Abstract
Tailed-bacteriophage virions contain a single linear dsDNA chromosome which can range in size from about 18 to 500 kbp across the known tailed-phage types. These linear chromosomes can have one of several known types of termini as follows: cohesive ends (\(5^{\prime}\)- or \(3^{\prime}\)-single-strand extensions), circularly permuted direct terminal repeats, short or long exact direct terminal repeats, terminal host DNA sequences, or covalently bound terminal proteins. These different types of ends reflect differing DNA replication strategies and especially differing terminase actions during DNA packaging. In general, complete genome sequence determination does not by itself elucidate the nature of these ends, so directed experimental analysis is usually required to understand the nature of the virion chromosome ends. This chapter discusses these methods.
Key Words
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Mousset, S. & Thomas, R. (1969) Ter, a function which generates the ends of the mature lambda chromosome. Nature 221, 242–244.
Feiss, M. & Campbell, A. (1974) Duplication of the bacteriophage lambda cohesive end site: genetic studies. J. Mol. Biol. 83, 527–540.
Jackson, E. N., Jackson, D. A. & Deans, R. J. (1978) EcoRI analysis of bacteriophage P22 DNA packaging. J. Mol. Biol. 118, 365–388.
Emmons, S. W. (1974) Bacteriophage lambda derivatives carrying two copies of the cohesive end site. J. Mol. Biol. 83, 511–525.
Adams, M. B., Hayden, M. & Casjens, S. (1983) On the sequential packaging of bacteriophage P22 DNA. J. Virol. 46, 673–677.
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. (2000) Structure of the bacteriophage f29 DNA packaging motor. Nature 408, 745–750.
Hershey, A. D. & Burgi, E. (1965) Complementary structure of interacting sites at the ends of lambda DNA molecules. Proc. Natl. Acad. Sci. USA 53, 325–330.
Wu, R. & Taylor, E. (1971) Nucleotide sequence analysis of DNA. II. Complete nucleotide sequence of the cohesive ends of bacteriophage lambda DNA. J. Mol. Biol. 57, 491–511.
Ellis, D. M. & Dean, D. H. (1985) Nucleotide sequence of the cohesive single-stranded ends of Bacillus subtilis temperate bacteriophage f105. J. Virol. 55, 513–515.
Padmanabhan, R., Wu, R. & Calendar, R. (1974) Complete nucleotide sequence of the cohesive ends of bacteriophage P2 deoxyribonucleic acid. J. Biol. Chem. 249, 6197–6207.
Fitzmaurice, W. P., Waldman, A. S., Benjamin, R. C., Huang, P. C. & Scocca, J. J. (1984) Nucleotide sequence and properties of the cohesive DNA termini from bacteriophage HP1c1 of Haemophilus influenzae Rd. Gene 31, 197–203.
Juhala, R. J., Ford, M. E., Duda, R. L., Youlton, A., Hatfull, G. F. & Hendrix, R. W. (2000) Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J. Mol. Biol. 299, 27–51.
Casjens, S. (2003) Prophages in bacterial genomics: What have we learned so far? Molec. Microbiol. 249, 277–300.
Hatfull, G. F. & Sarkis, G. J. (1993) DNA sequence, structure and gene expression of mycobacteriophage L5: a phage system for mycobacterial genetics. Molec. Microbiol. 7, 395–405.
Ford, M. E., Sarkis, G. J., Belanger, A. E., Hendrix, R. W. & Hatfull, G. F. (1998) Genome structure of mycobacteriophage D29: implications for phage evolution. J. Mol. Biol. 279, 143–164.
Lubbers, M., Ward, L., Beresford, T., Jarvis, B. & Jarvis, A. (1994) Sequencing and analysis of the cos region of the lactococcal bacteriophage c2. Mol. Gen. Genet. 245, 160–166.
van Sinderen, D., Karsens, H., Kok, J., Terpstra, P., Ruiters, M. H., Venema, G. & Nauta, A. (1996) Sequence analysis and molecular characterization of the temperate lactococcal bacteriophage r1t. Molec. Microbiol. 19, 1343–1355.
Streisinger, G., Enrich, J. & Stahl, M. (1967) Chromosome structure in T4. III. Terminal redundancy and length determination. Proc. Natl’l. Acad. Sci., U.S.A. 57, 292–295.
Wu, H., Sampson, L., Parr, R. & Casjens, S. (2002) The DNA site utilized by bacteriophage P22 for initiation of DNA packaging. Molec. Microbiol. 45, 1631–1646.
Tye, B. K., Huberman, J. A. & Botstein, D. (1974) Non-random circular permutation of phage P22 DNA. J. Mol. Biol. 85, 501–528.
Moore, S. D. & Prevelige, P. E., Jr. (2002) Bacteriophage P22 portal vertex formation in vivo. J. Mol. Biol. 315, 975–994.
