed]
39. Nguyen Y,, Sugiman-Marangos S,, Harvey H,, Bell SD,, Charlton CL,, Junop MS,, Burrows LL . 2015. Pseudomonas aeruginosa minor pilins prime type IVa pilus assembly and promote surface display of the PilY1 adhesin. J Biol Chem 290 : 601 611.[CrossRef][PubMed]
40. Nguyen Y,, Harvey H,, Sugiman-Marangos S,, Bell SD,, Buensuceso RN,, Junop MS,, Burrows LL . 2015. Structural and functional studies of the Pseudomonas aeruginosa minor pilin, PilE. J Biol Chem 290 : 26856 26865.[CrossRef][PubMed]
41. Korotkov KV,, Hol WG . 2008. Structure of the GspK-GspI-GspJ complex from the enterotoxigenic Escherichia coli type 2 secretion system. Nat Struct Mol Biol 15 : 462 468.[CrossRef][PubMed]
42. Cisneros DA,, Bond PJ,, Pugsley AP,, Campos M,, Francetic O . 2012. Minor pseudopilin self-assembly primes type II secretion pseudopilus elongation. EMBO J 31 : 1041 1053.[CrossRef][PubMed]
43. 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][PubMed]
44. Giltner CL,, Habash M,, Burrows LL . 2010. Pseudomonas aeruginosa minor pilins are incorporated into type IV pili. J Mol Biol 398 : 444 461.[CrossRef][PubMed]
45. Helaine S,, Dyer DH,, Nassif X,, Pelicic V,, Forest KT . 2007. 3D structure/function analysis of PilX reveals how minor pilins can modulate the virulence properties of type IV pili. Proc Natl Acad Sci U S A 104 : 15888 15893.[CrossRef][PubMed]
46. Wolfgang M,, van Putten JP,, Hayes SF,, Koomey M . 1999. The comP locus of Neisseria gonorrhoeae encodes a type IV prepilin that is dispensable for pilus biogenesis but essential for natural transformation. Mol Microbiol 31 : 1345 1357.[CrossRef][PubMed]
47. Brown DR,, Helaine S,, Carbonnelle E,, Pelicic V . 2010. Systematic functional analysis reveals that a set of seven genes is involved in fine-tuning of the multiple functions mediated by type IV pili in Neisseria meningitidis. Infect Immun 78 : 3053 3063.[CrossRef][PubMed]
48. Cehovin A,, Simpson PJ,, McDowell MA,, Brown DR,, Noschese R,, Pallett M,, Brady J,, Baldwin GS,, Lea SM,, Matthews SJ,, Pelicic V . 2013. Specific DNA recognition mediated by a type IV pilin. Proc Natl Acad Sci U S A 110 : 3065 3070.[CrossRef][PubMed]
49. Johnson MD,, Garrett CK,, Bond JE,, Coggan KA,, Wolfgang MC,, Redinbo MR . 2011. Pseudomonas aeruginosa PilY1 binds integrin in an RGD- and calcium-dependent manner. PLoS One 6 : e29629.[CrossRef][PubMed]
50. Rudel T,, Scheurerpflug I,, Meyer TF . 1995. Neisseria PilC protein identified as type-4 pilus tip-located adhesin. Nature 373 : 357 359.[CrossRef][PubMed]
51. Orans J,, Johnson MD,, Coggan KA,, Sperlazza JR,, Heiniger RW,, Wolfgang MC,, Redinbo MR . 2010. Crystal structure analysis reveals Pseudomonas PilY1 as an essential calcium-dependent regulator of bacterial surface motility. Proc Natl Acad Sci U S A 107 : 1065 1070.[CrossRef][PubMed]
52. Cheng Y,, Johnson MD,, Burillo-Kirch C,, Mocny JC,, Anderson JE,, Garrett CK,, Redinbo MR,, Thomas CE . 2013. Mutation of the conserved calcium-binding motif in Neisseria gonorrhoeae PilC1 impacts adhesion but not piliation. Infect Immun 81 : 4280 4289.[CrossRef][PubMed]
53. Takhar HK,, Kemp K,, Kim M,, Howell PL,, Burrows LL . 2013. The platform protein is essential for type IV pilus biogenesis. J Biol Chem 288 : 9721 9728.[CrossRef][PubMed]
54. 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]
