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The functions of the phage T4 immunity and spackle genes in genetic exclusion

Published online by Cambridge University Press:  14 April 2009

John W. Obringer
John W. Obringer
Affiliation:
Department of Microbiology and Immunology, College of Medicine, University of ArizonaTucson AZ 85724
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Summary

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Genetic exclusion is the ability of a primary infecting phage to prevent a secondary infecting phage from contributing its genetic information to the progeny. The molecular mechanism of the phenomenon is not well understood. The two genes in phage T4 mainly responsible for genetic exclusion are the immunity (imm) gene and the spackle (sp) gene. Evidence is presented that the imm gp enables the host exonuclease V to degrade superinfecting phage DNA. This appears to be accomplished by the imm gp altering gp 2/64, the presumed pilot protein, which protects the 5′ end(s) of the phage DNA. Exonuclease III is also involved in genetic exclusion but its action does not appear to depend upon the imm or sp gene products. Gp sp appears to interfere with the lysozyme activity of gp 5, a component of the central base plug, postulated to aid in tail tube penetration during the injection process. A molecular model of genetic exclusion is proposed. Genes imm and sp are part of a cluster of genes which also includes 42, beta-glucosyltransferase, and uvsX. The genes of this cluster encode proteins apparently adapted for competition and defence at the DNA level. These genes may encode fundamental adaptive strategies found throughout nature.

Type
Research Article
Information
Genetics Research , Volume 52 , Issue 2 , October 1988 , pp. 81 - 90
Copyright
Copyright © Cambridge University Press 1988

