Insights into bacteriophage T5 structure from analysis of its morphogenesis genes and protein components

Journal of Virology

Volumn 88, Issue 2, 2014, Pages 1162-1174

  Zivanovic, Yvan ^b   Confalonieri, Fabrice ^b   Ponchon, Luc ^c   Lurz, Rudi ^d   Chami, Mohamed ^e   Flayhan, Ali ^f   Renouard, Madalena ^a   Huet, Alexis ^a,h   Decottignies, Paulette ^a   Davidson, Alan R ^g   Breyton, Cécile ^f   Boulanger, Pascale ^a  

^a INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^e UNIVERSITY OF BASEL   (Switzerland)

^f UNIV GRENOBLE ALPES   (France)

^g UNIVERSITY OF TORONTO   (Canada)

^h UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; CHAPERONE; ENDONUCLEASE; VIRUS DNA; VIRUS PROTEIN;

ARTICLE; BACTERIOPHAGE T5; BIOINFORMATICS; CONTROLLED STUDY; DNA CONFORMATION; DNA STRAND; DNA TRANSFER; ELECTRON MICROSCOPY; GENE IDENTIFICATION; GENE STRUCTURE; GENOME ANALYSIS; IMMUNOLOCALIZATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEOMICS; VIRION; VIRUS ASSEMBLY; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS IDENTIFICATION; VIRUS MORPHOGENESIS; VIRUS MORPHOLOGY; VIRUS PARTICLE; VIRUS STRAIN;

AMINO ACID SEQUENCE; BACTERIOPHAGES; CAPSID; ESCHERICHIA COLI; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; SIPHOVIRIDAE; VIRAL PROTEINS;

EID: 84891710087     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02262-13     Document Type: Article

References (77)

