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Chapter 59 : Morphogenesis of Bacteriophage ϕ29

Authors: Dwight Anderson, Bernard Reilly
Content Type: Monograph
Publication Year: 1993

Category: Bacterial Pathogenesis; Microbial Genetics and Molecular Biology

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Morphogenesis of Bacteriophage ϕ29, Page 1 of 2

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Abstract:

Bacteriophages are very useful models for studying the protein-derived principles of form determination in virus assembly. Bacteriophage models cannot be ignored because of the assembly of the virus tail at the prohead portal vertex or connector, the entry point of double-stranded DNA. Bacteriophage ø29 of , illustrated in the family portrait with bacteriophage T2 of , features simplicity, efficient in vitro assembly, and advanced genetic and biochemical characterizations. This chapter emphasizes ø29 structure and the mechanisms of prohead assembly and DNA packaging, the major thrusts of current ø29 research in Minneapolis. The basic problem of ø29 morphogenesis is the mechanism by which a prolate shell of particular dimensions is assembled from subunits that are also capable of being assembled into incorrect structures. Mutants of asporogenous that cannot assemble ø29 (vam) were selected by the use of antibodies that reacted more strongly with the free connectors than with the portal vertex of proheads or phage. Bacteriophage DNA-packaging machines seem to have in common two packaging proteins and a connector with sixfold symmetry. Restriction enzyme digestion of DNA molecules extracted from DNase I-treated proheads shows that DNA-gp3 packaging is oriented with respect to the physical map. A gyrase action would be needed to generate supercoiled DNA for packaging.

Citation: Anderson D, Reilly B. 1993. Morphogenesis of Bacteriophage ϕ29, p 859-867. In Sonenshein A, Hoch J, Losick R (ed), and Other Gram-Positive Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555818388.ch59

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Morphogenesis of Bacteriophage ϕ29
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Citation: Anderson D, Reilly B. 1993. Morphogenesis of Bacteriophage ϕ29, p 859-867. In Sonenshein A, Hoch J, Losick R (ed), and Other Gram-Positive Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555818388.ch59
/content/10.1128/9781555818388.chap59.fig59-1
Figure 1

Family portrait of phages 29 and T2. Magnification, x 428,000.

10.1128/9781555818388/fig59-1_thmb.gif
10.1128/9781555818388/fig59-1.gif
Image of Figure 1
Figure 1

Family portrait of phages 29 and T2. Magnification, x 428,000.

Citation: Anderson D, Reilly B. 1993. Morphogenesis of Bacteriophage ϕ29, p 859-867. In Sonenshein A, Hoch J, Losick R (ed), and Other Gram-Positive Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555818388.ch59
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Figure 2

Pathway of 29 morphogenesis. Proteins composing a structure are listed below it. Prohead II and the 1¯, 12¯, and 13¯ particles are true intermediates in the pathway. The 10¯, 7¯, and 9¯ structures shown below the main pathway are abortive structures. Particle a has been observed only in restrictive 12(716) infection together with the 12¯ particle; its composition is inferred from morphology.

10.1128/9781555818388/fig59-2_thmb.gif
10.1128/9781555818388/fig59-2.gif
Image of Figure 2
Figure 2

Pathway of 29 morphogenesis. Proteins composing a structure are listed below it. Prohead II and the 1¯, 12¯, and 13¯ particles are true intermediates in the pathway. The 10¯, 7¯, and 9¯ structures shown below the main pathway are abortive structures. Particle a has been observed only in restrictive 12(716) infection together with the 12¯ particle; its composition is inferred from morphology.

Citation: Anderson D, Reilly B. 1993. Morphogenesis of Bacteriophage ϕ29, p 859-867. In Sonenshein A, Hoch J, Losick R (ed), and Other Gram-Positive Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555818388.ch59
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Figure 3

Three views of the modified ? = 3 model of the 29 prohead according to S. Casjens and R. Hendrix. The model contains 30 hexamers (light) and 11 pentamers (dark) of the major capsid protein. The panel on the right shows a view of the base, where the connector (not shown) is attached. The computer-generated schematics are by E. Egelman.

10.1128/9781555818388/fig59-3_thmb.gif
10.1128/9781555818388/fig59-3.gif
Image of Figure 3
Figure 3

Three views of the modified ? = 3 model of the 29 prohead according to S. Casjens and R. Hendrix. The model contains 30 hexamers (light) and 11 pentamers (dark) of the major capsid protein. The panel on the right shows a view of the base, where the connector (not shown) is attached. The computer-generated schematics are by E. Egelman.

Citation: Anderson D, Reilly B. 1993. Morphogenesis of Bacteriophage ϕ29, p 859-867. In Sonenshein A, Hoch J, Losick R (ed), and Other Gram-Positive Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555818388.ch59
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Figure 4

Secondary structure of 29 pRNA derived by phylogenetic analysis ( ). A through F, helical stems. Residues conserved in the 29-???, M2-Nf, SF5, and GA1 pRNA sequences are designated in boldface letters.

