1887

Abstract

The complete nucleotide sequence of ssRNA phage AP205 propagating in species is reported. The RNA has three large ORFs, which code for the following homologues of the RNA coliphage proteins: the maturation, coat and replicase proteins. Their gene order is the same as that in coliphages. RNA coliphages or fall into two genera: the alloleviviruses, like Q, which have a coat read-through protein, and the leviviruses, like MS2, which do not have this coat protein extension. AP205 has no read-through protein and may therefore be classified as a levivirus. A major digression from the known leviviruses is the apparent absence of a lysis gene in AP205 at the usual position, overlapping the coat and replicase proteins. Instead, two small ORFs are present at the 5′ terminus, preceding the maturation gene. One of these might encode a lysis protein. The other is of unknown function. Other new features concern the 3′-terminal sequence. In all ssRNA coliphages, there are always three cytosine residues at the 3′ end, but in AP205, there is only a single terminal cytosine. Distantly related viruses, like AP205 and the coliphages, do not have significant sequence identity; yet, important secondary structural features of the RNA are conserved. This is shown here for the 3′ UTR and the replicase-operator hairpin. Interestingly, although AP205 has the genetic map of a levivirus, its 3′ UTR has the length and RNA secondary structure of an allolevivirus. Sharing features with both MS2 and Q suggests that, in an evolutionary sense, AP205 should be placed between Q and MS2. A phylogenetic tree for the ssRNA phages is presented.

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2002-06-01
2020-08-13
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References

  1. Adhin M. R.. 1989; A comparative analysis of RNA coliphages. PhD thesis Leiden University; Leiden, The Netherlands:
  2. Adhin M. R., van Duin J.. 1990; Scanning model for translational reinitiation in eubacteria. Journal of Molecular Biology213:811–818
    [Google Scholar]
  3. Beekwilder M. J.. 1996; Secondary structure of the RNA genome of bacteriophage Qβ. PhD thesis Leiden University; Leiden, The Netherlands:
  4. Beekwilder M. J., Nieuwenhuizen R., van Duin J.. 1995; Secondary structure model for the last two domains of single-stranded RNA phage Qβ. Journal of Molecular Biology247:903–917
    [Google Scholar]
  5. Beekwilder M. J., Nieuwenhuizen R., Poot R., van Duin J.. 1996; Secondary structure model for the first three domains of Qβ RNA. Control of A-protein synthesis. Journal of Molecular Biology256:8–19
    [Google Scholar]
  6. Berkhout B., de Smit M. H., Spanjaard R., Blom T., van Duin J.. 1985; The amino terminal half of the MS2-coded lysis protein is dispensable for function: implications for our understanding of coding region overlaps. EMBO Journal4:3315–3320
    [Google Scholar]
  7. Biebricher C. K.. 1999; Mutation, competition and selection as measured with small RNA molecules. In Origin and Evolution of Viruses pp65–85 Edited by Domingo E., Webster R. G., Holland J.. London: Academic Press;
    [Google Scholar]
  8. Bollback J. P., Huelsenbeck J. P.. 2001; Phylogeny, genome evolution, and host specificity of single-stranded RNA bacteriophages (family Leviviridae . Journal of Molecular Evolution52:117–128
    [Google Scholar]
  9. Bouvet P. J. M., Jeanjean S.. 1989; Delineation of new proteolytic genomic species in the genus Acinetobacter . Research in Microbiology140:291–299
    [Google Scholar]
  10. Bradley D. E.. 1966; Structure and infective process of a P. aeruginosa phage containing RNA. Journal of General Microbiology45:83–96
    [Google Scholar]
  11. Coffi H.. 1995; Lysotypie des Acinetobacter . Thèse de Maîtrise dès Sciences Laval University; Québec, Canada:
    [Google Scholar]