1. Wang J, Jiang Y, Vincent M, Sun Y, Yu H, Bao Q, Kong H, Hu S. 2005. Complete genome sequence of bacteriophage T5. Virology 332:45-65. http://dx.doi.org/10.1016/j.virol.2004.10.049.
2. Rabsch W, Ma L, Wiley G, Najar FZ, Kaserer W, Schuerch DW, Klebba JE, Roe BA, Gomez JAL, Schallmey M, Newton SMC, Klebba PE. 2007. FepA- and TonB-dependent bacteriophage H8: receptor binding and genomic sequence. J. Bacteriol. 189:5658-5674. http://dx.doi.org/10.1128/JB.00437-07.
3. Hong J, Kim KP, Heu S, Lee SJ, Adhya S, Ryu S. 2008. Identification of host receptor and receptor-binding module of a newly sequenced T5-like phage EPS7. FEMS Microbiol. Lett. 289:202-209. http://dx.doi.org/10.1111/j.1574-6968.2008.01397.x.
4. Kim M, Ryu S. 2011. Characterization of a T5-like coliphage, SPC35, and differential development of resistance to SPC35 in Salmonella enterica serovar Typhimurium and Escherichia coli. Appl. Environ. Microbiol. 77:2042-2050. http://dx.doi.org/10.1128/AEM.02504-10.
5. Niu YD, Stanford K, Kropinski AM, Ackermann HW, Johnson RP, She YM, Ahmed R, Villegas A, McAllister TA. 2012. Genomic, proteomic and physiological characterization of a T5-like bacteriophage for control of Shiga toxin-producing Escherichia coli O157:H7. PLoS One 7:e34585. http://dx.doi.org/10.1371/journal.pone.0034585.
6. Kim JH, Jun JW, Choresca CH, Shin SP, Han JE, Park SC. 2012. Complete genome sequence of a novel marine siphovirus, pVp-1, infecting Vibrio parahaemolyticus. J. Virol. 86:7013-7014. http://dx.doi.org/10.1128/JVI.00742-12.
7. Lee DH, Lee JH, Shin H, Ji S, Roh E, Jung K, Ryu S, Choi J, Heu S. 2012. Complete genome sequence of Pectobacterium carotovorum subsp. carotovorum bacteriophage My1. J. Virol. 86:11410-11411. http://dx.doi.org/10.1128/JVI.01987-12.
8. Zweig M, Cummings DJ. 1973. Structural proteins of bacteriophage T5. Virology 51:443-453. http://dx.doi.org/10.1016/0042-6822(73)90443-1.
9. Effantin G, Boulanger P, Neumann E, Letellier L, Conway JF. 2006. Bacteriophage T5 structure reveals similarities with HK97 and T4 suggesting evolutionary relationships. J. Mol. Biol. 361:993-1002. http://dx.doi.org/10.1016/j.jmb.2006.06.081.
10. Huet A, Conway JF, Letellier L, Boulanger P. 2010. In vitro assembly of the t'13 procapsid of bacteriophage T5 with its scaffolding domain. J. Virol. 84:9350-9358. http://dx.doi.org/10.1128/JVI.00942-10.
11. Preux O, Durand D, Huet A, Conway JF, Bertin A, Boulogne C, Drouin-Wahbi J, Trevarin D, Perez J, Vachette P, Boulanger P. 2013. A two-state cooperative expansion converts the procapsid shell of bacteriophage T5 into a highly stable capsid isomorphous to the final virion head. J. Mol. Biol. 425:1999-2014. http://dx.doi.org/10.1016/j.jmb.2013.03.002.
12. Kaliman AV, Kulshin VE, Shlyapnikov MG, Ksenzenko VN, Kryukov VM. 1995. The nucleotide sequence of the bacteriophage T5 ltf gene. FEBS Lett. 366:46-48. http://dx.doi.org/10.1016/0014-5793(95)00482-O.
13. Saigo K. 1978. Isolation of high-density mutants and identification of nonessential structural proteins in bacteriophage T5; dispensability of Lshaped tail fibers and a secondary major head protein. Virology 85:422-433. http://dx.doi.org/10.1016/0042-6822(78)90449-X.
14. Schwarzer D, Stummeyer K, Gerardy-Schahn R, Muhlenhoff M. 2007. Characterization of a novel intramolecular chaperone domain conserved in endosialidases and other bacteriophage tail spike and fiber proteins. J. Biol. Chem. 282:2821-2831. http://dx.doi.org/10.1074/jbc.M609543200.
