Bacteriophages with ssRNA

Abstract

The single‐stranded ribonucleic acid (ssRNA) phages are small icosahedral viruses which infect their host via F‐ or polar pili. The best‐characterised are those infecting Escherichia coli, a Gram‐negative bacterium found in the gut and faecal sewage. The ssRNA phages are members of the Leviviridae family, which includes the two genera Levivirus and Allolevivirus. The family presently comprises about 100 isolates including the well‐known MS2 and Qβ coliphages.Their genome size ranges from 3400 to 4300 nt and codes for four proteins. The genome of ssRNA phages adopts a unique structure that regulates translation of the four genes, confers RNase resistance in the bacterial cytoplasm, ensures recognition by replicase and facilitates encapsidation by capsid or coat proteins. The interaction between RNA and coat protein by virtue of its high specificity and strength is used in many molecular biological applications.

Key Concepts:

  • ssRNA phages are members of the Leviviridae family which comprises the genera Levivirus and Allolevivirus.

  • ssRNA phages infect their hosts via pili.

  • The nonenveloped quasi‐icosahedral shell of the virion has a T=3 surface lattice.

  • RNA inside the virion is structured.

  • The genome encodes four types of proteins: maturation, coat, lysis and replicase.

  • Replication requires the use of host proteins.

  • Translation of the genes is regulated by RNA secondary structure.

  • Forced evolution experiments reveal constraints on RNA secondary structure.

  • Phage particles can be used to display foreign epitopes.

  • RNA phages are used as indicator organisms for the presence of pathogens in drink and surface water.

Keywords: RNA; phage; translation; replication; evolution; RNA recombination; RNA secondary structure; index organism; sewage; ribosome; fitness

Figure 1.

Schematic view of an RNA bacteriophage. The RNA is highly ordered and has very few unpaired regions.

Figure 2.

Genetic maps of group A and B RNA coliphages. Repression of replicase translation by the coat protein is shown. Lysis overlaps coat and replicase genes in the +1 frame.

Figure 3.

RNA phages attached to the F‐pili of E. coli. From Fiers .

Figure 4.

Example of forced evolution showing several pathways leading from the non‐viable mutant 45 to various viable revertants. The start codon and Shine‐Dalgarno sequence of the MS2 coat gene are boxed. Base changes with respect to wild type are highlighted in mutant 45. Highlighted bases in revertants indicate changes with respect to mutant 45. Thermodynamic stabilities were calculated on the mfold webserver at the University at Albany, State University of New York using version 2.3 energies, according to de Smit and van Duin . Reproduced from Olsthoorn et al. with permission from Nature Publishing Group.

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References

Adhin MR and van Duin J (1990) Scanning model for translational reinitiation in eubacteria. Journal of Molecular Biology 213: 811–818.

Barrera I, Schuppli D, Sogo JM and Weber H (2003) Different mechanisms of recognition of bacteriophage Qbeta plus and minus strand RNAs by Qbeta replicase. Journal of Molecular Biology 232: 512–521.

Basnak G, Morton VL, Rolfsson O et al. (2010) Viral genomic single‐stranded RNA directs the pathway toward a T=3 capsid. Journal of Molecular Biology 395: 924–936.

Beekwilder J, Nieuwenhuizen R, Havelaar AH and van Duin J (1996) An oligonucleotide hybridization assay for the identification and enumeration of F‐specific RNA phages in surface water. Journal of Applied Bacteriology 80: 179–186.

Beekwilder MJ, Nieuwenhuizen R and van Duin J (1995) Secondary structure model for the last two domains of single‐stranded RNA phage Q beta. Journal of Molecular Biology 247: 903–917.

Ben Said M, Masahiro O and Hassen A (2010) Detection of viable but non cultivable E. coli after UV irradiation using a lytic Qβ phage. Annals of Microbiology 60: 121–127.