10.1128/9781555818388/fig59-4_thmb.gif
10.1128/9781555818388/fig59-4.gif
Image of Figure 4
Figure 4

Secondary structure of 29 pRNA derived by phylogenetic analysis ( ). A through F, helical stems. Residues conserved in the 29-???, M2-Nf, SF5, and GA1 pRNA sequences are designated in boldface letters.

Citation: Anderson D, Reilly B. 1993. Morphogenesis of Bacteriophage ϕ29, p 859-867. In Sonenshein A, Hoch J, Losick R (ed), and Other Gram-Positive Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555818388.ch59
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References

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1. Anderson, D.,, and J. W. Bodley. 1990. Role of RNA in bacteriophage ø29 DNA packaging. J. Struct. Biol. 104: 70– 74.
2. Anderson, D. L.,, D. D. Hickman,, and B. E. Reilly. 1966. Structure of Bacillus subtilis bacteriophage ø29 and the length of ø29 deoxyribonucleic acid. J. Bacteriol. 91: 2081– 2089.
3. Anderson, D. L.,, and B. E. Reilly. 1974. Analysis of bacteriophage ø29 gene function: protein synthesis in suppressor-sensitive mutant infection of Bacillus subtilis. J. Virol. 13: 211– 221.
4. Atz, R.,, and D. Anderson. Unpublished data.
5. Atz, R.,, B. Rajagopal,, and D. Anderson. Unpublished data.
6. Bailey, S.,, J. Wichitwechkarn,, D. Johnson,, B. E. Reilly,, D. L. Anderson,, and J. W. Bodley. 1990. Phylogenetic analysis and secondary structure of the Bacillus subtilis bacteriophage RNA required for DNA packaging . J. Biol. Chem. 265: 22365– 22370.
7. Baker, T. S. ( Purdue University). 1990. Personal communication.1992
8. Bjornsti, M. A.,, B. E. Reilly,, and D. L. Anderson. 1981. In vitro assembly of the Bacillus subtilis bacteriophage ø29. Proc. Natl. Acad. Set. USA 78: 5861– 5865.
9. Bjornsti, M. A.,, B. E. Reilly,, and D. L. Anderson. 1983. Morphogenesis of bacteriophage ø29 of Bacillus subtilis: oriented and quantized in vitro packaging of DNA-gp3. J. Virol. 45: 383– 396.
10. Bjornsti, M. A.,, B. E. Reilly,, and D. L. Anderson. 1984. Bacteriophage ø29 proteins required for in vitro DNA-gp3 packaging. J. Virol. 50: 766– 772.
11. Burns, C. M.,, H. L. B. Chan,, and M. S. DuBow. 1990. In vitro maturation and encapsidation of the DNA of trans-posable Mu-like phage D108. Proc. Natl. Acad. Sci. USA 87: 6092– 6096.
12. Carazo, J. M.,, L. E. Donate,, L. Herranz,, J. P. Secilla,, and J. L. Carrascosa. 1986. Three-dimensional reconstruction of the connector of bacteriophage ø29 at 1.8 nm resolution. J. Mol. Biol. 192: 853– 867.
13. Carazo, J. M.,, A. Santisteban,, and J. L. Carrascosa. 1985. Three-dimensional reconstruction of bacteriophage ø29 neck particles at 2.2 nm resolution . J. Mol. Biol. 183: 79– 88.
14. Carrascosa, J. L.,, J. M. Carazo,, and N. Garcia. 1983. Structural localization of the proteins of the head to tail connecting region of bacteriophage ø29. Virology 124: 133– 143.
15. Carrascosa, J. L.,, E. Mendez,, J. Corral,, V. Rubio,, G. Ramirez,, M. Salas,, and E. Vinuela. 1981. Structural organization of Bacillus subtilis phage ø29. A model. Virology 111: 401– 413.
16. Carrascosa, J. L.,, E. Vinuela,, N. Garcia,, and A. Santisteban. 1982. Structure of the head-tail connector of bacteriophage ø29. J. Mol. Biol. 154: 311– 324.
17. Davison, B. L.,, T. Leighton,, and J. C. Rabinowltz. 1979. Purification of Bacillus subtilis RNA polymerase with heparin-agarose. J. Biol. Chem. 254: 9220– 9226.
18. Dot, R. ( University of California, Davis). 1991. Personal communication.1992
19. Donate, L. E.,, and J. L. Carrascosa. 1991. Characterization of a versatile in vitro DNA-packaging system based on hybrid lambda/ ø29 proheads. Virology 182: 534– 544.