15. Feucht A, Schmid A, Benz R, Schwarz H, Heller KJ. 1990. Pore formation associated with the tail-tip protein pb2 of bacteriophage T5. J. Biol. Chem. 265:18561-18567.
16. Boulanger P, Jacquot P, Plancon L, Chami M, Engel A, Parquet C, Herbeuval C, Letellier L. 2008. Phage T5 straight tail fiber is a multifunctional protein acting as a tape measure and carrying fusogenic and muralytic activities. J. Biol. Chem. 283:13556-13564. http://dx.doi.org/10.1074/jbc.M800052200.
17. Heller KJ, Schwarz H. 1985. Irreversible binding to the receptor of bacteriophages T5 and BF23 does not occur with the tip of the tail. J. Bacteriol. 162:621-625.
18. Davidson AR, Cardarelli L, Pell LG, Radford DR, Maxwell KL. 2012. Long noncontractile tail machines of bacteriophages. Adv. Exp. Med. Biol. 726:115-142. http://dx.doi.org/10.1007/978-1-4614-0980-9_6.
19. Heller KJ, Bryniok D. 1984. O antigen-dependent mutant of bacteriophage T5. J. Virol. 49:20-25.
20. Mondigler M, Holz T, Heller KJ. 1996. Identification of the receptorbinding regions of pb5 proteins of bacteriophages T5 and BF23. Virology 219:19-28. http://dx.doi.org/10.1006/viro.1996.0218.
21. Plançon L, Janmot C, Le Maire M, Desmadril M, Bonhivers M, Letellier L, Boulanger P. 2002. Characterization of a high-affinity complex between the bacterial outer membrane protein FhuA and the phage T5 protein pb5. J. Mol. Biol. 318:557-569. http://dx.doi.org/10.1016/S0022-2836(02)00089-X.
22. Flayhan A, Wien F, Paternostre M, Boulanger P, Breyton C. 2012. New insights into pb5, the receptor binding protein of bacteriophage T5, and its interaction with its Escherichia coli receptor FhuA. Biochimie 94:1982-1989. http://dx.doi.org/10.1016/j.biochi.2012.05.021.
23. Breyton C, Flayhan A, Gabel F, Lethier M, Durand G, Boulanger P, Chami M, Ebel C. 2013. Assessing the conformational changes of pb5, the receptor-binding protein of phage T5, upon binding to its Escherichia coli receptor FhuA. J. Biol. Chem. 288:30763-30772. http://dx.doi.org/10.1074/jbc.M113.501536.
24. Scheible PP, Rhoades M. 1975. Heteroduplex mapping of heat-resistant deletion mutants of bacteriophage T5. J. Virol. 15:1276-1280.
25. Lanni YT. 1958. Lysis inhibition with a mutant of bacteriophage T5. Virology 5:481-501. http://dx.doi.org/10.1016/0042-6822(58)90041-2.
26. Boulanger P. 2009. Purification of bacteriophages and SDS-PAGE analysis of phage structural proteins from ghost particles. Methods Mol. Biol. 502:227-238. http://dx.doi.org/10.1007/978-1-60327-565-1_13.
27. Delcher AL, Harmon D, Kasif S, White O, Salzberg SL. 1999. Improved microbial gene identification with GLIMMER. Nucleic Acids Res. 27:4636-4641. http://dx.doi.org/10.1093/nar/27.23.4636.
28. Gentz R, Bujard H. 1985. Promoters recognized by Escherichia coli RNA polymerase selected by function: highly efficient promoters from bacteriophage T5. J. Bacteriol. 164:70-77.
29. Noirclerc-Savoye M, Gallet B, Bernaudat F, Vernet T. 2010. Large scale purification of linear plasmid DNA for efficient high throughput cloning. Biotechnol. J. 5:978-985. http://dx.doi.org/10.1002/biot.201000132.
30. Harlow E, Lane D. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
31. Evrin C, Clarke P, Zech J, Lurz R, Sun J, Uhle S, Li H, Stillman B, Speck C. 2009. A double-hexameric MCM2-7 complex is loaded onto origin DNA during licensing of eukaryotic DNA replication. Proc. Natl. Acad. Sci. U. S. A. 106:20240-20245. http://dx.doi.org/10.1073/pnas.0911500106.
32. Ludtke SJ, Baldwin PR, Chiu W. 1999. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128:82-97. http://dx.doi.org/10.1006/jsbi.1999.4174.