Caldeira Jdo C, Medford A, Kines RC et al. (2010) Immunogenic display of diverse peptides, including a broadly cross‐type neutralizing human papillomavirus L2 epitope, on virus‐like particles of the RNA bacteriophage PP7. Vaccine 28: 4384–4393.

Cole D, Long SC and Sobsey MD (2003) Evaluation of F+ RNA and DNA coliphages as source‐specific indicators of fecal contamination in surface waters. Applied and Environmental Microbiology 69: 6507–6514.

Fiers W (1975) Chemical structure and biological activity of bacteriophage MS2 RNA. In: Zinder ND (ed.) RNA Phages. Monograph Series, pp. 353–396. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.

Friedman SD, Genthner FJ, Gentry J, Sobsey MD and Vinjé J (2009) Gene mapping and phylogenetic analysis of the complete genome from 30 single‐stranded RNA male‐specific coliphages (family Leviviridae). Journal of Virology 83: 11233–11243.

Furuse K (1987) Distribution of coliphages in the environment: general considerations. In: Goyal SM (ed.) Phage Ecology, pp. 87–124. New York: Wiley.

Golmohammadi R, Valegård K, Fridborg K and Liljas L (1993) The refined structure of bacteriophage MS2 at 2.8 A resolution. Journal of Molecular Biology 234: 620–639.

Groeneveld H, Thimon K and van Duin J (1995) Translational control of maturation‐protein synthesis in phage MS2: a role for the kinetics of RNA folding? RNA 1: 79–88.

Hsu FC, Shieh YS, van Duin J, Beekwilder MJ and Sobsey MD (1995) Genotyping male‐specific RNA coliphages by hybridization with oligonucleotide probes. Applied and Environmental Microbiology 61: 3960–3966.

Jayant L, Priano C and Mills DR (2010) In polycistronic Qbeta RNA, single‐strandedness at one ribosome binding site directly affects translational initiations at a distal upstream cistron. Nucleic Acids Research 38: 7199–7210.

Kidmose RT, Vasiliev NN, Chetverin AB, Andersen GR and Knudsen CR (2010) Structure of the Qbeta replicase, an RNA‐dependent RNA polymerase consisting of viral and host proteins. Proceedings of the National Academy of Sciences of the USA 107: 10884–10889.

Klovins J, van Duin J and Olsthoorn RCL (1997a) Rescue of the RNA phage genome from RNase III cleavage. Nucleic Acids Research 25: 4201–4208.

Klovins J, Tsareva NA, de Smit MH, Berzins V and van Duin J (1997b) Rapid evolution of translational control mechanisms in RNA genomes. Journal of Molecular Biology 265: 372–384.

Kolakofsky D and Weissmann C (1971) Possible mechanism for transition of viral RNA from polysome to replication complex. Nature New Biology 231: 42–46.

Kozlovska TM, Cielens I, Vasiljeva I et al. (1996) RNA phage Q beta coat protein as a carrier for foreign epitopes. Intervirology 39: 9–15.

Licis N and van Duin J (2006) Structural constraints and mutational bias in the evolutionary restoration of a severe deletion in RNA phage MS2. Journal of Molecular Evolution 63: 314–329.

Licis N, van Duin J, Balklava Z and Berzins V (1998) Long‐range translational coupling in single‐stranded RNA bacteriophages: an evolutionary analysis. Nucleic Acids Research 26: 3242–3246.

van Meerten D, Girard G and van Duin J (2001) Translational control by delayed RNA folding: identification of the kinetic trap. RNA 7: 483–494.

Meyer F, Weber H and Weissmann C (1981) Interactions of Q beta replicase with Q beta RNA. Journal of Molecular Biology 153: 631–660.

Mooijman KA, Ghameshlou Z, Bahar M, Jofre J and Havelaar AH (2005) Enumeration of bacteriophages in water by different laboratories of the European Union in two interlaboratory comparison studies. Journal of Virological Methods 127: 60–68.