References

Amundsen, S. K., Taylor, A. F., Chaudhury, A. M. & Smith, G. R. (1986). recD: The gene for an essential third subunit of exonuclease V. Proceedings of the National Academy of Sciences, (USA) 83, 5558–5562.Google Scholar
Anderson, C. W. & Eigner, J. (1971). Breakdown and exclusion of superinfecting T-even bacteriophage in Escherichia coli. J. Virology 8, 869–886.Google Scholar
Anderson, C. W., Williamson, J. R. & Eigner, J. (1971). Localization of parental deoxyribonucleic acid from superinfecting T4 bacteriophage in Escherichia coli. Journal of Virology 8, 887–893.Google Scholar
Bayer, M. E. (1968). Adsorption of bacteriophages to adhesions between wall and membrane of Escherichia coli. Virology 2(4), 346–356.Google Scholar
Bayer, M. H. (1970). Adsorption and superinfection and bacteriophage T2 as seen with the electron microscope. Biophysics Society Abstracts p. 268a.Google Scholar
Behme, M. T., Lilley, G. D. & Ebisuzaki, K. (1976). Postinfection control by bacteriophage of T4 of E. coli. rec BC nuclease activity. Journal of Virology 18, 20–25.Google Scholar
Bernstein, C. (1987). Damage in DNA of an infecting phage T4 shifts reproduction from asexual to sexual allowing rescue of its genes. Genetical Research 49(3), 183–190.Google Scholar
Bernstein, C. & Wallace, S. S. (1983). DNA repair in Bacteriophage T4 (ed. Matthews, C. K., Kutter, E. M., Mosig, G. and Berget, P. B. pp. 138–151. Washington, D.C.: American Society for Microbiology.Google Scholar
Birge, E. A. (1982). Bacterial and Bacteriophage Genetics New York: Springer-Verlag.Google Scholar
Childs, J. D. (1970). Superinfection exclusion by petit T4 bacteriophage. Canadian Journal of Genetics and Cytology 12, 377.Google Scholar
Childs, J. D. (1973). Superinfection exclusion by incomplete genomes of bacteriophage T4. Journal of Virology 11, 1–8.Google Scholar
Clowes, R. C. & Hayes, W. (1968). Experiments in Microbial Genetics New York: John Wiley and Sons.Google Scholar
Cornett, J. B. (1974). Spackle and immunity functions of bacteriophage T4. Journal of Virology 13, 312–321.Google Scholar
Dulbecco, R. (1952). Mutual exclusion between related phages. Journal of Bacteriology 63, 209–217.CrossRefGoogle ScholarPubMed
Emrich, J. (1968). Lysis of T4-infected bacteria in the absence of lysozyme. Virology 35, 158–165.Google Scholar
Fielding, P. E. & Lunt, M. R. (1970). The relationship between breakdown of superinfecting virus deoxyribo-nucleic acid and temporal exclusion induced by T4 and T5 bacteriophages. Journal of General Virology 6, 333–342.Google Scholar
French, R. C., Lesley, S. M., Graham, A. F. & van Rooyen, C. E. (1952). Studies on the relationship between virus and host cell. III. The breakdown of T2r+ upon infection of its host. Canadian Journal of Medical Science 29, 108–143.Google Scholar
Fujisawa, H., Yonesaki, T. & Minagawa, T. (1985). Sequence of the T4 recombination gene, uvsX, and its comparison with that of the recA gene of E. coli. Nucleic Acids Research 13(20), 7473–7481.Google Scholar
Goldberg, E. (1983). Recognition, attachment and injection. in Bacteriophage T4 (ed. Matthews, C. K., Kutter, E. M., Mosig, G. and Berget, P. B.). pp. 32–39. Washington, D.C.: American Society for Microbiology.Google Scholar
Granboulan, P. J., Sechaud, J. & Kellenberger, E. (1968). On the fragility of phage T4-related particles. Virology 46, 407–425.Google Scholar
Kao, S. & McClain, W. H. (1980 a). Baseplate protein of bacteriophage T4 with both structural and lytic functions. Journal of Virology 34, 95–103.Google Scholar
Kao, S. & McClain, W. H. (1980 b). Roles of bacteriophage gene 5 and gene s products in cell lysis. Journal of Virology 34, 104–107.Google Scholar
Kikuchi, Y., & King, J. (1975). Genetic control of bacteriophage T4 baseplate morphogenesis. I. Sequential assembly of the major precursor, in vivo and in vitro. Journal of Molecular Biology 99, 645–672.CrossRefGoogle ScholarPubMed
Kornberg, A. (1974). DNA Synthesis, pp. 240–241. San Francisco: W. H. Freeman and Co.Google Scholar
Kutter, E. & Ruger, W. (1985). Bacteriophage T4 genomic map-August, 1985. Abstracts of the 1985 Evergreen International Bacteriophage T4 Meeting, Evergreen State College, Olympia, Wa.Google Scholar
Mahmood, N. & Lund, M. R. (1972). Biochemical changes during mixed infections with bacteriophages T2 and T4. Journal of General Virology 16, 185–197.CrossRefGoogle ScholarPubMed
Maniatis, T., Fritsch, E. F. & Sambrook, J. (1982). Molecular Cloning: a Laboratory Manual Cold Spring Harbor Laboratory.Google Scholar
Milne, A. (1961). Definition of competition among animals. Symposium of the Society of Experimental Biology 15, 40.Google Scholar
Mufti, S. (1972). A bacteriophage mutant defective in protection against superinfecting phage. Journal of General Virology 17, 119–123.Google Scholar
Nakagawa, H., Arisaka, F. & Ishii, S. (1985). Isolation and characterization of the bacteriophage T4 tail-associated lysozyme. Journal of Virology 54(2), 460–466.Google Scholar
O'Farrell, P. Z. & Gold, L. M. (1973). The identification of prereplicative bacteriophage T4 proteins. Journal of Biological Chemistry 248, 5499–5501.CrossRefGoogle ScholarPubMed
Okamoto, K. (1973). Role of T4 phage-directed protein in the establishment of resistance to T4 ghosts. Virology 56, 595–603.Google Scholar
Peterson, R. F., Cohen, P. S. & Ennis, H. L. (1972). Properties of phage T4 messenger RNA synthesized in the absence of protein synthesis. Virology 48, 201–206.CrossRefGoogle ScholarPubMed
Revel, H. R. (1983). DNA modification: glucosylation. In Bacteriophage T4 (ed. Matthews, C. K., Kutter, E. M., Mosig, G. and Berget, P. B.), pp. 156–165. Washington, D.C.: American Society for Microbiology.Google Scholar
Sauri, C. J. & Earhart, C. F. (1971). Superinfection in bacteriophage T4: inverse relationship between genetic exclusion and membrane association of deoxyribonucleic acid of secondary bacteriophage. Journal of Virology 8, 856–859.Google Scholar
Silverstein, J. L. & Goldberg, E. B. (1976 a). T4 injection. I. Growth cycle of a gene 2 mutant. Virology 72, 195–211.Google Scholar
Silverstein, J. L. & Goldberg, E. B. (1976 b). T4 injection. II. Protection of entering DNA from the host exonuclease V. Virology 72, 212–223.Google Scholar
Smith, R. L. (1966). Ecology and Field Biology, pp. 424–484. New York: Harper and Row.Google Scholar
Stahl, F. W. & Murray, N. E. (1966). The evolution of gene clusters and genetic circularity in microorganisms. Genetics 53, 569–576.CrossRefGoogle ScholarPubMed
Steinberg, C. M. & Edgar, R. S. (1962). A critical test of a current theory of recombination in bacteriophage. Genetics 47, 187–208.Google Scholar
Telander-Muskavitch, K. M. & Linn, S. (1981). In The Enzymes, Vol. 14 (ed. Boyer, P. D.), pp. 233–250. New York: Academic Press.Google Scholar
Vallee, M. & Cornett, J. B. (1972). A new gene of bacteriophage T4 determining immunity against super-infecting ghosts and phage in T4-infected Escherichia coli. Virology 48, 777–784.Google Scholar
Vallee, M., Cornett, J. B. & Bernstein, H. (1972). The action of bacteriophage T4 ghosts on Escherichia coli and the immunity to this action developed in cells preinfected with T4. Virology 48, 766–776.CrossRefGoogle ScholarPubMed
Vallee, M. & Cornett, J. B. (1973). The immunity reaction of bacteriophage T4: a non-catalytic reaction. Virology 53, 441–447.CrossRefGoogle Scholar
Vallee, M. & deLapeyrière, M. (1975). The role of the genes imm and s in the development of immunity against T4 ghosts and exclusion of superinfecting phage in Escherichia coli infected with T4. Virology 67, 219–233.Google Scholar
Visconti, N. (1953). Resistance to lysis from without in bacteria infected with T2 bacteriophage. Journal of Bacteriology 66, 247–253.Google Scholar
Weiss, J. (1976). Endonuclease II of E. coli is exonuclease III. Journal of Biological Chemistry 251, 1896–1912.Google Scholar
Yutsudo, M. & Okamoto, K. (1973). Immediate-early expression of the gene causing superinfection breakdown in bacteriophage T4B. Journal of Virology 12, 1628–1630.Google Scholar