33. Boulanger P, le Maire M, Bonhivers M, Dubois S, Desmadril M, Letellier L. 1996. Purification and structural and functional characterization of FhuA, a transporter of the Escherichia coli outer membrane. Biochemistry 35:14216-14224. http://dx.doi.org/10.1021/bi9608673.
34. Hendrickson HE, McCorquodale DJ. 1971. Genetic and physiological studies of bacteriophage T5. I. An expanded genetic map of T5. J. Virol. 7:612-618.
35. Cheng H, Shen N, Pei J, Grishin NV. 2004. Double-stranded DNA bacteriophage prohead protease is homologous to herpesvirus protease. Protein Sci. 13:2260-2269. http://dx.doi.org/10.1110/ps.04726004.
36. Liu J, Mushegian A. 2004. Displacements of prohead protease genes in the late operons of double-stranded-DNA bacteriophages. J. Bacteriol. 186:4369-4375. http://dx.doi.org/10.1128/JB.186.13.4369-4375.2004.
37. Cardarelli L, Lam R, Tuite A, Baker LA, Sadowski PD, Radford DR, Rubinstein JL, Battaile KP, Chirgadze N, Maxwell KL, Davidson AR. 2010. The crystal structure of bacteriophage HK97 gp6: defining a large family of head-tail connector proteins. J. Mol. Biol. 395:754-768. http://dx.doi.org/10.1016/j.jmb.2009.10.067.
38. Casjens SR. 2011. The DNA-packaging nanomotor of tailed bacteriophages. Nat. Rev. Microbiol. 9:647-657. http://dx.doi.org/10.1038/nrmicro2632.
39. Ponchon L, Boulanger P, Labesse G, Letellier L. 2006. The endonuclease domain of bacteriophage terminases belongs to the resolvase/integrase/ribonuclease H superfamily: a bioinformatics analysis validated by a functional study on bacteriophage T5. J. Biol. Chem. 281:5829-5836. http://dx.doi.org/10.1074/jbc.M511817200.
40. Buttner CR, Chechik M, Ortiz-Lombardia M, Smits C, Ebong IO, Chechik V, Jeschke G, Dykeman E, Benini S, Robinson CV, Alonso JC, Antson AA. 2012. Structural basis for DNA recognition and loading into a viral packaging motor. Proc. Natl. Acad. Sci. U. S. A. 109:811-816. http://dx.doi.org/10.1073/pnas.1110270109.
41. Dunin-Horkawicz S, Feder M, Bujnicki JM. 2006. Phylogenomic analysis of the GIY-YIG nuclease superfamily. BMC Genomics 7:98. http://dx.doi.org/10.1186/1471-2164-7-98.
42. Mehta P, Katta K, Krishnaswamy S. 2004. HNH family subclassification leads to identification of commonality in the His-Me endonuclease superfamily. Protein Sci. 13:295-300. http://dx.doi.org/10.1110/ps.03115604.
43. Rogers SG, Godwin EA, Shinosky ES, Rhoades M. 1979. Interruptiondeficient mutants of bacteriophage T5. I. Isolation and general properties. J. Virol. 29:716-725.
44. Krauel V, Heller KJ. 1991. Cloning, sequencing, and recombinational analysis with bacteriophage BF23 of the bacteriophage T5 oad gene encoding the receptor-binding protein. J. Bacteriol. 173:1287-1297.
45. Pell LG, Liu A, Edmonds L, Donaldson LW, Howell PL, Davidson AR. 2009. The X-ray crystal structure of the phage lambda tail terminator protein reveals the biologically relevant hexameric ring structure and demonstrates a conserved mechanism of tail termination among diverse long-tailed phages. J. Mol. Biol. 389:938-951. http://dx.doi.org/10.1016/j.jmb.2009.04.072.
46. Auzat I, Dröge A, Weise F, Lurz R, Tavares P. 2008. Origin and function of the two major tail proteins of bacteriophage SPP1. Mol. Microbiol. 70:557-569. http://dx.doi.org/10.1111/j.1365-2958.2008.06435.x.
47. Pell LG, Gasmi-Seabrook GM, Morais M, Neudecker P, Kanelis V, Bona D, Donaldson LW, Edwards AM, Howell PL, Davidson AR, Maxwell KL. 2010. The solution structure of the C-terminal Ig-like domain of the bacteriophage lambda tail tube protein. J. Mol. Biol. 403:468-479. http://dx.doi.org/10.1016/j.jmb.2010.08.044.