Weigele, P. R., Sampson, L., Winn-Stapley, D. & Casjens, S. R. (2005) Molecular genetics of bacteriophage P22 scaffolding protein’s functional domains. J. Mol. Biol. 348, 831–844.
Casjens, S. & Hayden, M. (1988) Analysis in vivo of the bacteriophage P22 headful nuclease. J. Mol. Biol. 199, 467–474.
Schmieger, H., Taleghani, K. M., Meierl, A. & Weiss, L. (1990) A molecular analysis of terminase cuts in headful packaging of Salmonella phage P22. Mol. Gen. Genet. 221, 199–202.
Chow, L. T. & Bukhari, A. I. (1978) Heteroduplex electron microscopy of phage Mu mutants containing IS1 insertions and chloramphenicol resistance transposons. Gene 3, 333–346.
Humphreys, G. O. & Trautner, T. A. (1981) Maturation of bacteriophage SPPI DNA: limited precision in the sizing of mature bacteriophage genomes. J. Virol. 37, 832–835.
Casjens, S. & Huang, W. M. (1982) Initiation of sequential packaging of bacteriophage P22 DNA. J. Mol. Biol. 157, 287–298.
Deichelbohrer, I., Alonso, J. C., Luder, G. & Trautner, T. A. (1985) Plasmid transduction by Bacillus subtilis bacteriophage SPP1: effects of DNA homology between plasmid and bacteriophage. J. Bacteriol. 162, 1238–1243.
Sternberg, N. & Coulby, J. (1987) Recognition and cleavage of the bacteriophage P1 packaging site (pac). II. Functional limits of pac and location of pac cleavage termini. J. Mol. Biol. 194, 469–479.
Casjens, S., Sampson, L., Randall, S., Eppler, K., Wu, H., Petri, J. B. & Schmieger, H. (1992) Molecular genetic analysis of bacteriophage P22 gene 3 product, a protein involved in the initiation of headful DNA packaging. J. Mol. Biol. 227, 1086–1099.
Casjens, S., Winn-Stapley, D., Gilcrease, E., Moreno, R., Kühlewein, C., Chua, J. E., Manning, P. A., Inwood, W. & Clark, A. J. (2004) The chromosome of Shigella flexneri bacteriophage Sf6: complete nucleotide sequence, genetic mosaicism, and DNA packaging. J. Mol. Biol. 339, 379–394.
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. (2005) The generalized transducing Salmonella bacteriophage ES18: complete genome sequence and DNA packaging strategy. J. Bacteriol. 187, 1091–1104.
Chow, L. T. & Bukhari, A. I. (1977). Bacteriophage Mu genome: structural studies on Mu DNA and Mu mutants carrying insertions. In DNA insertion elements, plasmids, and episomes (Bukhari, A. I., Shapiro, J. A. & Adhya, S. L., eds.), pp. 295–306. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
Sternberg, N. (1986) The production of generalized transducing phage by bacteriophage lambda. Gene 50, 69–85.
Bachi, B. & Arber, W. (1977) Physical mapping of BglII, BamHI, EcoRI, HindIII and PstI restriction fragments of bacteriophage P1 DNA. Mol. Gen. Genet. 153, 311–324.
Lin, H. & Black, L. W. (1998) DNA requirements in vivo for phage T4 packaging. Virology 242, 118–127.
Obregon, V., Garcia, J. L., Garcia, E., Lopez, R. & Garcia, P. (2004) Peculiarities of the DNA of MM1, a temperate phage of Streptococcus pneumoniae. Int. Microbiol. 7, 133–137.
Loessner, M. J., Inman, R. B., Lauer, P. & Calendar, R. (2000) Complete nucleotide sequence, molecular analysis and genome structure of bacteriophage A118 of Listeria monocytogenes: implications for phage evolution. Molec. Microbiol. 35, 324–340.
Plunkett, G., 3rd, Rose, D. J., Durfee, T. J. & Blattner, F. R. (1999) Sequence of Shiga toxin 2 phage 933 W from Escherichia coli O157:H7: Shiga toxin as a phage late-gene product. J. Bacteriol. 181, 1767–1778.
Chung, Y. B., Nardone, C. & Hinkle, D. C. (1990) Bacteriophage T7 DNA packaging. III. A “hairpin” end formed on T7 concatemers may be an intermediate in the processing reaction. J. Mol. Biol. 216, 939–948.
Zhang, X. & Studier, F. W. (2004) Multiple roles of T7 RNA polymerase and T7 lysozyme during bacteriophage T7 infection. J. Mol. Biol. 340, 707–730.
Dunn, J. & Studier, W. (1983) Complete nucleotide sequence of bacteriophage T7 DNA and the locations of T7 genetic elements. J. Mol. Biol. 166, 477–535.
Dobbins, A. T., George, M., Jr., Basham, D. A., Ford, M. E., Houtz, J. M., Pedulla, M. L., Lawrence, J. G., Hatfull, G. F. & Hendrix, R. W. (2004) Complete genomic sequence of the virulent Salmonella bacteriophage SP6. J. Bacteriol. 186, 1933–1944.
Scholl, D., Kieleczawa, J., Kemp, P., Rush, J., Richardson, C. C., Merril, C., Adhya, S. & Molineux, I. J. (2004) Genomic analysis of bacteriophages SP6 and K1-5, an estranged subgroup of the T7 supergroup. J. Mol. Biol. 335, 1151–1171.
Wang, J., Jiang, Y., Vincent, M., Sun, Y., Yu, H., Wang, J., Bao, Q., Kong, H. & Hu, S. (2005) Complete genome sequence of bacteriophage T5. Virology 332, 45–65.
Fischhoff, D., MacNeil, D. & Kleckner, N. (1976) Terminal redundancy heterozygotes involving the first-step-transfer region of the bacteriophage T5 chromosome. Genetics 82, 145–159.
Cregg, J. M. & Stewart, C. R. (1978) Terminal redundancy of “high frequency of recombination” markers of Bacillus subtilis phage SPO1. Virology 86, 530–541.
Rhoades, M. & Rhoades, E. A. (1972) Terminal repetition in the DNA of bacteriophage T5. J. Mol. Biol. 69, 187–200.
Perkus, M. E. & Shub, D. A. (1985) Mapping the genes in the terminal redundancy of bacteriophage SPO1 with restriction endonucleases. J. Virol. 56, 40–48.
Wiest, J. S. & McCorquodale, D. J. (1990) Characterization of pre-early genes in the terminal repetition of bacteriophage BF23 DNA by nucleotide sequencing and restriction mapping. Virology 177, 745–754.
Panganiban, A. T. & Whiteley, H. R. (1983) Bacillus subtilis RNAase III cleavage sites in phage SP82 early mRNA. Cell 33, 907–913.
George, M. & Bukhari, A. I. (1981) Heterogeneous host DNA attached to the left end of mature bacteriophage Mu DNA. Nature 292, 175–176.
Groenen, M. A. & van de Putte, P. (1985) Mapping of a site for packaging of bacteriophage Mu DNA. Virology 144, 520–522.
Bukhari, A. I. & Taylor, A. L. (1975) Influence of insertions on packaging of host sequences covalently linked to bacteriophage Mu DNA. Proc. Natl. Acad. Sci., U S A 72, 4399–4403.
Morgan, G., Hatfull, G., Casjens, S. & Hendrix, R. (2002) Bacteriophage Mu genome sequence: analysis and comparison with Mu-like prophages in Haemophilus, Neisseria and Deinococcus. J. Mol. Biol. 317, 337–359.
Summer, E. J., Gonzalez, C. F., Carlisle, T., Mebane, L. M., Cass, A. M., Savva, C. G., LiPuma, J. & Young, R. (2004) Burkholderia cenocepacia phage BcepMu and a family of Mu-like phages encoding potential pathogenesis factors. J. Mol. Biol. 340, 49–65.
Ito, J. (1978) Bacteriophage f29 terminal protein: its association with the \(5^{\prime}\) termini of the f29 genome. J. Virol. 28, 895–904.
Salas, M., Mellado, R. P. & Vinuela, E. (1978) Characterization of a protein covalently linked to the \(5^{\prime}\) termini of the DNA of Bacillus subtilis phage f29. J. Mol. Biol. 119, 269–291.
Jeanmougin, F., Thompson, J. D., Gouy, M., Higgins, D. G. & Gibson, T. J. (1998) Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23, 403–405.
Maniatis, T., Fritsch, E. & Sambrook, J. (1982). Molecular cloning A laboratory manual, pp. pp150–163. Cold Spring Harbor Labortory, Cold Spring Harbor, NY.
Southern, E. (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol. 98, 503–517.
Earnshaw, W., Casjens, S. & Harrison, S. (1976) Assembly of the head of bacteriophage P22, X-ray diffraction from heads, proheads and related structures. J. Mol. Biol. 104, 387–410.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2009 Humana Press, a part of Springer Science+Business Media, LLC
About this protocol
Cite this protocol
Casjens, S.R., Gilcrease, E.B. (2009). Determining DNA Packaging Strategy by Analysis of the Termini of the Chromosomes in Tailed-Bacteriophage Virions. In: Clokie, M.R., Kropinski, A.M. (eds) Bacteriophages. Methods in Molecular Biology™, vol 502. Humana Press. https://doi.org/10.1007/978-1-60327-565-1_7
Download citation
DOI: https://doi.org/10.1007/978-1-60327-565-1_7
Publisher Name: Humana Press
Print ISBN: 978-1-60327-564-4
Online ISBN: 978-1-60327-565-1
eBook Packages: Springer Protocols