  12. de Smit M. H., van Duin J.. 1990; Secondary structure of the ribosome binding site determines translational efficiency: a quantitative analysis. Proceedings of the National Academy of Sciences, USA87:7668–7672
    [Google Scholar]
  13. Furuse K.. 1987; Distribution of the coliphages in the environment: general considerations. In Phage Ecology pp87–124 Edited by Goya S. M., Gerba C. P., Bitton G.. New York: Wiley Interscience;
    [Google Scholar]
  14. Goessens W. H. F., Driessen J. M., Wilschut J., van Duin J.. 1988; A synthetic peptide corresponding to the C-terminal 25 residues of phage MS2 coded lysis protein dissipates the protonmotive force in Escherichia coli membrane vesicles by generating hydophilic pores. EMBO Journal7:867–873
    [Google Scholar]
  15. Groeneveld H.. 1997; Secondary structure of bacteriophage MS2 RNA. Translational control by kinetics of RNA folding. PhD thesis Leiden University; Leiden, The Netherlands:
  16. Groeneveld H., Thimon H., van Duin J.. 1995; Translational control of maturation-protein synthesis in phage MS2: a role for the kinetics of RNA folding?. RNA1:79–88
    [Google Scholar]
  17. Inokuchi Y., Takahashi R., Hirose T., Inayama S., Jacobson A. B., Hirashima A.. 1986; The complete nucleotide sequence of group II RNA coliphage GA. Journal of Biochemistry99:1169–1180
    [Google Scholar]
  18. Inokuchi Y., Jacobson A. B., Hirose T., Inayama S., Hirashima A.. 1988; Analysis of the complete nucleotide sequence of the group IV RNA coliphage SP. Nucleic Acids Research16:6205–6221
    [Google Scholar]
  19. Karnik S., Billeter M.. 1983; The lysis function of RNA bacteriophage Qβ is mediated by the maturation protein. EMBO Journal2:1521–1526
    [Google Scholar]
  20. Klovins J., van Duin J.. 1999; A long-range pseudoknot in Qβ RNA is essential for replication. Journal of Molecular Biology294:875–884
    [Google Scholar]
  21. Klovins J., Tsareva N. A., de Smit M. H., Berzins V., van Duin J.. 1997; Rapid evolution of translational control mechanisms in RNA genomes. Journal of Molecular Biology265:372–384
    [Google Scholar]
  22. Licis N., Balklava Z., van Duin J.. 2000; Forced retroevolution of an RNA bacteriophage. Virology271:298–306
    [Google Scholar]
  23. Luftig R. B.. 1967; An accurate measurement of the catalase crystal period and its use as an internal marker for electron microscopy. Journal of Ultrastructure Research20:91–102
    [Google Scholar]
  24. Mathews D. H., Sabina J., Zuker M., Turner D. H.. 1999; Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. Journal of Molecular Biology288:911–940
    [Google Scholar]
  25. Olsen G. J., Woese C. R., Overbeek R.. 1994; The winds of (evolutionary) change: breathing new life into microbiology. Journal of Bacteriology176:1–6
    [Google Scholar]
  26. Olsthoorn R. C. L.. 1996; Structure and evolution of RNA phages. PhD thesis Leiden University; Leiden, The Netherlands:
  27. Olsthoorn R. C. L., van Duin J.. 1996a; Evolutionary reconstruction of a hairpin deleted from the genome of an RNA virus. Proceedings of the National Academy of Sciences, USA93:12256–12261
    [Google Scholar]
  28. Olsthoorn R. C. L., van Duin J.. 1996b; Random removal of inserts from an RNA genome: selection against single-stranded RNA. Journal of Virology70:729–736
    [Google Scholar]
  29. Olsthoorn R. C. L., Garde G., Dayhuff T., Atkins J. F., van Duin J.. 1995; Nucleotide sequence of a single-stranded RNA phage from Pseudomonas aeruginosa : kinship to coliphages and conservation of regulatory RNA structures. Virology206:611–625
    [Google Scholar]
  30. Remaut E., Stanssens P., Fiers W.. 1981; Plasmid vectors for high-efficiency expression controlled by the PL promoter of coliphage λ. Gene15:81–93
    [Google Scholar]
