Function and horizontal transfer of the small terminase subunit of the tailed bacteriophage Sf6 DNA packaging nanomotor

Virology

Volumn 440, Issue 2, 2013, Pages 117-133

  Leavitt, Justin C ^a   Gilcrease, Eddie B ^b   Wilson, Kassandra ^b   Casjens, Sherwood R ^a,b  

^a UNIVERSITY OF UTAH   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Bacteriophage P22; Bacteriophage Sf6; DNA packaging; Small terminase subunit; TerS

Indexed keywords

BACTERIAL PROTEIN; TERMINASE SUBUNIT PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIOPHAGE; BACTERIOPHAGE P22; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; COVALENT BOND; DNA CLEAVAGE; DNA PACKAGING; DNA SEQUENCE; ESCHERICHIA COLI; GENE FUNCTION; GENETIC ANALYSIS; HORIZONTAL GENE TRANSFER; IN VIVO STUDY; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE BINDING SITE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SALMONELLA ENTERICA; SHIGELLA FLEXNERI; TERMINASE SUBUNIT GENE;

AMINO ACID SEQUENCE; BACTERIOPHAGES; DNA PACKAGING; DNA, VIRAL; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN SUBUNITS; SEQUENCE HOMOLOGY, AMINO ACID; VIRAL PROTEINS;

EID: 84876815569     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.02.023     Document Type: Article

References (100)