55. McCallum M,, Tammam S,, Little DJ,, Robinson H,, Koo J,, Shah M,, Calmettes C,, Moraes TF,, Burrows LL,, Howell PL . 2016. PilN binding modulates the structure and binding partners of the Pseudomonas aeruginosa type IVa pilus protein PilM. J Biol Chem 291 : 11003 11015.[CrossRef][PubMed]
56. 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]
57. Bischof LF,, Friedrich C,, Harms A,, Søgaard-Andersen L,, van der Does C . 2016. The type IV pilus assembly ATPase PilB of Myxococcus xanthus interacts with the inner membrane platform protein PilC and the nucleotide-binding protein PilM. J Biol Chem 291 : 6946 6957.[CrossRef][PubMed]
58. Collins RF,, Saleem M,, Derrick JP . 2007. Purification and three-dimensional electron microscopy structure of the Neisseria meningitidis type IV pilus biogenesis protein PilG. J Bacteriol 189 : 6389 6396.[CrossRef][PubMed]
59. Mancl JM,, Black WP,, Robinson H,, Yang Z,, Schubot FD . 2016. Crystal structure of a type IV pilus assembly ATPase: insights into the molecular mechanism of PilB from Thermus thermophilus. Structure 24 : 1886 1897.[CrossRef][PubMed]
60. McCallum M,, Tammam S,, Khan A,, Burrows LL,, Howell PL . 2017. The molecular mechanism of the type IVa pilus motors. Nat Commun 8 : 15091.[CrossRef][PubMed]
61. Solanki V,, Kapoor S,, Thakur KG . 2018. Structural insights into the mechanism of type IVa pilus extension and retraction ATPase motors. FEBS J 285 : 3402 3421.[CrossRef][PubMed]
62. Collins R,, Karuppiah V,, Siebert CA,, Dajani R,, Thistlethwaite A,, Derrick JP . 2018. Structural cycle of the Thermus thermophilus PilF ATPase: the powering of type IVa pilus assembly. Sci Rep 8 : 14022.[CrossRef][PubMed]
63. Kinosita Y,, Uchida N,, Nakane D,, Nishizaka T . 2016. Direct observation of rotation and steps of the archaellum in the swimming halophilic archaeon Halobacterium salinarum. Nat Microbiol 1 : 16148.[CrossRef][PubMed]
64. Reindl S,, Ghosh A,, Williams GJ,, Lassak K,, Neiner T,, Henche AL,, Albers SV,, Tainer JA . 2013. Insights into FlaI functions in archaeal motor assembly and motility from structures, conformations, and genetics. Mol Cell 49 : 1069 1082.[CrossRef][PubMed]
65. Alam M,, Oesterhelt D . 1984. Morphology, function and isolation of halobacterial flagella. J Mol Biol 176 : 459 475.[CrossRef]
66. Marwan W,, Alam M,, Oesterhelt D . 1991. Rotation and switching of the flagellar motor assembly in Halobacterium halobium. J Bacteriol 173 : 1971 1977.[CrossRef][PubMed]
67. Shahapure R,, Driessen RP,, Haurat MF,, Albers SV,, Dame RT . 2014. The archaellum: a rotating type IV pilus. Mol Microbiol 91 : 716 723.[CrossRef][PubMed]
68. Chaudhury P,, van der Does C,, Albers SV . 2018. Characterization of the ATPase FlaI of the motor complex of the Pyrococcus furiosus archaellum and its interactions between the ATP-binding protein FlaH. Peer J 6 : e4984.[CrossRef][PubMed]
69. Wang YC,, Chin KH,, Tu ZL,, He J,, Jones CJ,, Sanchez DZ,, Yildiz FH,, Galperin MY,, Chou SH . 2016. Nucleotide binding by the widespread high-affinity cyclic di-GMP receptor MshEN domain. Nat Commun 7 : 12481.[CrossRef][PubMed]
70. Hendrick WA,, Orr MW,, Murray SR,, Lee VT,, Melville SB . 2017. Cyclic di-GMP binding by an assembly ATPase (PilB2) and control of type IV pilin polymerization in the Gram-positive pathogen Clostridium perfringens. J Bacteriol 199 : e00034-17.[CrossRef][PubMed]
71. Jones CJ,, Utada A,, Davis KR,, Thongsomboon W,, Zamorano Sanchez D,, Banakar V,, Cegelski L,, Wong GC,, Yildiz FH . 2015. C-di-GMP regulates motile to sessile transition by modulating MshA pili biogenesis and near-surface motility behavior in Vibrio cholerae. PLoS Pathog 11 : e1005068.[CrossRef][PubMed]