20. Donate, L. E.,, H. Murialdo,, and J. L. Carrascosa. 1990. Production of lambda- ø29 phage chimeras. Virology 179: 936– 940.
21. Garcia, J. A.,, E. Mendez,, and M. Salas. 1984. Cloning, nucleotide sequence and high level expression of the gene coding for the connector protein of Bacillus subtilis phage ø29. Gene 30: 87– 98.
22. Grimes, S.,, and D. Anderson. 1989. In vitro packaging of bacteriophage ø29 DNA restriction fragments and the role of the terminal protein gp3. J. Mol. Biol. 209: 91– 100.
23. Grimes, S.,, and D. Anderson. 1989. Cleaving the prohead RNA of bacteriophage ø29 alters the in vitro packaging of restriction fragments of DNA-gp3. J. Mol. Biol. 209: 101– 108.
24. Grimes, S.,, and D. Anderson. 1990. RNA dependence of the bacteriophage ø29 DNA packaging ATPase. J. Mol. Biol. 215: 559– 566.
25. Grimes, S.,, P. Guo,, C. Peterson,, and D. Anderson. 1986. Protein stoichiometry and biological activity of ø29 proheads. Abstr. Xth Biennial Meet. Bacteriophage Assembly 1986.
26. Guo, P.,, and D. Anderson. Unpublished data.
27. Guo, P.,, S. Bailey,, J. W. Bodley,, and D. Anderson. 1987. Characterization of the small RNA of the bacteriophage ø29 DNA packaging machine. Nucleic Acids Res. 15: 7081– 7090.
28. Guo, P.,, S. Erickson,, and D. Anderson. 1987. A small viral RNA is required for in vitro packaging of bacteriophage ø29 DNA . Science 236: 690– 694.
29. Guo, P.,, S. Erickson,, W. Xu,, N. Olson,, T. S. Baker,, and D. Anderson. 1991. Regulation of the phage ø29 prohead shape and size by the portal vertex. Virology 183: 366– 373.
30. Guo, P.,, S. Grimes,, and D. Anderson. 1986. A defined system for in vitro packaging of DNA-gp3 of the Bacillus subtilis bacteriophage ø29. Proc. Natl. Acad. Sci. USA 83: 3505– 3509.
31. Guo, P.,, C. Peterson,, and D. Anderson. 1987. Initiation events in in vitro packaging of bacteriophage ø29 DNA-gp3. J. Mol. Biol. 197: 219– 228.
32. Guo, P.,, C. Peterson,, and D. Anderson. 1987. Prohead and DNA-gp3-dependent ATPase activity of the DNA packaging protein gp16 of bacteriophage ø29. J. Mol. Biol. 197: 229– 236.
33. Guo, P.,, B. S. Rajagopal,, D. Anderson,, S. Erickson,, and C.-S. Lee. 1991. sRNA of phage ø29 of Bacillus subtilis mediates DNA packaging of ø29 proheads assembled in Escherichia coli. Virology 185: 395– 400.
34. Hagen, E. W.,, B. E. Reilly,, M. E. Tosi,, and D. L. Anderson. 1976. Analysis of gene function of bacteriophage ø29 of Bacillus subtilis: identification of cistrons essential for viral assembly. J. Virol. 19: 501– 517.
35. Haggard, E.,, C. Hailing,, and R. Calendar. 1991. DNA sequence of three tail genes of bacteriophage P2: further evidence for horizontal transfer of tail fiber genes among unrelated bacteriophages. Abstr. XIIth Int. Conf. Bacteriophage Assembly 1991.
36. Hendrix, R.,, Z. Xie,, R. Duda,, and K. Martincic. 1991. Genetics of HK97 head assembly and in vitro shell assembly. Abstr. XIIth Int. Conf. Bacteriophage Assembly 1991.
37. Hendrix, R. W. 1978. Symmetry mismatch and DNA packaging in large bacteriophages. Proc. Natl. Acad. Sci. USA 75: 4779– 4783.
38. Hendrix, R. W., 1985. Shape determination in virus assembly: the bacteriophage example, p. 170– 203. In S. Casjens (ed.). Virus Structure and Assembly. Jones and Bartlett, Portola Valley, Calif.
39. Herranz, L.,, J. Bordas,, E. Towns-Andrews,, E. Mendez,, P. Usobiaga,, and J. L. Carrascosa. 1990. Conformational changes in bacteriophage ø29 connector prevents DNA-binding activity. J. Mol. Biol. 213: 263– 273.
40. Kellenberger, E. 1990. Form determination of the heads of bacteriophages. Eur. I. Biochem. 190: 233– 248.