1. Al-Zahrani A.S., Kondabagil K., Gao S., Kelly N., Ghosh-Kumar M., Rao V.B. The small terminase, gp16, of bacteriophage T4 is a regulator of the DNA packaging motor. J. Biol. Chem. 2009, 284:24490-24500.
2. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
3. Black L.W., Showe M., Steven A.C. Morphogenesis of the T4 head. Molecular Biology of Bacteriophage T4 1994, 218-258. ASM Press, Washington, DC. J. Karam (Ed.).
4. Buttner C.R., Chechik M., Ortiz-Lombardia M., Smits C., Ebong I.O., Chechik V., Jeschke G., Dykeman E., Benini S., Robinson C.V., Alonso J.C., Antson A.A. Structural basis for DNA recognition and loading into a viral packaging motor. Proc. Natl. Acad. Sci. USA 2012, 109:811-816.
5. Camacho A., Jimenez F., De La Torre J., Carrascosa J.L., Mellado R.P., Vasquez C., Vinuela E., Salas M. Assembly of Bacillus subtilis phage q29. 1. Mutants in the cistrons coding for the structural proteins. Eur. J. Biochem 1977, 73:39-55.
6. Casjens S. Principles of virion structure, function and assembly. Structural Biology of Viruses 1997, 3-37. Oxford University Press, Oxford. W. Chiu, R. Burnett, R. Garcea (Eds.).
7. Casjens S. Prophages and bacterial genomics: what have we learned so far?. Mol. Microbiol. 2003, 49:277-300.
8. Casjens S. Diversity among the tailed-bacteriophages that infect the Enterobacteriaceae. Res. Microbiol. 2008, 159:340-348.
9. Casjens S., Delange M., Ley H.L., Rosa P., Huang W.M. Linear chromosomes of Lyme disease agent spirochetes: genetic diversity and conservation of gene order. J. Bacteriol. 1995, 177:2769-2780.
10. Casjens S., Eppler K., Parr R., Poteete A.R. Nucleotide sequence of the bacteriophage P22 gene 19 to 3 region: identification of a new gene required for lysis. Virology 1989, 171:588-598.
11. Casjens S., Huang W.M. Initiation of sequential packaging of bacteriophage P22 DNA. J. Mol. Biol. 1982, 157:287-298.
12. Casjens S., Huang W.M. Linear chromosomal physical and genetic map of Borrelia burgdorferi, the Lyme disease agent. Mol. Microbiol. 1993, 8:967-980.
13. Casjens S., King J. P22 morphogenesis. I: catalytic scaffolding protein in capsid assembly. J. Supramol. Struct 1974, 2:202-224.
14. Casjens S., Sampson L., Randall S., Eppler K., Wu H., Petri J.B., Schmieger H. Molecular genetic analysis of bacteriophage P22 gene 3 product, a protein involved in the initiation of headful DNA packaging. J. Mol. Biol. 1992, 227:1086-1099.
15. Casjens S., Winn-Stapley D., Gilcrease E., Moreno R., Kühlewein C., Chua J.E., Manning P.A., Inwood W., Clark A.J. The chromosome of Shigella flexneri bacteriophage Sf6: complete nucleotide sequence, genetic mosaicism, and DNA packaging. J. Mol. Biol. 2004, 339:379-394.
16. Casjens S., Wyckoff E., Hayden M., Sampson L., Eppler K., Randall S., Moreno E., Serwer P. Bacteriophage P22 portal protein is part of the gauge that regulates packing density of intravirion DNA. J. Mol. Biol. 1992, 224:1055-1074.
17. Casjens S.R. The DNA-packaging nanomotor of tailed bacteriophages. Nat. Rev. Microbiol. 2011, 9:647-657.
18. Casjens S.R., Gilcrease E.B., Winn-Stapley D.A., Schicklmaier P., Schmieger H., Pedulla M.L., Ford M.E., Houtz J.M., Hatfull G.F., Hendrix R.W. The generalized transducing Salmonella bacteriophage ES18: complete genome sequence and DNA packaging strategy. J. Bacteriol. 2005, 187:1091-1104.
19. Casjens S.R., Thuman-Commike P.A. Evolution of mosaically related tailed bacteriophage genomes seen through the lens of phage P22 virion assembly. Virology 2011, 411:393-415.
20. Chai S., Kruft V., Alonso J.C. Analysis of the Bacillus subtilis bacteriophages SPP1 and SF6 gene 1 product: a protein involved in the initiation of headful packaging. Virology 1994, 202:930-939.
21. Chai S., Lurz R., Alonso J.C. The small subunit of the terminase enzyme of Bacillus subtilis bacteriophage SPP1 forms a specialized nucleoprotein complex with the packaging initiation region. J. Mol. Biol. 1995, 252:386-398.
22. Cortines J.R., Weigele P.R., Gilcrease E.B., Casjens S.R., Teschke C.M. Decoding bacteriophage P22 assembly: identification of two charged residues in scaffolding protein responsible for coat protein interaction. Virology 2011, 421:1-11.
23. Datsenko K.A., Wanner B.L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 2000, 97:6640-6645.