Olsthoorn RCL and van Duin J (1996a) Random removal of inserts from an RNA genome: selection against single‐stranded RNA. Journal of Virology 70: 729–736.

Olsthoorn RCL and van Duin J (1996b) Evolutionary reconstruction of a hairpin deleted from the genome of an RNA virus. Proceedings of the National Academy of Sciences of the USA 93: 12256–12261.

Olsthoorn RCL, Licis N and van Duin J (1994) Leeway and constraints in the forced evolution of a regulatory RNA helix. EMBO Journal 13: 2660–2668.

Peabody DS (1993) The RNA binding site of bacteriophage MS2 coat protein. EMBO Journal 12: 595–600.

Poot RA, Tsareva NV, Boni IV and van Duin J (1997) RNA folding kinetics regulates translation of phage MS2 maturation gene. Proceedings of the National Academy of Sciences of the USA 94: 10110–10115.

Ruokoranta TM, Grahn AM, Ravantti JJ, Poranen MM and Bamford DH (2006) Complete genome sequence of the broad host range single‐stranded RNA phage PRR1 places it in the Levivirus genus with characteristics shared with Alloleviviruses. Journal of Virology 80: 9326–9330.

Schuppli D, Miranda G, Tsui HC et al. (1997) Altered 3′‐terminal RNA structure in phage Qbeta adapted to host factor‐less E. coli. Proceedings of the National Academy of Sciences of the USA 94: 10239–10242.

de Smit MH and van Duin J (1990) Secondary structure of the ribosome binding site determines translational efficiency: a quantitative analysis. Proceedings of the National Academy of Sciences of the USA 87: 7668–7672.

de Smit MH and van Duin J (1993) Translational initiation at the coat‐protein gene of phage MS2: native upstream RNA relieves inhibition by local secondary structure. Molecular Microbiology 9: 1079–1088.

de Smit MH and van Duin J (2003) Translational standby sites: how ribosomes may deal with the rapid folding kinetics of mRNA. Journal of Molecular Biology 331: 737–743.

Valegård K, Murray JB, Stockley NJ, Stonehouse NJ and Liljas L (1994) Crystal structure of an RNA bacteriophage coat protein‐operator complex. Nature 371: 623–626.

van den Worm SH, Koning RI, Warmenhoven HJ, Koerten HK and van Duin J (2006) Cryo electron microscopy reconstructions of the Leviviridae unveil the densest icosahedral RNA packing possible. Journal of Molecular Biology 363: 858–865.

Further Reading

Ackermann HW and Dubow MS (eds) (1987) Natural groups of bacteriophages. In: Viruses of Prokaryotes, vol. 2, pp. 85–100. Boca Raton, FL: CRC Press.

Armon R and Kott Y (1996) Bacteriophages as indicators of pollution. Critical Reviews in Environmental Science and Technology 26: 299–306.

Brown D and Gold L (1996) RNA replication by Qβ replicase: a working model. Proceedings of the National Academy of Sciences of the USA 93: 11558–11562.

van Duin J and Tsareva N (1988) Single stranded RNA phages. In: Calendar R (ed.) The Bacteriophages, pp. 175–196. New York: Plenum Press.

Fiers W (1979) Structure and function of RNA bacteriophages. In: Fraenkel‐Conrat H and Wagner RR (eds) Comprehensive Virology, vol. 13, pp. 69–204. New York: Plenum Press.

Havelaar HA (1991) Bacteriophages as model viruses in water quality control. IAWPRC Study Group on Health Related Water Microbiology. Water Research 25: 529–545.

Horn WT, Tars K, Grahn E et al. (2006) Structural basis of RNA binding discrimination between bacteriophages Qbeta and MS2. Structure 14: 487–495.

Rohde N, Daum H and Biebricher K (1995) The mutant distribution of an RNA species replicated by Qβ replicase. Journal of Molecular Biology 294: 754–762.

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Olsthoorn, René, and van Duin, Jan(Jul 2011) Bacteriophages with ssRNA. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000778.pub3]