72. Lu C,, Korotkov KV,, Hol WGJ . 2014. Crystal structure of the full-length ATPase GspE from the Vibrio vulnificus type II secretion system in complex with the cytoplasmic domain of GspL. J Struct Biol 187 : 223 235.[CrossRef][PubMed]
73. 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][PubMed]
74. Jain R,, Sliusarenko O,, Kazmierczak BI . 2017. Interaction of the cyclic-di-GMP binding protein FimX and the type 4 pilus assembly ATPase promotes pilus assembly. PLoS Pathog 13 : e1006594.[CrossRef][PubMed]
75. Guzzo CR,, Salinas RK,, Andrade MO,, Farah CS . 2009. PILZ protein structure and interactions with PILB and the FIMX EAL domain: implications for control of type IV pilus biogenesis. J Mol Biol 393 : 848 866.[CrossRef][PubMed]
76. Chin KH,, Kuo WT,, Yu YJ,, Liao YT,, Yang MT,, Chou SH . 2012. Structural polymorphism of c-di-GMP bound to an EAL domain and in complex with a type II PilZ-domain protein. Acta Crystallogr D Biol Crystallogr 68 : 1380 1392.[CrossRef][PubMed]
77. Merz AJ,, So M,, Sheetz MP . 2000. Pilus retraction powers bacterial twitching motility. Nature 407 : 98 102.[CrossRef][PubMed]
78. Maier B,, Potter L,, So M,, Long CD,, Seifert HS,, Sheetz MP . 2002. Single pilus motor forces exceed 100 pN. Proc Natl Acad Sci U S A 99 : 16012 16017.[CrossRef][PubMed]
79. Clausen M,, Koomey M,, Maier B . 2009. Dynamics of type IV pili is controlled by switching between multiple states. Biophys J 96 : 1169 1177.[CrossRef][PubMed]
80. Beaussart A,, Baker AE,, Kuchma SL,, El-Kirat-Chatel S,, O’Toole GA,, Dufrêne YF . 2014. Nanoscale adhesion forces of Pseudomonas aeruginosa type IV pili. ACS Nano 8 : 10723 10733.[CrossRef][PubMed]
81. Clausen M,, Jakovljevic V,, Søgaard-Andersen L,, Maier B . 2009. High-force generation is a conserved property of type IV pilus systems. J Bacteriol 191 : 4633 4638.[CrossRef][PubMed]
82. Chiang P,, Habash M,, Burrows LL . 2005. Disparate subcellular localization patterns of Pseudomonas aeruginosa type IV pilus ATPases involved in twitching motility. J Bacteriol 187 : 829 839.[CrossRef][PubMed]
83. Chiang P,, Sampaleanu LM,, Ayers M,, Pahuta M,, Howell PL,, Burrows LL . 2008. Functional role of conserved residues in the characteristic secretion NTPase motifs of the Pseudomonas aeruginosa type IV pilus motor proteins PilB, PilT and PilU. Microbiology 154 : 114 126.[CrossRef][PubMed]
84. Kurre R,, Höne A,, Clausen M,, Meel C,, Maier B . 2012. PilT2 enhances the speed of gonococcal type IV pilus retraction and of twitching motility. Mol Microbiol 86 : 857 865.[CrossRef][PubMed]
85. Bradley DE . 1972. Shortening of Pseudomonas aeruginosa pili after RNA-phage adsorption. J Gen Microbiol 72 : 303 319.[CrossRef][PubMed]
86. Wolfgang M,, Lauer P,, Park HS,, Brossay L,, Hébert J,, Koomey M . 1998. PilT mutations lead to simultaneous defects in competence for natural transformation and twitching motility in piliated Neisseria gonorrhoeae. Mol Microbiol 29 : 321 330.[CrossRef][PubMed]
87. Forest KT,, Satyshur KA,, Worzalla GA,, Hansen JK,, Herdendorf TJ . 2004. The pilus-retraction protein PilT: ultrastructure of the biological assembly. Acta Crystallogr D Biol Crystallogr 60 : 978 982.[CrossRef][PubMed]
88. 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]
89. 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]