  31. Schuppli D., Georgijevic J., Weber H.. 2000; Synergism of mutations in Qβ RNA affecting host factor dependence of Qβ replicase. Journal of Molecular Biology295:149–154
    [Google Scholar]
  32. Tars K., Bundule M., Fridborg K., Liljas L.. 1997; The crystal structure of bacteriophage GA and a comparison of bacteriophages belonging to the major groups of Escherichia coli leviviruses. Journal of Molecular Biology271:759–773
    [Google Scholar]
  33. Tars K., Fridborg K., Bundule M., Liljas L.. 2000; The three-dimensional structure of bacteriophage PP7 from Pseudomonas aeruginosa at 3·7 Å resolution. Virology272:331–337
    [Google Scholar]
  34. Thompson J. D., Higgins D. G., Gibson T. J.. 1994; CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research22:4673–4680
    [Google Scholar]
  35. Towner K. J.. 1997; Clinical importance and antibiotic resistance of Acinetobacter spp. Journal of Medical Microbiology46:721–746
    [Google Scholar]
  36. Valegård K., Liljas L., Fridborg K., Unge T.. 1990; The three-dimensional structure of the bacterial virus MS2. Nature345:36–41
    [Google Scholar]
  37. Valegård K., Murray J. B., Stockley P. G., Stonehouse N. J., Liljas L.. 1994; Crystal structure of an RNA bacteriophage coat protein-operator complex. Nature371:623–626
    [Google Scholar]
  38. van Duin J.. 1988; The single-stranded RNA bacteriophages. In The Viruses pp117–167 Edited by Fraenkel-Conrat H., Wagner R.. New York: Plenum;
    [Google Scholar]
  39. van Duin J.. 1999; Single-stranded RNA phages. In Encyclopedia of Virology pp1663–1668 London: Academic Press;
    [Google Scholar]
  40. van Duin J.. 2000; Leviviridae. In Virus Taxonomy. Seventh Report of the International Committee on Taxonomy of Viruses pp645–646 Edited by van Regenmortel M. H. V., Fauquet C. M., Bishop D. H. L., Carstens E. B., Estes M. K., Lemon S. M., Maniloff J., Mayo M. A., McGeoch D. J., Pringle C. R., Wickner R. B.. San Diego: Academic Press;
    [Google Scholar]
  41. Voorma H. O., Benne R., den Hertog T. J. A.. 1971; Binding of aminoacyl-tRNA to ribosome programmed with bacteriophage MS2-RNA. European Journal of Biochemistry18:451–462
    [Google Scholar]
  42. Walderich B., Ursinus-Wossner A., van Duin J., Höltje J.-V.. 1988; Induction of the autolytic system of Escherichia coli by specific insertion of bacteriophage MS2 lysis protein into the bacterial cell envelope. Journal of Bacteriology170:5027–5033
    [Google Scholar]
  43. Weber H.. 1999; Qβ replicase. In Encyclopaedia of Molecular Biology . pp2085–2087 Edited by Creighton T. E.. New York: John Wiley;
  44. Winter R. G., Gold L.. 1983; Overproduction of bacteriophage Qβ maturation (A2) protein leads to cell lysis. Cell33:877–885
    [Google Scholar]
  45. Witherell G. W., Uhlenbeck O. C.. 1989; Specific RNA binding by Qβ coat protein. Biochemistry28:71–76
    [Google Scholar]
  46. Witherell G. W., Gott J. M., Uhlenbeck O. C.. 1991; Specific interaction between RNA phage coat proteins and RNA. Progress in Nucleic Acid Research and Molecular Biology40:185–220
    [Google Scholar]
  47. Young R.. 1992; Bacteriophage lysis: mechanism and regulation. Microbiology Reviews56:430–481
    [Google Scholar]
  48. Zamora H., Luce R., Biebricher C. K.. 1995; Design of artificial short-chained RNA species that are replicated by Qβ replicase. Biochemistry34:1261–1266
    [Google Scholar]
  49. Zinder N. D.. 1975; RNA Phages Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  50. Zinder N. D.. 1980; Portraits of viruses: RNA phage. Intervirology13:257–270
    [Google Scholar]
  51. Zuker M., Mathews D. H., Turner D. H.. 1999; Algorithms and thermodynamics for RNA secondary structure prediction: a practical guide. In RNA Biochemistry and Biotechnology pp11–43 Edited by Barciszewski J., Clark B. F. C.. Amsterdam: Kluwer;
    [Google Scholar]
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