41. Mellado, R. P.,, F. Moreno,, E. Vinuela,, M. Salas,, B. E. Reilly,, and D. L. Anderson. 1976. Genetic analysis of bacteriophage ø29 of Bacillus subtilis: integration and mapping of reference mutants of two collections. J. Virol. 19: 495– 500.
42. Nelson, R. A.,, B. E. Reilly,, and D. L. Anderson. 1976. Morphogenesis of bacteriophage ø29 of Bacillus subtilis: preliminary isolation and characterization of intermediate particles of the assembly pathway. J. Virol. 19: 518– 532.
43. Olson, N. H.,, W. Xu,, W. D. Grochulskl,, D. L. Anderson,, and T. S. Baker. 1990. Electron microscopy of negatively stained and frozen-hydrated bacteriophage ø29, abstr, p. 270. Abstr. Proc. XIIth Int. Congr. Electron Microscopy 1990.
44. Peterson, C.,, R. Atz,, and D. Anderson. Unpublished data.
45. Peterson, C.,, R. Atz,, M. Simon,, E. Egelman,, and D. Anderson. Unpublished data.
46. Peterson, C.,, S. Grimes,, and D. Anderson. Unpublished data.
47. Peterson, C.,, S. Grimes,, R. Atz,, E. Egelman,, and D. Anderson. 1991. The mass, composition and biological activity of ϕ29 proheads. Abstr. XIIth Int. Conf. Bacteriophage Assembly 1991.
48. Rajagopal, B.,, B. Reilly,, and D. Anderson. 1991. Bacillus subtilis participation in phage ϕ29 assembly. Abstr. XIIth Int. Conf. Bacteriophage Assembly 1991.
49. Rajagopal, B.,, B. Reilly,, and D. Anderson. Unpublished data.
50. Reid, R.,, J. Wichitwechkarn,, and D. Anderson. 1991. Structure and function of phage ϕ29 prohead RNA in DNA-gp3 packaging. Abstr. XIIth Int. Conf. Bacteriophage Assembly 1991.
51. Rajagopal, B.,, B. Reilly,, and D. Anderson. 1977. Morphogenesis of bacteriophage ϕ29 of Bacillus subtilis: mapping and functional analysis of the head fiber gene. J. Virol. 24: 363– 377.
52. Reilly, B. E.,, and J. Spizizen. 1965. Bacteriophage deox-yribonucleate infection of competent Bacillus subtilis. J. Bacteriol. 89: 782– 790.
53. Reilly, B. E.,, M. E. Tosi,, and D. L. Anderson. 1975. Genetic analysis of bacteriophage ø29 of Bacillus subtilis: mapping of the cistrons coding for structural proteins. J. Virol. 16: 1010– 1016.
54. Sogo, J. M.,, M. R. Inciarte,, J. Corral,, E. Vinuela,, and M. Salas. 1979. RNA polymerase binding sites and transcription map of the DNA of Bacillus subtilis phage ø29. J. Mol. Biol. 127: 411– 436.
55. Thacker, K. 1984. Ph.D. thesis. University of Minnesota, Minneapolis.1992
56. Tosi, M.,, and D. L. Anderson. 1973. Antigenic properties of bacteriophage ø29 structural proteins. J. Virol. 12: 1548– 1559.
57. Tosi, M. E.,, B. E. Reilly,, and D. L. Anderson. 1975. Morphogenesis of bacteriophage ø29 of Bacillus subtilis: cleavage and assembly of the neck appendage protein. J. Virol. 16: 1282– 1295.
58. Turnquist, S.,, M. Simon,, E. Egelman,, and D. Anderson. 1992. Supercoiled DNA wraps around the bacteriophage ø29 head-tail connector. Proc. Natl. Acad. Set. USA 89: 10479– 10483.
59. Turnquist, S.,, D. Thomas,, and D. Anderson. Unpublished data.
60. Vinuela, E.,, A. Camacho,, F. Jimenez,, J. L. Carrascosa,, G. Ramirez,, and M. Salas. 1976. Structure and assembly of phage ø29. Phil. Trans. R. Soc. Lond. Sect. B 276: 29– 35.
61. Wetzstein, M.,, U. Volker,, J. Dedio,, U. Zuber,, C. Herget,, A. Schmidt,, M. Hecker,, and W. Schumann. 1991. Analysis of the heat shock response of Bacillus subtilis. Abstr. 6th Int. Conf. Bacilli 1991.
62. Wichitwechkarn, J.,, S. Bailey,, J. W. Bodley,, and D. Anderson. 1989. Prohead RNA of bacteriophage ø29: size, stoichiometry and biological activity. Nucleic Acids Res. 17: 3459– 3468.
63. Wichitwechkarn, J.,, D. Johnson,, and D. Anderson. 1992. Mutant prohead RNAs in the in vitro packaging of bacteriophage ø29 DNA-gp3. J. Mol. Biol. 223: 991– 998.

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