24. de Beer T., Fang J., Ortega M., Yang q., Maes L., Duffy C., Berton N., Sippy J., Overduin M., Feiss M., Catalano C.E. Insights into specific DNA recognition during the assembly of a viral genome packaging machine. Mol. Cell 2002, 9:981-991.
25. Deichelbohrer I., Messer W., Trautner T.A. Genome of Bacillus subtilis Bacteriophage SPP1: Structure and Nucleotide Sequence of pac, the Origin of DNA Packaging. J. Virol. 1982, 42:83-90.
26. Duffy C., Feiss M. The large subunit of bacteriophage lambda's terminase plays a role in DNA translocation and packaging termination. J. Mol. Biol 2002, 316:547-561.
27. Feiss M., Rao V.B. The bacteriophage DNA packaging machine. Adv Exp. Med. Biol. 2012, 726:489-509.
28. Frackman S., Siegele D.A., Feiss M. A functional domain of bacteriophage lambda terminase for prohead binding. J. Mol. Biol. 1984, 180:283-300.
29. Frackman S., Siegele D.A., Feiss M. The terminase of bacteriophage lambda. Functional domains for cosB binding and multimer assembly. J. Mol. Biol. 1985, 183:225-238.
30. Gao S., Rao V. Specificity of interactions among the DNA-packaging machine components of T4-related bacteriophages. J. Biol. Chem. 2011, 286:3944-3956.
31. German G., Misra R., Kropinski A. The T1-like bacteriophages. The Bacteriophages 2006, 211-224. Oxford University Press, Oxford. Second Edition. R. Calendar (Ed.).
32. Groenen M.A., van de Putte P. Mapping of a site for packaging of bacteriophage Mu DNA. Virology 1985, 144:520-522.
33. Harel J., Duplessis L., Kahn J.S., DuBow M.S. The cis-acting DNA sequences required in vivo for bacteriophage Mu helper-mediated transposition and packaging. Arch. Microbiol. 1990, 154:67-72.
34. Hatfull G.F. The secret lives of mycobacteriophages. Adv. Virus Res. 2012, 82:179-288.
35. Hegde S., Padilla-Sanchez V., Draper B., Rao V.B. Portal-large terminase interactions of the bacteriophage T4 DNA packaging machine implicate a molecular lever mechanism for coupling ATPase to DNA translocation. J. Virol 2012, 86:4046-4057.
36. Jackson E.N., Jackson D.A., Deans R.J. EcoRI analysis of bacteriophage P22 DNA packaging. J. Mol. Biol. 1978, 118:365-388.
37. Jackson E.N., Laski F., Andres C. Bacteriophage P22 mutants that alter the specificity of DNA packaging. J. Mol. Biol. 1982, 154:551-563.
38. Jiang W., Li Z., Zhang Z., Baker M.L., Prevelige P.E., Chiu W. Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions. Nat. Struct. Biol 2003, 10:131-135.
39. Karlinsey J.E. Lambda-Red genetic engineering in Salmonella enterica serovar Typhimurium. Methods Enzymol. 2007, 421:199-209.
40. Kondabagil K.R., Zhang Z., Rao V.B. The DNA translocating ATPase of bacteriophage T4 packaging motor. J. Mol. Biol. 2006, 363:786-799.
41. Kulesus R.R., Diaz-Perez K., Slechta E.S., Eto D.S., Mulvey M.A. Impact of the RNA chaperone Hfq on the fitness and virulence potential of uropathogenic Escherichia coli. Infect. Immun. 2008, 76:3019-3026.
42. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
43. Lebedev A.A., Krause M.H., Isidro A.L., Vagin A.A., Orlova E.V., Turner J., Dodson E.J., Tavares P., Antson A.A. Structural framework for DNA translocation via the viral portal protein. EMBO J. 2007, 26:1984-1994.
44. Lee Y.D., Park J.H., Chang H.I. Genomic sequence analysis of virulent Cronobacter sakazakii bacteriophage ES2. Arch. Virol. 2011, 156:2105-2108.
45. Liebeschuetz J., Ritchie D.A. Phage T1-mediated transduction of a plasmid containing the T1 pac site. J. Mol. Biol. 1986, 192:681-692.
46. Lin H., Rao V.B., Black L.W. Analysis of capsid portal protein and terminase functional domains: interaction sites required for DNA packaging in bacteriophage T4. J. Mol. Biol. 1999, 289:249-260.
47. Linderoth N.A., Ziermann R., Haggard-Ljungquist E., Christie G.E., Calendar R. Nucleotide sequence of the DNA packaging and capsid synthesis genes of bacteriophage P2. Nucleic Acids Res. 1991, 19:7207-7214.
48. Lobocka M.B., Rose D.J., Plunkett G., Rusin M., Samojedny A., Lehnherr H., Yarmolinsky M.B., Blattner F.R. Genome of bacteriophage P1. J. Bacteriol. 2004, 186:7032-7068.
49. Maluf N., Yang q., Catalano C. Self-association properties of the bacteriophage lambda terminase holoenzyme: implications for the DNA packaging motor. J. Mol. Biol. 2005, 347:523-542.
50. Morgan G.J., Hatfull G.F., Casjens S., Hendrix R.W. Bacteriophage Mu genome sequence: analysis and comparison with Mu-like prophages in Haemophilus, Neisseria and Deinococcus. J. Mol. Biol. 2002, 317:337-359.
