Abstract
Seldom has the study of a set of genes contributed more to our understanding of molecular genetics than has the characterization of the rapid-lysis genes of bacteriophage T4. For example, T4 rII mutants were used to define gene structure and mutagen effects at the molecular level and to help unravel the genetic code. The large-plaque morphology of these mutants reflects a block in expressing lysis inhibition (LIN), the ability to delay lysis for several hours in response to sensing external related phages attacking the cell, which is a unique and highly adaptive attribute of the T4 family of phages. However, surprisingly little is known about the mechanism of LIN, or how the various r genes affect its expression. Here, we review the extensive old literature about the r genes and the lysis process and try to sort out the major players affecting lysis inhibition. We confirm that superinfection can induce lysis inhibition even while infected cells are lysing, suggesting that the signal response is virtually instantaneous and thus probably the result of post-translational regulation. We identify the rI gene as ORF tk.-2, based on sequence analysis of canonical rI mutants. The rI gene encodes a peptide of 97 amino acids (Mr = 11.1 kD; pI = 4.8) that probably is secreted into the periplasmic space. This gene is widely conserved among T-even phage. We then present a model for LIN, postulating that rI is largely responsible for regulating the gpt holin protein in response to superinfection. The evidence suggests that the rIIA and B genes are not directly involved in lysis inhibition; rather, when they are absent, an alternate pathway for lysis develops which depends on the presence of genes from any of several possible prophages and is not sensitive to lysis inhibition.
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Selected References
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- Abedon S. T. Lysis of lysis-inhibited bacteriophage T4-infected cells. J Bacteriol. 1992 Dec;174(24):8073–8080. doi: 10.1128/jb.174.24.8073-8080.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Abedon S. T. Selection for lysis inhibition in bacteriophage. J Theor Biol. 1990 Oct 21;146(4):501–511. doi: 10.1016/s0022-5193(05)80375-3. [DOI] [PubMed] [Google Scholar]
- Ackermann H. W., Krisch H. M. A catalogue of T4-type bacteriophages. Arch Virol. 1997;142(12):2329–2345. doi: 10.1007/s007050050246. [DOI] [PubMed] [Google Scholar]
- Benzer S. FINE STRUCTURE OF A GENETIC REGION IN BACTERIOPHAGE. Proc Natl Acad Sci U S A. 1955 Jun 15;41(6):344–354. doi: 10.1073/pnas.41.6.344. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berger H., Kozinski A. W. Suppression of T4D ligase mutations by rIIa and rIIb mutations. Proc Natl Acad Sci U S A. 1969 Nov;64(3):897–904. doi: 10.1073/pnas.64.3.897. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bläsi U., Chang C. Y., Zagotta M. T., Nam K. B., Young R. The lethal lambda S gene encodes its own inhibitor. EMBO J. 1990 Apr;9(4):981–989. doi: 10.1002/j.1460-2075.1990.tb08200.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bode W. Lysis inhibition in Escherichia coli infected with bacteriophage T4. J Virol. 1967 Oct;1(5):948–955. doi: 10.1128/jvi.1.5.948-955.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boyd D., Schierle C., Beckwith J. How many membrane proteins are there? Protein Sci. 1998 Jan;7(1):201–205. doi: 10.1002/pro.5560070121. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carlson K., Kozinski A. W. Parent-to-progeny transfer and recombination of T4rII bacteriophage. J Virol. 1970 Sep;6(3):344–352. doi: 10.1128/jvi.6.3.344-352.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carlson K., Lorkiewicz Z. K., Kozinski A. W. Host-mediated repair of discontinuities in DNA from T4 bacteriophage. J Virol. 1973 Aug;12(2):310–319. doi: 10.1128/jvi.12.2.310-319.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DOERMANN A. H. The intracellular growth of bacteriophages. I. Liberation of intracellular bacteriophage T4 by premature lysis with another phage or with cyanide. J Gen Physiol. 1952 Mar;35(4):645–656. doi: 10.1085/jgp.35.4.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Doermann A. H. Lysis and Lysis Inhibition with Escherichia coli Bacteriophage. J Bacteriol. 1948 Feb;55(2):257–276. doi: 10.1128/jb.55.2.257-276.1948. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ebisuzaki K., Campbell L. On the role of ligase in genetic recombination in bacteriophage T4. Virology. 1969 Aug;38(4):701–703. doi: 10.1016/0042-6822(69)90190-1. [DOI] [PubMed] [Google Scholar]
- Emrich J. Lysis of T4-infected bacteria in the absence of lysozyme. Virology. 1968 May;35(1):158–165. doi: 10.1016/0042-6822(68)90315-2. [DOI] [PubMed] [Google Scholar]