48. Pell LG, Kanelis V, Donaldson LW, Howell PL, Davidson AR. 2009. The phage lambda major tail protein structure reveals a common evolution for long-tailed phages and the type VI bacterial secretion system. Proc. Natl. Acad. Sci. U. S. A. 106:4160-4165. http://dx.doi.org/10.1073/pnas.0900044106.
49. Xu J, Hendrix RW, Duda RL. 2004. Conserved translational frameshift in dsDNA bacteriophage tail assembly genes. Mol. Cell 16:11-21. http://dx.doi.org/10.1016/j.molcel.2004.09.006.
50. Xu J, Hendrix RW, Duda RL. 2013. A balanced ratio of proteins from gene G and frameshift-extended gene GT is required for phage lambda tail assembly. J. Mol. Biol. 425:3476-3487. http://dx.doi.org/10.1016/j.jmb.2013.07.002.
51. Katsura I, Kuhl PW. 1975. Morphogenesis of the tail of bacteriophage lambda. III. Morphogenetic pathway. J. Mol. Biol. 91:257-273.
52. Heller K, Braun V. 1982. Polymannose O-antigens of Escherichia coli, the binding sites for the reversible adsorption of bacteriophage T5+ via the L-shaped tail fibers. J. Virol. 41:222-227.
53. Bartual SG, Otero JM, Garcia-Doval C, Llamas-Saiz AL, Kahn R, Fox GC, van Raaij MJ. 2010. Structure of the bacteriophage T4 long tail fiber receptor-binding tip. Proc. Natl. Acad. Sci. U. S. A. 107:20287-20292. http://dx.doi.org/10.1073/pnas.1011218107.
54. Garcia-Doval C, van Raaij MJ. 2012. Crystallization of the C-terminal domain of the bacteriophage T7 fibre protein gp17. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 68:166-171. http://dx.doi.org/10.1107/S1744309111051049.
55. Steven AC, Trus BL, Maizel JV, Unser M, Parry DA, Wall JS, Hainfeld JF, Studier FW. 1988. Molecular substructure of a viral receptorrecognition protein. The gp17 tail-fiber of bacteriophage T7. J. Mol. Biol. 200:351-365.
56. Flayhan A, Vellieux FMD, Lurz R, Maury O, Contreras-Martel C, Girard E, Boulanger P, Breyton C. 2014. Crystal structure of pb9, the distal tail protein of bacteriophage T5: a conserved structural motif among all siphophages. J. Virol. 88:820-828. http://dx.doi.org/10.1128/JVI.02135-13.
57. Tam W, Pell LG, Bona D, Tsai A, Dai XX, Edwards AM, Hendrix RW, Maxwell KL, Davidson AR. 2013. Tail tip proteins related to bacteriophage lambda gpL coordinate an iron-sulfur cluster. J. Mol. Biol. 425:2450-2462. http://dx.doi.org/10.1016/j.jmb.2013.03.032.
58. Hendrix RW, Casjens S. 2006. Bacteriophage lambda and its genetic neighborhood, p 409-447. In Calendar R (ed), The bacteriophages. Oxford University Press, Oxford, United Kingdom.
59. Kanamaru S, Leiman PG, Kostyuchenko VA, Chipman PR, Mesyanzhinov VV, Arisaka F, Rossmann MG. 2002. Structure of the cellpuncturing device of bacteriophage T4. Nature 415:553-557. http://dx.doi.org/10.1038/415553a.
60. Kondou Y, Kitazawa D, Takeda S, Tsuchiya Y, Yamashita E, Mizuguchi M, Kawano K, Tsukihara T. 2005. Structure of the central hub of bacteriophage Mu baseplate determined by X-ray crystallography of gp44. J. Mol. Biol. 352:976-985. http://dx.doi.org/10.1016/j.jmb.2005.07.044.
61. Sciara G, Bebeacua C, Bron P, Tremblay D, Ortiz-Lombardia M, Lichiere J, van Heel M, Campanacci V, Moineau S, Cambillau C. 2010. Structure of lactococcal phage p2 baseplate and its mechanism of activation. Proc. Natl. Acad. Sci. U. S. A. 107:6852-6857. http://dx.doi.org/10.1073/pnas.1000232107.
62. Lambert O, Plançon L, Rigaud JL, Letellier L. 1998. Protein-mediated DNA transfer into liposomes. Mol. Microbiol. 30:761-765. http://dx.doi.org/10.1046/j.1365-2958.1998.01107.x.