51. Morita M., Tasaka M., Fujisawa H. Structural and functional domains of the large subunit of the bacteriophage T3 DNA packaging enzyme: importance of the C-terminal region in prohead binding. J. Mol. Biol 1995, 245:635-644.
52. Nemecek D., Gilcrease E.B., Kang S., Prevelige P.E., Casjens S., Thomas G.J. Subunit conformations and assembly states of a DNA-translocating motor: the terminase of bacteriophage P22. J. Mol. Biol. 2007, 374:817-836.
53. Nemecek D., Lander G.C., Johnson J.E., Casjens S.R., Thomas G.J. Assembly architecture and DNA binding of the bacteriophage P22 terminase small subunit. J. Mol. Biol. 2008, 383:494-501.
54. Olia A.S., Prevelige P.E., Johnson J.E., Cingolani G. Three-dimensional structure of a viral genome-delivery portal vertex. Nat. Struct. Mol. Biol. 2011, 18:597-603.
55. Oliveira L., Alonso J.C., Tavares P. A defined in vitro system for DNA packaging by the bacteriophage SPP1: insights into the headful packaging mechanism. J. Mol. Biol 2005, 353:529-539.
56. Oliveira L., Henriques A.O., Tavares P. Modulation of the viral ATPase activity by the portal protein correlates with DNA packaging efficiency. J. Biol. Chem. 2006, 281:21914-21923.
57. Padilla-Meier G.P., Gilcrease E.B., Weigele P.R., Cortines J.R., Siegel M., Leavitt J.C., Teschke C.M., Casjens S.R. Unraveling the role of the C-terminal helix turn helix of the coat-binding domain of bacteriophage P22 scaffolding protein. J. Biol. Chem. 2012, 287:33766-33780.
58. Parent K.N., Gilcrease E.B., Casjens S.R., Baker T.S. Structural evolution of the P22-like phages: comparison of Sf6 and P22 procapsid and virion architectures. Virology 2012, 427:177-188.
59. Parent K.N., Khayat R., Tu L.H., Suhanovsky M.M., Cortines J.R., Teschke C.M., Johnson J.E., Baker T.S. P22 coat protein structures reveal a novel mechanism for capsid maturation: stability without auxiliary proteins or chemical crosslinks. Structure 2010, 18:390-401.
60. Pimkin M., Pimkina J., Markham G.D. A regulatory role of the Bateman domain of IMP dehydrogenase in adenylate nucleotide biosynthesis. J. Biol. Chem. 2009, 284:7960-7969.
61. Poteete A.R., Botstein D. Purification and properties of proteins essential to DNA encapsulation by phage P22. Virology 1979, 95:565-573.
62. Ray K., Oram M., Ma J., Black L.W. Portal control of viral prohead expansion and DNA packaging. Virology 2009, 391:44-50.
63. Roberts M.D., Martin N.L., Kropinski A.M. The genome and proteome of coliphage T1. Virology 2004, 318:245-266.
64. Rose R.E. The nucleotide sequence of pACYC177. Nucleic Acids Res. 1988, 16:356.
65. Roy A., Bhardwaj A., Datta P., Lander G., Cingolani G. Small terminase couples viral DNA-binding to genome-packaging ATPase activity. Structure 2012, 20:1403-1413.
66. Roy A., Cingolani G. Structure of P22 headful packaging nuclease. J. Biol. Chem. 2012, 287:28196-28205.
67. Schmieger H. Phage P22-mutants with increased or decreased transduction abilities. Mol. Gen. Genet. 1972, 119:75-88.
68. Schmieger H. pac sites are indispensable for in vivo packaging of DNA by phage P22. Mol. Gen. Genet. 1984, 195:252-255.
69. Schmieger H., Koch E. In vitro assay of packaging protein gp3 of Salmonella phage P22. Intervirology 1987, 28:157-162.
70. Shinder G., Gold M. The Nul subunit of bacteriophage lambda terminase binds to specific sites in cos DNA. J. Virol. 1988, 62:387-392.
71. Shultz J., Silhavy T.J., Berman M.L., Fiil N., Emr S.D. A previously unidentified gene in the spc operon of Escherichia coli K12 specifies a component of the protein export machinery. Cell 1982, 31:227-235.
72. Simpson A.A., Tao Y., Leiman P.G., Badasso M.O., He Y., Jardine P.J., Olson N.H., Morais M.C., Grimes S., Anderson D.L., Baker T.S., Rossmann M.G. Structure of the bacteriophage φ29 DNA packaging motor. Nature 2000, 408:745-750.
73. Sippy J., Feiss M. Analysis of a mutation affecting the specificity domain for prohead binding of the bacteriophage lambda terminase. J. Bacteriol 1992, 174:850-856.
74. Sternberg N., Coulby J. Recognition and cleavage of the bacteriophage P1 packaging site (pac). II. Functional limits of pac and location of pac cleavage termini. J. Mol. Biol 1987, 194:469-479.
75. Summer E., Berry J., Tran T., Niu L., Struck D., Young R. Rz/Rz1 lysis gene equivalents in phages of Gram-negative hosts. J. Mol. Biol. 2007, 373:1098-1112.
76. Sun S., Gao S., Kondabagil K., Xiang Y., Rossmann M.G., Rao V.B. Structure and function of the small terminase component of the DNA packaging machine in T4-like bacteriophages. Proc. Natl. Acad. Sci. USA 2012, 109:817-822.
77. Tang J., Lander G.C., Olia A.S., Li R., Casjens S., Prevelige P., Cingolani G., Baker T.S., Johnson J.E. Peering down the barrel of a bacteriophage portal: the genome packaging and release valve in P22. Structure 2011, 19:496-502.
78. Tavares P., Santos M.A., Lurz R., Morelli G., de Lencastre H., Trautner T.A. Identification of a gene in Bacillus subtilis bacteriophage SPP1 determining the amount of packaged DNA. J. Mol. Biol. 1992, 225:81-92.
79. Tsay J.M., Sippy J., DelToro D., Andrews B.T., Draper B., Rao V., Catalano C.E., Feiss M., Smith D.E. Mutations altering a structurally conserved loop-helix-loop region of a viral packaging motor change DNA translocation velocity and processivity. J. Biol. Chem. 2010, 285:24282-24289.
80. Tsay J.M., Sippy J., Feiss M., Smith D.E. The q motif of a viral packaging motor governs its force generation and communicates ATP recognition to DNA interaction. Proc. Natl. Acad. Sci. USA 2009, 106:14355-14360.
81. Tye B.K., Huberman J.A., Botstein D. Non-random circular permutation of phage P22 DNA. J. Mol. Biol. 1974, 85:501-528.
82. Warming S., Costantino N., Court D.L., Jenkins N.A., Copeland N.G. Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res. 2005, 33:e36.
83. Weaver S., Levine M. Replication in situ and DNA encapsulation following induction of an excision-defective lysogen of Salmonella bacteriophage P22. J. Mol. Biol 1978, 118:389-411.
84. Wikoff W.R., Liljas L., Duda R.L., Tsuruta H., Hendrix R.W., Johnson J.E. Topologically linked protein rings in the bacteriophage HK97 capsid. Science 2000, 289:2129-2133.
85. Winston F., Botstein D., Miller J.H. Characterization of amber and ochre suppressors in Salmonella typhimurium. J. Bacteriol. 1979, 137:433-439.
86. Wu C.H., Black L.W. Mutational analysis of the sequence-specific recombination box for amplification of gene 17 of bacteriophage T4. J. Mol. Biol 1995, 247:604-617.
87. Wu C.H., Lin H., Black L.W. Bacteriophage T4 gene 17 amplification mutants: evidence for initiation by the T4 terminase subunit gp16. J. Mol. Biol. 1995, 247:523-528.
88. Wu H., Sampson L., Parr R., Casjens S. The DNA site utilized by bacteriophage P22 for initiation of DNA packaging. Mol. Microbiol. 2002, 45:1631-1646.
89. Yang q., Berton N., Manning M.C., Catalano C.E. Domain structure of gpNu1, a phage lambda DNA packaging protein. Biochemistry 1999, 38:14238-14247.
90. Yang q., Berton N., Manning M.C., Catalano C.E. Domain structure of gpNu1, a phage lambda DNA packaging protein. Biochemistry 1999, 38:14238-14247.
91. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 1985, 33:103-119.
92. Yeo A., Feiss M. Mutational analysis of the prohead binding domain of the large subunit of terminase, the bacteriophage lambda DNA packaging enzyme. J. Mol. Biol. 1995, 245:126-140.
93. Yeo A., Feiss M. Specific interaction of terminase, the DNA packaging enzyme of bacteriophage lambda, with the portal protein of the prohead. J. Mol. Biol. 1995, 245:141-150.
94. Youderian P., Chadwick S.J., Susskind M.M. Autogenous regulation by the bacteriophage P22 arc gene product. J. Mol. Biol. 1982, 154:449-464.
95. Youderian P., Sugiono P., Brewer K.L., Higgins N.P., Elliott T. Packaging specific segments of the Salmonella chromosome with locked-in Mud-P22 prophages. Genetics 1988, 118:581-592.
96. Youderian P., Vershon A., Bouvier S., Sauer R.T., Susskind M.M. Changing the DNA-binding specificity of a repressor. Cell 1983, 35:777-783.
97. Zhang Z., Kottadiel V.I., Vafabakhsh R., Dai L., Chemla Y.R., Ha T., Rao V.B. A promiscuous DNA packaging machine from bacteriophage T4. PLoS Biol. 2011, 9:e1000592.
98. Zhao H., Finch C.J., Sequeira R.D., Johnson B.A., Johnson J.E., Casjens S.R., Tang L. Crystal structure of the DNA-recognition component of the bacterial virus Sf6 genome-packaging machine. Proc. Natl. Acad. Sci. USA 2010, 107:1971-1976.
99. Zhao H., Kamau Y.N., Christensen T.E., Tang L. Structural and functional studies of the phage Sf6 terminase small subunit reveal a DNA-spooling device facilitated by structural plasticity. J. Mol. Biol 2012, 423:413-426.
100. Ziermann R., Calendar R. Characterization of the cos sites of bacteriophages P2 and P4. Gene 1990, 96:9-15.