- Ennis H. L., Kievitt K. D. Association of the rIIA protein with the bacterial membrane. Proc Natl Acad Sci U S A. 1973 May;70(5):1468–1472. doi: 10.1073/pnas.70.5.1468. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fraser D., Mahler H. R., Shug A. L., Thomas C. A. THE INFECTION OF SUB-CELLULAR ESCHERICHIA COLI, STRAIN B, WITH A DNA PREPARATION FROM T2 BACTERIOPHAGE. Proc Natl Acad Sci U S A. 1957 Nov 15;43(11):939–947. doi: 10.1073/pnas.43.11.939. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hershey A. D., Rotman R. Linkage Among Genes Controlling Inhibition of Lysis in a Bacterial Virus. Proc Natl Acad Sci U S A. 1948 Mar;34(3):89–96. doi: 10.1073/pnas.34.3.89. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Josslin R. The lysis mechanism of phage T4: mutants affecting lysis. Virology. 1970 Mar;40(3):719–726. doi: 10.1016/0042-6822(70)90216-3. [DOI] [PubMed] [Google Scholar]
- Kao S. H., McClain W. H. Roles of bacteriophage T4 gene 5 and gene s products in cell lysis. J Virol. 1980 Apr;34(1):104–107. doi: 10.1128/jvi.34.1.104-107.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Karam J. D. DNA replication of phage T4 rII mutants without polynucleotide ligase (gene 30). Biochem Biophys Res Commun. 1969 Oct 22;37(3):416–422. doi: 10.1016/0006-291x(69)90931-0. [DOI] [PubMed] [Google Scholar]
- Krylov V. N., Yankovsky N. K. Mutations in the new gene stIII of bacteriophage T4B suppressing the lysis defect of gene stII and a gene e mutant. J Virol. 1975 Jan;15(1):22–26. doi: 10.1128/jvi.15.1.22-26.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McPheeters D. S., Christensen A., Young E. T., Stormo G., Gold L. Translational regulation of expression of the bacteriophage T4 lysozyme gene. Nucleic Acids Res. 1986 Jul 25;14(14):5813–5826. doi: 10.1093/nar/14.14.5813. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Monod C., Repoila F., Kutateladze M., Tétart F., Krisch H. M. The genome of the pseudo T-even bacteriophages, a diverse group that resembles T4. J Mol Biol. 1997 Mar 28;267(2):237–249. doi: 10.1006/jmbi.1996.0867. [DOI] [PubMed] [Google Scholar]
- Mosig G., Breschkin A. M. Genetic evidence for an additional function of phage T4 gene 32 protein: interaction with ligase. Proc Natl Acad Sci U S A. 1975 Apr;72(4):1226–1230. doi: 10.1073/pnas.72.4.1226. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mosig G., Shaw M., Garcia G. M. On the role of DNA replication, endonuclease VII, and rII proteins in processing of recombinational intermediates in phage T4. Cold Spring Harb Symp Quant Biol. 1984;49:371–382. doi: 10.1101/sqb.1984.049.01.044. [DOI] [PubMed] [Google Scholar]
- Mukai F., Streisinger G., Miller B. The mechanism of lysis in phage T4-infected cells. Virology. 1967 Nov;33(3):398–404. doi: 10.1016/0042-6822(67)90115-8. [DOI] [PubMed] [Google Scholar]
- Obringer J., McCreary P., Bernstein H. Bacteriophage T4 genes sp and 40 apparently are the same. J Virol. 1988 Aug;62(8):3043–3045. doi: 10.1128/jvi.62.8.3043-3045.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Parma D. H., Snyder M., Sobolevski S., Nawroz M., Brody E., Gold L. The Rex system of bacteriophage lambda: tolerance and altruistic cell death. Genes Dev. 1992 Mar;6(3):497–510. doi: 10.1101/gad.6.3.497. [DOI] [PubMed] [Google Scholar]
- Raudonikiene A., Nivinskas R. Gene rIII is the nearest downstream neighbour of bacteriophage T4 gene 31. Gene. 1992 May 1;114(1):85–90. doi: 10.1016/0378-1119(92)90711-w. [DOI] [PubMed] [Google Scholar]
- Riede I. Lysis gene t of T-even bacteriophages: evidence that colicins and bacteriophage genes have common ancestors. J Bacteriol. 1987 Jul;169(7):2956–2961. doi: 10.1128/jb.169.7.2956-2961.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Russell R. L., Huskey R. J. Partial exclusion between T-even bacteriophages: an incipient genetic isolation mechanism. Genetics. 1974 Dec;78(4):989–1014. doi: 10.1093/genetics/78.4.989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rutberg B., Rutberg L. Role of superinfecting phage in lysis inhibition with phage T4 in Escherichia coli. J Bacteriol. 1965 Oct;90(4):891–894. doi: 10.1128/jb.90.4.891-894.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
- STREISINGER G., EDGAR R. S., DENHARDT G. H. CHROMOSOME STRUCTURE IN PHAGE T4. I. CIRCULARITY OF THE LINKAGE MAP. Proc Natl Acad Sci U S A. 1964 May;51:775–779. doi: 10.1073/pnas.51.5.775. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smith L. A., Drake J. W. Aspects of the ultraviolet photobiology of some T-even bacteriophages. Genetics. 1998 Apr;148(4):1611–1618. doi: 10.1093/genetics/148.4.1611. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ziermann R., Bartlett B., Calendar R., Christie G. E. Functions involved in bacteriophage P2-induced host cell lysis and identification of a new tail gene. J Bacteriol. 1994 Aug;176(16):4974–4984. doi: 10.1128/jb.176.16.4974-4984.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
