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Journal of Molecular Evolution

, Volume 76, Issue 6, pp 359–364 | Cite as

Mechanisms for RNA Capture by ssDNA Viruses: Grand Theft RNA

  • Kenneth StedmanEmail author
Review

Abstract

Viruses contain three common types of packaged genomes; double-stranded DNA (dsDNA), RNA (mostly single and occasionally double stranded) and single-stranded DNA (ssDNA). There are relatively straightforward explanations for the prevalence of viruses with dsDNA and RNA genomes, but the evolutionary basis for the apparent success of ssDNA viruses is less clear. The recent discovery of four ssDNA virus genomes that appear to have been formed by recombination between co-infecting RNA and ssDNA viruses, together with the high mutation rate of ssDNA viruses provide possible explanations. RNA–DNA recombination allows ssDNA viruses to access much broader sequence space than through nucleotide substitution and DNA–DNA recombination alone. Multiple non-exclusive mechanisms, all due to the unique replication of ssDNA viruses, are proposed for this unusual RNA capture. RNA capture provides an explanation for the evolutionary success of the ssDNA viruses and may help elucidate the mystery of integrated RNA viruses in viral and cellular DNA genomes.

Keywords

Recombination Evolution Rep protein Endonuclease Ligase RNA–DNA ligation 

Notes

Acknowledgments

Thanks to the Stedman lab for stimulating discussions and Geoff Diemer and Christoph Deeg comments on this manuscript. Thanks also to Ian Hewson and Lauren McDaniel for sharing data before publication. Thanks to Mya Breitbart, Sandy Lazarowitz and Bentley Fane for stimulating discussions. This work was supported by the Gordon and Betty Moore Foundation, the US National Science Foundation Microbial Observatories Program, Grant number MCB 0702020, and Portland State University.

