Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1995 Apr;69(4):2322–2327. doi: 10.1128/jvi.69.4.2322-2327.1995

Halophage HF2: genome organization and replication strategy.

S D Nuttall 1, M L Dyall-Smith 1
PMCID: PMC188903  PMID: 7884878

Abstract

Halophage HF2 is a lytic, broad-host-range bacteriophage of the extremely halophilic domain Archaea. It has a 79.7-kb double-stranded DNA genome which is linear, contains no modified nucleotides, and is not susceptible to cleavage by many type II restriction endonucleases. This insensitivity is attributed to selection against palindromic restriction sites, a commonly observed feature of broad-host-range phages. Interestingly, enzymes that did cut the genome recognized AT-rich sites, and five such enzymes, DraI, AseI, HpaI, HindIII, and SspI, were used to construct a physical map of the genome. Southern hybridization experiments used to order fragments on the map indicated homologies between the phage termini, and subsequent sequence analysis showed that HF2 possessed 306-bp direct terminal repeats. The presence of such repeats suggested replication through concatameric intermediates, and this was confirmed by analysis of the state of the phage genome in infected cells. This is a replication strategy adopted by many well-studied bacterial phages, for example T3 and T7. Other similarities between the terminal repeats of T3 or T7 and HF2 include a putative nick site at the repeat border and a series of short imperfect repeats. These observations suggest a long evolutionary history for concatamer-based strategies of phage replication, possibly predating the divergence of Archaea/Eucarya and Bacteria, or alternatively, indicate possible lateral transfer of phage genes or modules between the domains Archaea and Bacteria.