90. Ng D,, Harn T,, Altindal T,, Kolappan S,, Marles JM,, Lala R,, Spielman I,, Gao Y,, Hauke CA,, Kovacikova G,, Verjee Z,, Taylor RK,, Biais N,, Craig L . 2016. The Vibrio cholerae minor pilin TcpB initiates assembly and retraction of the toxin-coregulated pilus. PLoS Pathog 12 : e1006109.[CrossRef][PubMed]
91. Ellison CK,, Kan J,, Dillard RS,, Kysela DT,, Ducret A,, Berne C,, Hampton CM,, Ke Z,, Wright ER,, Biais N,, Dalia AB,, Brun YV . 2017. Obstruction of pilus retraction stimulates bacterial surface sensing. Science 358 : 535 538.[CrossRef][PubMed]
92. 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]
93. Abendroth J,, Bagdasarian M,, Sandkvist M,, Hol WG . 2004. The structure of the cytoplasmic domain of EpsL, an inner membrane component of the type II secretion system of Vibrio cholerae: an unusual member of the actin-like ATPase superfamily. J Mol Biol 344 : 619 633.[CrossRef][PubMed]
94. 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]
95. 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]
96. Leighton TL,, Mok MC,, Junop MS,, Howell PL,, Burrows LL . 2018. Conserved, unstructured regions in Pseudomonas aeruginosa PilO are important for type IVa pilus function. Sci Rep 8 : 2600.[CrossRef][PubMed]
97. Leighton TL,, Yong DH,, Howell PL,, Burrows LL . 2016. Type IV pilus alignment subcomplex proteins PilN and PilO form homo- and heterodimers in vivo. J Biol Chem 291 : 19923 19938.[CrossRef][PubMed]
98. Leighton TL,, Dayalani N,, Sampaleanu LM,, Howell PL,, Burrows LL . 2015. A novel role for PilNO in type IV pilus retraction revealed by alignment subcomplex mutations. J Bacteriol 197 : 2229 2238.[CrossRef][PubMed]
99. Golovanov AP,, Balasingham S,, Tzitzilonis C,, Goult BT,, Lian LY,, Homberset H,, Tønjum T,, Derrick JP . 2006. The solution structure of a domain from the Neisseria meningitidis lipoprotein PilP reveals a new beta-sandwich fold. J Mol Biol 364 : 186 195.[CrossRef][PubMed]
100. 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]
101. Berry JL,, Phelan MM,, Collins RF,, Adomavicius T,, Tønjum T,, Frye SA,, Bird L,, Owens R,, Ford RC,, Lian LY,, Derrick JP . 2012. Structure and assembly of a trans-periplasmic channel for type IV pili in Neisseria meningitidis. PLoS Pathog 8 : e1002923.[CrossRef][PubMed]
102. 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]
103. 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]
104. 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]
105. Kuchma SL,, Ballok AE,, Merritt JH,, Hammond JH,, Lu W,, Rabinowitz JD,, O’Toole GA . 2010. Cyclic-di-GMP-mediated repression of swarming motility by Pseudomonas aeruginosa: the pilY1 gene and its impact on surface-associated behaviors. J Bacteriol 192 : 2950 2964.[CrossRef][PubMed]
106. Luo Y,, Zhao K,, Baker AE,, Kuchma SL,, Coggan KA,, Wolfgang MC,, Wong GC,, O’Toole GA . 2015. A hierarchical cascade of second messengers regulates Pseudomonas aeruginosa surface behaviors. mBio 6 : e02456-14.[CrossRef][PubMed]
107. Siryaporn A,, Kuchma SL,, O’Toole GA,, Gitai Z . 2014. Surface attachment induces Pseudomonas aeruginosa virulence. Proc Natl Acad Sci U S A 111 : 16860 16865.[CrossRef][PubMed]
108. Rodesney CA,, Roman B,, Dhamani N,, Cooley BJ,, Katira P,, Touhami A,, Gordon VD . 2017. Mechanosensing of shear by Pseudomonas aeruginosa leads to increased levels of the cyclic-di-GMP signal initiating biofilm development. Proc Natl Acad Sci U S A 114 : 5906 5911.[CrossRef][PubMed]