References

  1. Acheson NH (2011) Fundamentals of Molecular Virology. Wiley, New YorkGoogle Scholar
  2. Belyi VA, Levine AJ, Skalka AM (2010) Sequences from ancestral single-stranded DNA viruses in vertebrate genomes: the Parvoviridae and Circoviridae are more than 40 to 50 million years old. J Virol 84:12458–12462. doi: 10.1128/JVI.01789-10 CrossRefPubMedGoogle Scholar
  3. Cheung AK (2012) Porcine circovirus: transcription and DNA replication. Virus Res 164:46–53. doi: 10.1016/j.virusres.2011.10.012 CrossRefPubMedGoogle Scholar
  4. Cui J, Holmes EC (2012) Endogenous RNA viruses of plants in insect genomes. Virology 427:77–79. doi: 10.1016/j.virol.2012.02.014 CrossRefPubMedGoogle Scholar
  5. Delwart E, Li L (2012) Rapidly expanding genetic diversity and host range of the circoviridae viral family and other rep encoding small circular ssDNA genomes. Virus Res 164:114–121. doi: 10.1016/j.virusres.2011.11.021 CrossRefPubMedGoogle Scholar
  6. Diemer GS, Stedman KM (2012) A novel virus genome discovered in an extreme environment suggests recombination between unrelated groups of RNA and DNA viruses. Biol Direct 7/13. http://www.biology-direct.com/content/7/1/13. doi: 10.1186/1745-6150-7-13
  7. Duffy S, Shackelton LA, Holmes EC (2008) Rates of evolutionary change in viruses: patterns and determinants. Nature Rev Genet 9:267–276. doi: 10.1038/nrg2323 CrossRefPubMedGoogle Scholar
  8. Fane BA, Brentlinger KL, Burch AD, Chen M, Hafenstein S, Moore E, Novak CR, Uchiyama A (2006) ΦX174 et al., the Microviridae. In: Calendar R (ed) The Bacteriophages, 2nd edn. Oxford University Press, New York, pp 129–145Google Scholar
  9. Feschotte C, Gilbert C (2012) Endogenous viruses: insights into viral evolution and impact on host biology. Nat Rev Genet 13:283–288. doi: 10.1038/nrg3199 CrossRefPubMedGoogle Scholar
  10. Finnegan DJ (2012) Retrotransposons. Curr Biol 22:R432–R437. doi: 10.1016/j.cub.2012.04.025 CrossRefPubMedGoogle Scholar
  11. Firth C, Charleston MA, Duffy S, Shapiro B, Holmes EC (2009) Insights into the evolutionary history of an emerging livestock pathogen: Porcine Circovirus 2. J Virol 83:12813–12821. doi: 10.1128/JVI.01719-09 CrossRefPubMedGoogle Scholar
  12. Forterre P (2002) The origin of DNA genomes and DNA replication proteins. Curr Opin Microbiol 5:525–532CrossRefPubMedGoogle Scholar
  13. Forterre P (2006) The origin of viruses and their possible roles in major evolutionary transitions. Virus Res 117:5–16. doi: 10.1016/j.virusres.2006.01.010 Google Scholar
  14. Gutierrez C (2002) Strategies for geminivirus DNA replication and cell cycle interference. Physiol Molec Plant Path 60:219–230. doi: 10.1006/pmpp.2002.0401 CrossRefGoogle Scholar
  15. Hendrix RW, Smith MCM, Burns RN, Ford ME, Hatfull GF (1999) Evolutionary relationships among diverse bacteriophages and prophages: all the world’s a phage. Proc Natl Acad Sci USA 96:2192–2197CrossRefPubMedGoogle Scholar
  16. Hewson I, Ng G, Li W, LaBarre BA, Aguirre I, Barbosa JG, Breitbart M, Greco AW, Kearns CM, Looi A, Schaffner LR, Thompson PD, Hairston NG Jr (2013) Metagenomic identification, seasonal dynamics and potential transmission mechanisms of a Daphnia-associated putative RNA–DNA hybrid virus in two temperate lakes. Limnol Ocean (in press)Google Scholar
  17. Holmes EC (2009) The evolution and emergence of RNA viruses. Oxford University Press, New YorkGoogle Scholar
  18. Holmes EC (2011) What does virus evolution tell us about virus origins? J Virol 85:5247–5251. doi: 10.1128/JVI.02203-10 CrossRefPubMedGoogle Scholar
  19. Horie M, Tomonaga K (2011) Non-retroviral fossils in vertebrate genomes. Viruses 3:1836–1848. doi: 10.3390/v3101836 CrossRefPubMedGoogle Scholar
  20. Jalasvuori M, Bamford JKH (2008) Structural co-evolution of viruses and cells in the primordial world. Ori Life Evol Biosphere 38:165–181. doi: 10.1007/s11084-008-9121-x CrossRefGoogle Scholar
  21. Kim K-H, Bae J-W (2011) Amplification methods bias metagenomic libraries of uncultured single-stranded and double-stranded DNA viruses. Appl Environ Microbiol 77:7663–7668. doi: 10.1128/aem.00289-11 CrossRefPubMedGoogle Scholar
  22. King AMQ, Lefkowitz E, Adams MJ, Carstens EB (eds) (2011) Virus Taxonomy : Ninth Report of the International Committee on Taxonomy of Viruses. Academic Press, San DiegoGoogle Scholar
  23. Koonin EV, Senkevich TG, Dolja VV (2006) The ancient Virus World and evolution of cells. Biol Direct 1: 29. http://www.biology-direct.com/content/1/1/29. doi:  10.1186/1745-5610-1-29