63. Huang RK, Khayat R, Lee KK, Gertsman I, Duda RL, Hendrix RW, Johnson JE. 2011. The prohead-I structure of bacteriophage HK97: implications for scaffold-mediated control of particle assembly and maturation. J. Mol. Biol. 408:541-554. http://dx.doi.org/10.1016/j.jmb.2011.01.016.
64. Medina E, Wieczorek D, Medina EM, Yang Q, Feiss M, Catalano CE. 2010. Assembly and maturation of the bacteriophage lambda procapsid: gpC is the viral protease. J. Mol. Biol. 401:813-830. http://dx.doi.org/10.1016/j.jmb.2010.06.060.
65. Black LW, Showe MK. 1993. Morphogenesis of T4 head, p 218-258. In Karam JD (ed), Molecular biology of bacteriophage T4.ASMPress, Washington, DC.
66. Marvik OJ, Sharma P, Dokland T, Lindqvist BH. 1994. Bacteriophage P2 and P4 assembly: alternative scaffolding proteins regulate capsid size. Virology 200:702-714. http://dx.doi.org/10.1006/viro.1994.1234.
67. Thomas JA, Weintraub ST, Wu W, Winkler DC, Cheng N, Steven AC, Black LW. 2012. Extensive proteolysis of head and inner body proteins by a morphogenetic protease in the giant Pseudomonas aeruginosa phage phiKZ. Mol. Microbiol. 84:324-339. http://dx.doi.org/10.1111/j.1365-2958.2012.08025.x.
68. Tavares P, Zinn-Justin S, Orlova EV. 2012. Genome gating in tailed bacteriophage capsids. Adv. Exp. Med. Biol. 726:585-600. http://dx.doi.org/10.1007/978-1-4614-0980-9_25.
69. Fokine A, Zhang Z, Kanamaru S, Bowman VD, Aksyuk AA, Arisaka F, Rao VB, Rossmann MG. 2013. The molecular architecture of the bacteriophage T4 neck. J. Mol. Biol. 425:1731-1744. http://dx.doi.org/10.1016/j.jmb.2013.02.012.
70. Goulet A, Lai-Kee-Him J, Veesler D, Auzat I, Robin G, Shepherd DA, Ashcroft AE, Richard E, Lichiere J, Tavares P, Cambillau C, Bron P. 2011. The opening of the SPP1 bacteriophage tail, a prevalent mechanism in Gram-positive-infecting siphophages. J. Biol. Chem. 286:25397-25405. http://dx.doi.org/10.1074/jbc.M111.243360.
71. Vinga I, Baptista C, Auzat I, Petipas I, Lurz R, Tavares P, Santos MA, Sao-Jose C. 2012. Role of bacteriophage SPP1 tail spike protein gp21 on host cell receptor binding and trigger of phage DNA ejection. Mol. Microbiol. 83:289-303. http://dx.doi.org/10.1111/j.1365-2958.2011.07931.x.
72. Hu B, Margolin W, Molineux IJ, Liu J. 2013. The bacteriophage T7 virion undergoes extensive structural remodeling during infection. Science 339:576-579. http://dx.doi.org/10.1126/science.1231887.
73. Leiman PG, Basler M, Ramagopal UA, Bonanno JB, Sauder JM, Pukatzki S, Burley SK, Almo SC, Mekalanos JJ. 2009. Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc. Natl. Acad. Sci. U. S. A. 106:4154-4159. http://dx.doi.org/10.1073/pnas.0813360106.
74. Sao-Jose C, Lhuillier S, Lurz R, Melki R, Lepault J, Santos MA, Tavares P. 2006. The ectodomain of the viral receptor YueB forms a fiber that triggers ejection of bacteriophage SPP1 DNA. J. Biol. Chem. 281:11464-11470. http://dx.doi.org/10.1074/jbc.M513625200.
75. Böhm J, Lambert O, Frangakis AS, Letellier L, Baumeister W, Rigaud JL. 2001. FhuA-mediated phage genome transfer into liposomes: a cryoelectron tomography study. Curr. Biol. 11:1168-1175. http://dx.doi.org/10.1016/S0960-9822(01)00349-9.
76. McCorquodale JD, Warner HR. 1988. Bacteriophages T5 and related phages, p 439-476. In Calendar R (ed), The viruses, vol 1. Plenum Press, New York, NY.
77. Catherinot V, Labesse G. 2004. ViTO: tool for refinement of protein sequence-structure alignments. Bioinformatics 20:3694-3696. http://dx.doi.org/10.1093/bioinformatics/bth429.