109. Carter T,, Buensuceso RN,, Tammam S,, Lamers RP,, Harvey H,, Howell PL,, Burrows LL . 2017. The type IVa pilus machinery is recruited to sites of future cell division. mBio 8 : e02103-16.[CrossRef][PubMed]
110. Seitz P,, Blokesch M . 2013. DNA-uptake machinery of naturally competent Vibrio cholerae. Proc Natl Acad Sci U S A 110 : 17987 17992.[CrossRef][PubMed]
111. 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]
112. Imam S,, Chen Z,, Roos DS,, Pohlschröder M . 2011. Identification of surprisingly diverse type IV pili, across a broad range of gram-positive bacteria. PLoS One 6 : e28919.[CrossRef][PubMed]
113. D’Imprima E,, Salzer R,, Bhaskara RM,, Sánchez R,, Rose I,, Kirchner L,, Hummer G,, Kühlbrandt W,, Vonck J,, Averhoff B . 2017. Cryo-EM structure of the bifunctional secretin complex of Thermus thermophilus. eLife 6 : e30483.[CrossRef][PubMed]
114. Koo J,, Lamers RP,, Rubinstein JL,, Burrows LL,, Howell PL . 2016. Structure of the Pseudomonas aeruginosa type IVa pilus secretin at 7.4 Å. Structure 24 : 1778 1787.[CrossRef][PubMed]
115. Jain S,, Mościcka KB,, Bos MP,, Pachulec E,, Stuart MC,, Keegstra W,, Boekema EJ,, van der Does C . 2011. Structural characterization of outer membrane components of the type IV pili system in pathogenic Neisseria. PLoS One 6 : e16624.[CrossRef][PubMed]
116. 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 USA 111 : E953 E961.[CrossRef][PubMed]
117. Zhao X,, Schwartz CL,, Pierson J,, Giovannoni SJ,, McIntosh JR,, Nicastro D . 2017. Three-dimensional structure of the ultraoligotrophic marine bacterium “ Candidatus Pelagibacter ubique.” Appl Environ Microbiol 83 : e02807-16.[CrossRef][PubMed]
118. Salzer R,, D’Imprima E,, Gold VA,, Rose I,, Drechsler M,, Vonck J,, Averhoff B . 2016. Topology and structure/function correlation of ring- and gate-forming domains in the dynamic secretin complex of Thermus thermophilus. J Biol Chem 291 : 14448 14456.[CrossRef][PubMed]
119. 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][PubMed]
120. Yin M,, Yan Z,, Li X . 2018. Structural insight into the assembly of the type II secretion system pilotin-secretin complex from enterotoxigenic Escherichia coli. Nat Microbiol 3 : 581 587.[CrossRef][PubMed]
121. Hay ID,, Belousoff MJ,, Dunstan RA,, Bamert RS,, Lithgow T . 2018. Structure and membrane topography of the vibrio-type secretin complex from the type 2 secretion system of enteropathogenic Escherichia coli. J Bacteriol 200 : e00521-17.[PubMed]
122. Hay ID,, Belousoff MJ,, Lithgow T . 2017. Structural basis of type 2 secretion system engagement between the inner and outer bacterial membranes. mBio 8 : e01344-17.[CrossRef][PubMed]
123. Yan Z,, Yin M,, Xu D,, Zhu Y,, Li X . 2017. Structural insights into the secretin translocation channel in the type II secretion system. Nat Struct Mol Biol 24 : 177 183.[CrossRef][PubMed]
124. Seike K,, Yasuda M,, Hatazaki K,, Mizutani K,, Yuhara K,, Ito Y,, Fujimoto Y,, Ito S,, Tsuchiya T,, Yokoi S,, Nakano M,, Deguchi T . 2016. Novel penA mutations identified in Neisseria gonorrhoeae with decreased susceptibility to ceftriaxone isolated between 2000 and 2014 in Japan. J Antimicrob Chemother 71 : 2466 2470.[CrossRef][PubMed]
125. Semmler AB,, Whitchurch CB,, Leech AJ,, Mattick JS . 2000. Identification of a novel gene, fimV, involved in twitching motility in Pseudomonas aeruginosa. Microbiology 146 : 1321 1332.[CrossRef][PubMed]
126. Trindade MB,, Job V,, Contreras-Martel C,, Pelicic V,, Dessen A . 2008. Structure of a widely conserved type IV pilus biogenesis factor that affects the stability of secretin multimers. J Mol Biol 378 : 1031 1039.[CrossRef][PubMed]
127. Kelley LA,, Mezulis S,, Yates CM,, Wass MN,, Sternberg MJ . 2015. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10 : 845 858.[CrossRef][PubMed]
128. Yang J,, Yan R,, Roy A,, Xu D,, Poisson J,, Zhang Y . 2015. The I-TASSER Suite: protein structure and function prediction. Nat Methods 12 : 7 8.[CrossRef][PubMed]
129. Kim DE,, Chivian D,, Baker D . 2004. Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res 32 : W526 W531.[CrossRef][PubMed]
130. Collins RF,, Hassan D,, Karuppiah V,, Thistlethwaite A,, Derrick JP . 2013. Structure and mechanism of the PilF DNA transformation ATPase from Thermus thermophilus. Biochem J 450 : 417 425.[CrossRef][PubMed]
131. Koo J,, Burrows LL,, Howell PL . 2012. Decoding the roles of pilotins and accessory proteins in secretin escort services. FEMS Microbiol Lett 328 : 1 12.[CrossRef][PubMed]
132. Nudleman E,, Wall D,, Kaiser D . 2006. Polar assembly of the type IV pilus secretin in Myxococcus xanthus. Mol Microbiol 60 : 16 29.[CrossRef][PubMed]
133. Rumszauer J,, Schwarzenlander C,, Averhoff B . 2006. Identification, subcellular localization and functional interactions of PilMNOWQ and PilA4 involved in transformation competency and pilus biogenesis in the thermophilic bacterium Thermus thermophilus HB27. FEBS J 273 : 3261 3272.[CrossRef][PubMed]
134. Koo J,, Tammam S,, Ku SY,, Sampaleanu LM,, Burrows LL,, Howell PL . 2008. PilF is an outer membrane lipoprotein required for multimerization and localization of the Pseudomonas aeruginosa type IV pilus secretin. J Bacteriol 190 : 6961 6969.[CrossRef][PubMed]
135. Robert-Paganin J,, Nonin-Lecomte S,, Réty S . 2012. Crystal structure of an EAL domain in complex with reaction product 5′-pGpG. PLoS One 7 : e52424.[CrossRef][PubMed]
136. Navarro MV,, De N,, Bae N,, Wang Q,, Sondermann H . 2009. Structural analysis of the GGDEF-EAL domain-containing c-di-GMP receptor FimX. Structure 17 : 1104 1116.[CrossRef][PubMed]
137. Guzzo CR,, Dunger G,, Salinas RK,, Farah CS . 2013. Structure of the PilZ-FimXEAL-c-di-GMP complex responsible for the regulation of bacterial type IV pilus biogenesis. J Mol Biol 425 : 2174 2197.[CrossRef][PubMed]
138. Li TN,, Chin KH,, Liu JH,, Wang AH,, Chou SH . 2009. XC1028 from Xanthomonas campestris adopts a PilZ domain-like structure without a c-di-GMP switch. Proteins 75 : 282 288.[CrossRef][PubMed]
139. Kim K,, Oh J,, Han D,, Kim EE,, Lee B,, Kim Y . 2006. Crystal structure of PilF: functional implication in the type 4 pilus biogenesis in Pseudomonas aeruginosa. Biochem Biophys Res Commun 340 : 1028 1038.[CrossRef][PubMed]
140. Buensuceso RN,, Nguyen Y,, Zhang K,, Daniel-Ivad M,, Sugiman-Marangos SN,, Fleetwood AD,, Zhulin IB,, Junop MS,, Howell PL,, Burrows LL . 2016. The conserved tetratricopeptide repeat-containing C-terminal domain of Pseudomonas aeruginosa FimV is required for its cyclic AMP-dependent and -independent functions. J Bacteriol 198 : 2263 2274.[CrossRef][PubMed]


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List of available T4aP structures

Citation: McCallum M, Burrows L, Howell P. 2019. The Dynamic Structures of the Type IV Pilus, p 113-128. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0006-2018

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