  24. Krupovic M (2012) Recombination between RNA viruses and plasmids might have played a central role in the origin and evolution of small DNA viruses. BioEssays 34:867–870. doi: 10.1002/bies.201200083 CrossRefPubMedGoogle Scholar
  25. Krupovic M, Ravantti JJ, Bamford DH (2009) Geminiviruses: a tale of a plasmid becoming a virus. BMC Evol Biol 9:112. http://www.biomedcentral.com/1471-2148/9/112. doi:  10.1186/1471-2148-9-112
  26. Lefeuvre P, Lett JM, Varsani A, Martin DP (2009) Widely conserved recombination patterns among single-stranded DNA viruses. J Virol 83:2697–2707. doi: 10.1128/jvi.02152-08 CrossRefPubMedGoogle Scholar
  27. Liu H, Fu Y, Li B, Yu X, Xie J, Cheng J, Ghabrial SA, Li G, Yi X, Jiang D (2011) Widespread horizontal gene transfer from circular single-stranded DNA viruses to eukaryotic genomes. BMC Evol Biol 11:276. http://www.biomedcentral.com/1471-2148/11/276. doi:  10.1186/1471-2148-11-276 Google Scholar
  28. Lopez-Bueno A, Tamames J, Velazquez D, Moya A, Quesada A, Alcami A (2009) High diversity of the viral community from an Antarctic lake. Science 326:858–861. doi: 10.1126/science.1179287 CrossRefPubMedGoogle Scholar
  29. Martin DP, Biagini P, Lefeuvre P, Golden M, Roumagnac P, Varsani A (2011) Recombination in eukaryotic single stranded DNA viruses. Viruses 3:1699–1738. doi: 10.3390/v3091699 CrossRefPubMedGoogle Scholar
  30. McDaniel L, Rosario K, Breitbart M, Paul J (2013) Comparative metagenomics : Natural populations of induced prophages demonstrate highly unique, lower diversity viral sequences. Env Microbiol (in press)Google Scholar
  31. Mochizuki T, Krupovic M, Pehau-Arnaudet G, Sako Y, Forterre P, Prangishvili D (2012) Archaeal virus with exceptional virion architecture and the largest single-stranded DNA genome. Proc Natl Acad Sci USA 109:13386–13391. doi: 10.1073/pnas.1203668109 CrossRefPubMedGoogle Scholar
  32. Morens DM, Fauci AS (2012) Emerging infectious diseases in 2012: 20 years after the Institute of Medicine report. mBio 3 e00494-12. doi:  10.1128/mBio.00494-12
  33. Pietilä MK, Roine E, Paulin L, Kalkkinen N, Bamford DH (2009) An ssDNA virus infecting archaea: a new lineage of viruses with a membrane envelope. Mol Microbiol 72:307–319. doi: 10.1111/j.1365-2958.2009.06642.x CrossRefPubMedGoogle Scholar
  34. Rosario K, Dayaram A, Marinov M, Ware J, Kraberger S, Stainton D, Breitbart M, Varsani A (2012a) Diverse circular ssDNA viruses discovered in dragonflies (Odonata: epiprocta). J Gen Virol 93:2668–2681. doi: 10.1099/vir.0.045948-0 CrossRefPubMedGoogle Scholar
  35. Rosario K, Duffy S, Breitbart M (2012b) A field guide to eukaryotic circular single-stranded DNA viruses: insights gained from metagenomics. Arch Virol 157:1851–1871. doi: 10.1007/s00705-012-1391-y CrossRefPubMedGoogle Scholar
  36. Saccardo F, Cettul E, Palmano S, Noris E, Firrao G (2011) On the alleged origin of geminiviruses from extrachromosomal DNAs of phytoplasmas. BMC Evol Biol 11: 185 http://www.biomedcentral.com/1471-2148/11/185. doi:  10.1186/1471-2148-11-185
  37. Villarreal LP (2004) Viruses and the evolution of life. ASM Press, WashingtonGoogle Scholar
  38. Villarreal LP, DeFilippis VR (2000) A hypothesis for DNA viruses as the origin of eukaryotic replication proteins. J Virol 74:7079–7084. doi: 10.1128/JVI.74.15.7079-7084.2000 CrossRefPubMedGoogle Scholar
  39. Watson J, Baker T, Bell S, Gann A, Levine M, Losick R (2014) Molecular Biology of the Gene. Cold Spring Harbor Press, New YorkGoogle Scholar
  40. Whon TW, Kim M-S, Roh SW, Shin N-R, Lee H-W, Bae J-W (2012) Metagenomic characterization of airborne viral DNA diversity in the near-surface atmosphere. J Virol 86:8221–8231. doi: 10.1128/jvi.00293-12 CrossRefPubMedGoogle Scholar
  41. Yang W (2010) Topoisomerases and site-specific recombinases: similarities in structure and mechanism. Crit Rev Biochem Mol Biol 45:520–534. doi: 10.3109/10409238.2010.513375 Google Scholar
  42. Yaniv M (2009) Small DNA tumour viruses and their contributions to our understanding of transcription control. Virology 384:369–374. doi: 10.1016/j.virol.2008.11.002 CrossRefPubMedGoogle Scholar
  43. Yu X, Li B, Fu Y, Jiang D, Ghabrial SA, Li G, Peng Y, Xie J, Cheng J, Huang J, Yi X (2010) A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc Natl Acad Sci USA 107:8387–8392. doi: 10.1073/pnas.0913535107 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Biology Department, Center for Life in Extreme EnvironmentsPortland State UniversityPortlandUSA

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