Full Text

The Full Text of this article is available as a PDF (451.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bickle T. A., Krüger D. H. Biology of DNA restriction. Microbiol Rev. 1993 Jun;57(2):434–450. doi: 10.1128/mr.57.2.434-450.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brown J. W., Daniels C. J., Reeve J. N. Gene structure, organization, and expression in archaebacteria. Crit Rev Microbiol. 1989;16(4):287–338. doi: 10.3109/10408418909105479. [DOI] [PubMed] [Google Scholar]
  3. Cline S. W., Doolittle W. F. Efficient transfection of the archaebacterium Halobacterium halobium. J Bacteriol. 1987 Mar;169(3):1341–1344. doi: 10.1128/jb.169.3.1341-1344.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cline S. W., Lam W. L., Charlebois R. L., Schalkwyk L. C., Doolittle W. F. Transformation methods for halophilic archaebacteria. Can J Microbiol. 1989 Jan;35(1):148–152. doi: 10.1139/m89-022. [DOI] [PubMed] [Google Scholar]
  5. Dietz A., Kössel H., Hausmann R. On the evolution of the terminal redundancies of Klebsiella phage No. 11 and of coliphages T3 and T7. J Gen Virol. 1985 Jan;66(Pt 1):181–186. doi: 10.1099/0022-1317-66-1-181. [DOI] [PubMed] [Google Scholar]
  6. Dressler D., Wolfson J., Magazin M. Initiation and reinitiation of DNA synthesis during replication of bacteriophage T7. Proc Natl Acad Sci U S A. 1972 Apr;69(4):998–1002. doi: 10.1073/pnas.69.4.998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dunn J. J., Studier F. W. Nucleotide sequence from the genetic left end of bacteriophage T7 DNA to the beginning of gene 4. J Mol Biol. 1981 Jun 5;148(4):303–330. doi: 10.1016/0022-2836(81)90178-9. [DOI] [PubMed] [Google Scholar]
  8. Dyall-Smith M. L., Doolittle W. F. Construction of composite transposons for halophilic Archaea. Can J Microbiol. 1994 Nov;40(11):922–929. doi: 10.1139/m94-148. [DOI] [PubMed] [Google Scholar]
  9. Fujisawa H., Kimura M., Hashimoto C. In vitro cleavage of the concatemer joint of bacteriophage T3 DNA. Virology. 1990 Jan;174(1):26–34. doi: 10.1016/0042-6822(90)90050-2. [DOI] [PubMed] [Google Scholar]
  10. Fujisawa H., Sugimoto K. On the terminally redundant sequences of bacteriophage T3 DNA. Virology. 1983 Jan 30;124(2):251–258. doi: 10.1016/0042-6822(83)90342-2. [DOI] [PubMed] [Google Scholar]
  11. Gachechiladze K. K., Balardshishvili N. S., Adamia R. S., Chanishvili T. G., Krüger D. H. Host-controlled modification and restriction as a criterion of evaluating the therapeutical potential of Pseudomonas phage. J Basic Microbiol. 1991;31(2):101–106. doi: 10.1002/jobm.3620310206. [DOI] [PubMed] [Google Scholar]
  12. Gropp F., Grampp B., Stolt P., Palm P., Zillig W. The immunity-conferring plasmid p phi HL from the Halobacterium salinarium phage phi H: nucleotide sequence and transcription. Virology. 1992 Sep;190(1):45–54. doi: 10.1016/0042-6822(92)91191-v. [DOI] [PubMed] [Google Scholar]
  13. Holmes M. L., Dyall-Smith M. L. A plasmid vector with a selectable marker for halophilic archaebacteria. J Bacteriol. 1990 Feb;172(2):756–761. doi: 10.1128/jb.172.2.756-761.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Holmes M., Pfeifer F., Dyall-Smith M. Improved shuttle vectors for Haloferax volcanii including a dual-resistance plasmid. Gene. 1994 Aug 19;146(1):117–121. doi: 10.1016/0378-1119(94)90844-3. [DOI] [PubMed] [Google Scholar]
  15. Iwabe N., Kuma K., Hasegawa M., Osawa S., Miyata T. Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9355–9359. doi: 10.1073/pnas.86.23.9355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Juez G., Rodriguez-Valera F., Herrero N., Mojica F. J. Evidence for salt-associated restriction pattern modifications in the archaeobacterium Haloferax mediterranei. J Bacteriol. 1990 Dec;172(12):7278–7281. doi: 10.1128/jb.172.12.7278-7281.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ken R., Hackett N. R. Halobacterium halobium strains lysogenic for phage phi H contain a protein resembling coliphage repressors. J Bacteriol. 1991 Feb;173(3):955–960. doi: 10.1128/jb.173.3.955-960.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Krüger D. H., Bickle T. A. Bacteriophage survival: multiple mechanisms for avoiding the deoxyribonucleic acid restriction systems of their hosts. Microbiol Rev. 1983 Sep;47(3):345–360. doi: 10.1128/mr.47.3.345-360.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Krüger D. H., Schroeder C. Bacteriophage T3 and bacteriophage T7 virus-host cell interactions. Microbiol Rev. 1981 Mar;45(1):9–51. doi: 10.1128/mr.45.1.9-51.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lam W. L., Doolittle W. F. Shuttle vectors for the archaebacterium Halobacterium volcanii. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5478–5482. doi: 10.1073/pnas.86.14.5478. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nuttall S. D., Dyall-Smith M. L. Ch2, a novel halophilic archaeon from an Australian solar saltern. Int J Syst Bacteriol. 1993 Oct;43(4):729–734. doi: 10.1099/00207713-43-4-729. [DOI] [PubMed] [Google Scholar]
  22. Nuttall S. D., Dyall-Smith M. L. HF1 and HF2: novel bacteriophages of halophilic archaea. Virology. 1993 Dec;197(2):678–684. doi: 10.1006/viro.1993.1643. [DOI] [PubMed] [Google Scholar]
  23. Paetkau V., Langman L., Bradley R., Scraba D., Miller R. C., Jr Folded, concatenated genomes as replication intermediates of bacteriophage T7 DNA. J Virol. 1977 Apr;22(1):130–141. doi: 10.1128/jvi.22.1.130-141.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Patterson N. H., Pauling C. Evidence for two restriction-modification systems in Halobacterium cutirubrum. J Bacteriol. 1985 Aug;163(2):783–784. doi: 10.1128/jb.163.2.783-784.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Reanney D. C., Ackermann H. W. Comparative biology and evolution of bacteriophages. Adv Virus Res. 1982;27:205–280. doi: 10.1016/s0065-3527(08)60436-4. [DOI] [PubMed] [Google Scholar]
  26. Reiter W. D., Hüdepohl U., Zillig W. Mutational analysis of an archaebacterial promoter: essential role of a TATA box for transcription efficiency and start-site selection in vitro. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9509–9513. doi: 10.1073/pnas.87.24.9509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schnabel H., Zillig W., Pfäffle M., Schnabel R., Michel H., Delius H. Halobacterium halobium phage øH. EMBO J. 1982;1(1):87–92. doi: 10.1002/j.1460-2075.1982.tb01129.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schroeder C., Jurkschat H., Meisel A., Reich J. G., Krüger D. Unusual occurrence of EcoP1 and EcoP15 recognition sites and counterselection of type II methylation and restriction sequences in bacteriophage T7 DNA. Gene. 1986;45(1):77–86. doi: 10.1016/0378-1119(86)90134-4. [DOI] [PubMed] [Google Scholar]
  29. Serwer P. Complexes between bacteriophage T7 capsids and T7 DNA. Virology. 1974 May;59(1):89–107. doi: 10.1016/0042-6822(74)90208-6. [DOI] [PubMed] [Google Scholar]
  30. Stolt P., Zillig W. Antisense RNA mediates transcriptional processing in an archaebacterium, indicating a novel kind of RNase activity. Mol Microbiol. 1993 Mar;7(6):875–882. doi: 10.1111/j.1365-2958.1993.tb01178.x. [DOI] [PubMed] [Google Scholar]
  31. Stolt P., Zillig W. In vivo and in vitro analysis of transcription of the L region from the Halobacterium salinarium phage phi H: definition of a repressor-enhancing gene. Virology. 1993 Aug;195(2):649–658. doi: 10.1006/viro.1993.1416. [DOI] [PubMed] [Google Scholar]
  32. Stolt P., Zillig W. In vivo studies on the effects of immunity genes on early lytic transcription in the Halobacterium salinarium phage phi H. Mol Gen Genet. 1992 Nov;235(2-3):197–204. doi: 10.1007/BF00279361. [DOI] [PubMed] [Google Scholar]
  33. White J. H., Richardson C. C. Processing of concatemers of bacteriophage T7 DNA in vitro. J Biol Chem. 1987 Jun 25;262(18):8851–8860. [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES