A field guide to eukaryotic circular single-stranded DNA viruses: insights gained from metagenomics

Archives of Virology volume 157, pages1851–1871(2012)Cite this article

An Erratum to this article was published on 11 August 2012

Abstract

Despite their small size and limited protein-coding capacity, the rapid evolution rates of single-stranded DNA (ssDNA) viruses have led to their emergence as serious plant and animal pathogens. Recently, metagenomics has revealed an unprecedented diversity of ssDNA viruses, expanding their known environmental distributions and host ranges. This review summarizes and contrasts the basic characteristics of known circular ssDNA viral groups, providing a resource for analyzing the wealth of ssDNA viral sequences identified through metagenomics. Since ssDNA viruses are largely identified based on conserved rolling circle replication proteins, this review highlights distinguishing motifs and catalytic residues important for replication. Genomes identified through metagenomics have demonstrated unique ssDNA viral genome architectures and revealed characteristics that blur the boundaries between previously well-defined groups. Metagenomic discovery of ssDNA viruses has created both a challenge to current taxonomic classification schemes and an opportunity to revisit hypotheses regarding the evolutionary history of these viruses.

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References

  1. 1.

    Balamurugan V, Kataria JM (2006) Economically important non-oncogenic immunosuppressive viral diseases of chicken—current status. Vet Res Commun 30:541–566

    PubMed  CAS  Article  Google Scholar 

  2. 2.

    Bassami MR, Berryman D, Wilcox GE, Raidal SR (1998) Psittacine beak and feather disease virus nucleotide sequence analysis and its relationship to porcine circovirus, plant circoviruses, and chicken anaemia virus. Virology 249:453–459

    PubMed  CAS  Article  Google Scholar 

  3. 3.

    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

    PubMed  CAS  Article  Google Scholar 

  4. 4.

    Bergoin M, Tijssen P (2010) Densoviruses: a highly diverse group of arthropod parvoviruses. In: Asgari S, Johnson K (eds) Insect Virology. Caister Academic Press, Great Britain, pp 59–82

    Google Scholar 

  5. 5.

    Biagini P, Gallian P, Attoui H, Touinssi M, Cantaloube JF, de Micco P, de Lamballerie X (2001) Genetic analysis of full-length genomes and subgenomic sequences of TT virus-like mini virus human isolates. J Gen Virol 82:379–383

    PubMed  CAS  Google Scholar 

  6. 6.

    Biagini P (2011) ICTV taxonomy proposal: restructuring and expansion of the family Anelloviridae. http://talk.ictvonline.org/files/proposals/taxonomy_proposals_vertebrate1/m/vert01/3911.aspx

  7. 7.

    Biagini P (2011) ICTV taxonomy proposal: restructuring and expansion of the family Circoviridae. http://talk.ictvonline.org/files/proposals/taxonomy_proposals_vertebrate1/m/vert01/3912.aspx

  8. 8.

    Binga EK, Lasken RS, Neufeld JD (2008) Something from (almost) nothing: the impact of multiple displacement amplification on microbial ecology. ISME J 2:233–241

    PubMed  CAS  Article  Google Scholar 

  9. 9.

    Blinkova O, Victoria J, Li Y, Keele BF, Sanz C, Ndjango J-BN, Peeters M, Travis D, Lonsdorf EV, Wilson ML, Pusey AE, Hahn BH, Delwart EL (2010) Novel circular DNA viruses in stool samples of wild-living chimpanzees. J Gen Virol 91:74–86

    PubMed  CAS  Article  Google Scholar 

  10. 10.

    Breitbart M, Rohwer F (2005) Method for discovering novel DNA viruses in blood using viral particle selection and shotgun sequencing. Biotechniques 39:729–736

    PubMed  CAS  Article  Google Scholar 

  11. 11.

    Briddon RW, Bull SE, Amin I, Idris AM, Mansoor S, Bedford ID, Dhawan P, Rishi N, Siwatch SS, Abdel-Salam AM, Brown JK, Zafar Y, Markham PG (2003) Diversity of DNA beta, a satellite molecule associated with some monopartite begomoviruses. Virology 312:106–121

    PubMed  CAS  Article  Google Scholar 

  12. 12.

    Briddon RW, Bull SE, Amin I, Mansoor S, Bedford ID, Rishi N, Siwatch SS, Zafar Y, Abdel-Salam AM, Markham PG (2004) Diversity of DNA 1: a satellite-like molecule associated with monopartite begomovirus-DNA beta complexes. Virology 324:462–474

    PubMed  CAS  Article  Google Scholar 

  13. 13.

    Briddon RW, Stanley J (2006) Subviral agents associated with plant single-stranded DNA viruses. Virology 344:198–210

    PubMed  CAS  Article  Google Scholar 

  14. 14.

    Briddon RW, Patil BL, Bagewadi B, Nawaz-ul-Rehman MS, Fauquet CM (2010) Distinct evolutionary histories of the DNA-A and DNA-B components of bipartite begomoviruses. BMC Evol Biol 10:97

    PubMed  Article  CAS  Google Scholar 

  15. 15.

    Carstens E (2010) Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2009). Arch Virol 155:133–146

    PubMed  CAS  Article  Google Scholar 

  16. 16.

    Cheung AK (2004) Identification of an octanucleotide motif sequence essential for viral protein, DNA, and progeny virus biosynthesis at the origin of DNA replication of porcine circovirus type 2. Virology 324:28–36

    PubMed  CAS  Article  Google Scholar 

  17. 17.

    Cheung AK (2004) Detection of template strand switching during initiation and termination of DNA replication of porcine circovirus. J Virol 78:4268–4277

    PubMed  CAS  Article  Google Scholar 

  18. 18.

    Choudhury NR, Malik PS, Singh DK, Islam MN, Kaliappan K, Mukherjee SK (2006) The oligomeric Rep protein of Mungbean yellow mosaic India virus (MYMIV) is a likely replicative helicase. Nucl Acids Res 34:6362–6377

    PubMed  CAS  Article  Google Scholar 

  19. 19.

    Clerot D, Bernardi F (2006) DNA helicase activity is associated with the replication initiator protein Rep of Tomato yellow leaf curl geminivirus. J Virol 80:11322–11330

    PubMed  CAS  Article  Google Scholar 

  20. 20.

    Culley AI, Lang AS, Suttle CA (2006) Metagenomic analysis of coastal RNA virus communities. Science 312:1795–1798

    PubMed  CAS  Article  Google Scholar 

  21. 21.

    Davidson I, Shulman LM (2008) Unraveling the puzzle of human anellovirus infections by comparison with avian infections with the chicken anemia virus. Virus Res 137:1–15

    PubMed  CAS  Article  Google Scholar 

  22. 22.

    Day JM, Ballard LL, Duke MV, Scheffler BE, Zsak L (2010) Metagenomic analysis of the turkey gut RNA virus community. Virol J 7:313

    PubMed  Article  CAS  Google Scholar 

  23. 23.

    de Villiers E-M, zur Hausen H (2009) TT viruses—the still elusive human pathogens. Springer, Berlin

    Google Scholar 

  24. 24.

    de Villiers EM, Borkosky SS, Kimmel R, Gunst K, Fei JW (2011) The diversity of torque teno viruses: In vitro replication leads to the formation of additional replication-competent subviral molecules. J Virol 85:7284–7295

    PubMed  Article  CAS  Google Scholar 

  25. 25.

    del Solar G, Giraldo R, Ruiz-Echevarria MJ, Espinosa M, Diaz-Orejas R (1998) Replication and control of circular bacterial plasmids. Microbiol Mol Biol Rev 62:434–464

    PubMed  Google Scholar 

  26. 26.

    Desbiez C, David C, Mettouchi A, Laufs J, Gronenborn B (1995) Rep protein of tomato yellow leaf curl geminivirus has an ATPase activity required for viral DNA replication. Proc Natl Acad Sci USA 92:5640–5644

    PubMed  CAS  Article  Google Scholar 

  27. 27.

    Djikeng A, Kuzmickas R, Anderson NG, Spiro DJ (2009) Metagenomic analysis of RNA viruses in a fresh water lake. PLoS ONE 4:e7264

    PubMed  Article  CAS  Google Scholar 

  28. 28.

    Dry IB, Krake LR, Rigden JE, Rezaian MA (1997) A novel subviral agent associated with a geminivirus: The first report of a DNA satellite. Proc Natl Acad Sci USA 94:7088–7093

    PubMed  CAS  Article  Google Scholar 

  29. 29.

    Duffy S, Shackelton LA, Holmes EC (2008) Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9:267–276

    PubMed  CAS  Article  Google Scholar 

  30. 30.

    Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    PubMed  CAS  Article  Google Scholar 

  31. 31.

    Fauquet C, Briddon R, Brown J, Moriones E, Stanley J, Zerbini M, Zhou X (2008) Geminivirus strain demarcation and nomenclature. Arch Virol 153:783–821

    PubMed  CAS  Article  Google Scholar 

  32. 32.

    Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (2005) Virus Taxonomy: eighth report of the international committee on Taxonomy of Viruses. Academic Press, San Diego

    Google Scholar 

  33. 33.

    Faurez F, Dory D, Grasland B, Jestin A (2009) Replication of porcine circoviruses. Virol J 6:60

    PubMed  Article  CAS  Google Scholar 

  34. 34.

    Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz H-R, Ceric G, Forslund K, Eddy SR, Sonnhammer ELL, Bateman A (2008) The Pfam protein families database. Nucleic Acids Res 36:D281–D288

    PubMed  CAS  Article  Google Scholar 

  35. 35.

    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

    PubMed  CAS  Article  Google Scholar 

  36. 36.

    Ge XY, Li JL, Peng C, Wu LJ, Yang XL, Wu YQ, Zhang YZ, Shi ZL (2011) Genetic diversity of novel circular ssDNA viruses in bats in China. J Gen Virol 92:2646–2653

    PubMed  CAS  Article  Google Scholar 

  37. 37.

    Gibbs MJ, Weiller GF (1999) Evidence that a plant virus switched hosts to infect a vertebrate and then recombined with a vertebrate-infecting virus. Proc Natl Acad Sci USA 96:8022–8027

    PubMed  CAS  Article  Google Scholar 

  38. 38.

    Gibbs MJ, Smeianov VV, Steele JL, Upcroft P, Efimov BA (2006) Two families of Rep-like genes that probably originated by interspecies recombination are represented in viral, plasmid, bacterial, and parasitic protozoan genomes. Mol Biol Evol 23:1097–1100

    PubMed  CAS  Article  Google Scholar 

  39. 39.

    Gorbalenya AE, Koonin EV, Wolf YI (1990) A new superfamily of putative NTP-binding domains encoded by genomes of small DNA and RNA viruses. FEBS Lett 262:145–148

    PubMed  CAS  Article  Google Scholar 

  40. 40.

    Gorbalenya AE, Koonin EV (1993) Helicases: amino acid sequence comparisons and structure-function relationships. Curr Opin Struct Biol 3:419–429

    CAS  Article  Google Scholar 

  41. 41.

    Grigoras I, Timchenko T, Grande-Perez A, Katul L, Vetten HJ, Gronenborn B (2010) High variability and rapid evolution of a nanovirus. J Virol 84:9105–9117

    PubMed  CAS  Article  Google Scholar 

  42. 42.

    Gutierrez C (1999) Geminivirus DNA replication. Cell Mol Life Sci 56:313–329

    PubMed  CAS  Article  Google Scholar 

  43. 43.

    Hafner GJ, Stafford MR, Wolter LC, Harding RM, Dale JL (1997) Nicking and joining activity of banana bunchy top virus replication protein in vitro. J Gen Virol 78:1795–1799

    PubMed  CAS  Google Scholar 

  44. 44.

    Hanley-Bowdoin L, Settlage SB, Orozco BM, Nagar S, Robertson D (1999) Geminiviruses: Models for plant DNA replication, transcription, and cell cycle regulation. Crit Rev Plant Sci 18:71–106

    CAS  Article  Google Scholar 

  45. 45.

    Heyraud-Nitschke F, Schumacher S, Laufs J, Schaefer S, Schell J, Gronenborn B (1995) Determination of the origin cleavage and joining domain of geminivirus Rep proteins. Nucleic Acids Res 23:910–916

    PubMed  CAS  Article  Google Scholar 

  46. 46.

    Heyraud F, Matzeit V, Kammann M, Schaefer S, Schell J, Gronenborn B (1993) Identification of the initiation sequence for viral-strand DNA synthesis of wheat dwarf virus. EMBO J 12:4445–4452

    PubMed  CAS  Google Scholar 

  47. 47.

    Ilyina TV, Koonin EV (1992) Conserved sequence motifs in the initiator proteins for rolling circle DNA replication encoded by diverse replicons from eubacteria, eucaryotes and archaebacteria. Nucleic Acids Res 20:3279–3285

    PubMed  CAS  Article  Google Scholar 

  48. 48.

    Iyer LM, Balaji S, Koonin EV, Aravind L (2006) Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res 117:156–184

    PubMed  CAS  Article  Google Scholar 

  49. 49.

    Jeske H, Lutgemeier M, Preiss W (2001) DNA forms indicate rolling circle and recombination-dependent replication of Abutilon mosaic virus. EMBO J 20:6158–6167

    PubMed  CAS  Article  Google Scholar 

  50. 50.

    Kapitonov VV, Jurka J (2001) Rolling-circle transposons in eukaryotes. Proc Natl Acad Sci USA 98:8714–8719

    PubMed  CAS  Article  Google Scholar 

  51. 51.

    Katzourakis A, Gifford RJ (2010) Endogenous viral elements in animal genomes. PLoS Genet 6:e1001191

    PubMed  Article  CAS  Google Scholar 

  52. 52.

    Khan SA (1997) Rolling-circle replication of bacterial plasmids. Microbiol Mol Biol Rev 61:442–455

    PubMed  CAS  Google Scholar 

  53. 53.

    Kim KH, Chang HW, Nam YD, Roh SW, Kim MS, Sung Y, Jeon CO, Oh HM, Bae JW (2008) Amplification of uncultured single-stranded DNA viruses from rice paddy soil. Appl Environ Microbiol 74:5975–5985

    PubMed  CAS  Article  Google Scholar 

  54. 54.

    Kim KH, Bae JW (2011) Amplification methods bias metagenomic libraries of uncultured single-stranded and double-stranded DNA viruses. Appl Environ Microbiol 77:7663–7668

    PubMed  CAS  Article  Google Scholar 

  55. 55.

    Koonin EV, Ilyina TV (1992) Geminivirus replication proteins are related to prokaryotic plasmid rolling circle DNA-replication initiator proteins. J Gen Virol 73:2763–2766

    PubMed  CAS  Article  Google Scholar 

  56. 56.

    Krupovic M, Ravantti JJ, Bamford DH (2009) Geminiviruses: a tale of a plasmid becoming a virus. BMC Evol Biol 9:112

    PubMed  Article  CAS  Google Scholar 

  57. 57.

    Latham G (2001) DNase I demystified (Ambion, Inc.). http://www.invitrogen.com/site/us/en/home/References/Ambion-Tech-Support/nuclease-enzymes/general-articles/dnase-i-demystified.html

  58. 58.

    Laufs J, Jupin I, David C, Schumacher S, HeyraudNitschke F, Gronenborn B (1995) Geminivirus replication: Genetic and biochemical characterization of Rep protein function, a review. Biochimie 77:765–773

    PubMed  CAS  Article  Google Scholar 

  59. 59.

    Laufs J, Schumacher S, Geisler N, Jupin I, Gronenborn B (1995) Identification of the nicking tyrosine of geminivirus Rep protein. FEBS Lett 377:258–262

    PubMed  CAS  Article  Google Scholar 

  60. 60.

    Laufs J, Traut W, Heyraud F, Matzeit V, Rogers SG, Schell J, Gronenborn B (1995) In vitro cleavage and joining at the viral origin of replication by the replication initiator protein of tomato yellow leaf curl virus. Proc Natl Acad Sci USA 92:3879–3883

    PubMed  CAS  Article  Google Scholar 

  61. 61.

    Lefeuvre P, Lett JM, Varsani A, Martin DP (2009) Widely conserved recombination patterns among single-stranded DNA viruses. J Virol 83:2697–2707

    PubMed  CAS  Article  Google Scholar 

  62. 62.

    Lefeuvre P, Harkins GW, Lett JM, Briddon RW, Chase MW, Moury B, Martin DP (2011) Evolutionary time-scale of the begomoviruses: Evidence from integrated sequences in the Nicotiana genome. PLoS ONE 6:e19193

    PubMed  CAS  Article  Google Scholar 

  63. 63.

    Leppik L, Gunst K, Lehtinen M, Dillner J, Streker K, de Villiers E-M (2007) In vivo and in vitro intragenomic rearrangement of TT viruses. J Virol 81:9346–9356

    PubMed  CAS  Article  Google Scholar 

  64. 64.

    Li L, Kapoor A, Slikas B, Bamidele OS, Wang C, Shaukat S, Masroor MA, Wilson ML, Ndjango J-BN, Peeters M, Gross-Camp ND, Muller MN, Hahn BH, Wolfe ND, Triki H, Bartkus J, Zaidi SZ, Delwart E (2010) Multiple diverse circoviruses infect farm animals and are commonly found in human and chimpanzee feces. J Virol 84:1674–1682

    PubMed  CAS  Article  Google Scholar 

  65. 65.

    Li L, Victoria JG, Wang C, Jones M, Fellers GM, Kunz TH, Delwart E (2010) Bat guano virome: predominance of dietary viruses from insects and plants plus novel mammalian viruses. J Virol 84:6955–6965

    PubMed  CAS  Article  Google Scholar 

  66. 66.

    Li LL, Shan TL, Soji OB, Alam MM, Kunz TH, Zaidi SZ, Delwart E (2011) Possible cross-species transmission of circoviruses and cycloviruses among farm animals. J Gen Virol 92:768–772

    PubMed  CAS  Article  Google Scholar 

  67. 67.

    Liu HQ, Fu YP, Li B, Yu X, Xie JT, Cheng JS, Ghabrial SA, Li GQ, Yi XH, Jiang DH (2011) Widespread horizontal gene transfer from circular single-stranded DNA viruses to eukaryotic genomes. BMC Evol Biol 11:276

    PubMed  Article  CAS  Google Scholar 

  68. 68.

    Londono A, Riego-Ruiz L, Arguello-Astorga GR (2010) DNA-binding specificity determinants of replication proteins encoded by eukaryotic ssDNA viruses are adjacent to widely separated RCR conserved motifs. Arch Virol 155:1033–1046

    PubMed  CAS  Article  Google Scholar 

  69. 69.

    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

    PubMed  CAS  Article  Google Scholar 

  70. 70.

    Lorinez M, Csagola A, Farkas SL, Szekely C, Tuboly T (2011) First detection and analysis of a fish circovirus. J Gen Virol 92:1817–1821

    Article  CAS  Google Scholar 

  71. 71.

    Ma Y, Paulsen IT, Palenik B (2011) Analysis of two marine metagenomes reveals the diversity of plasmids in oceanic environments. Environ Microbiol 14:453–466

    PubMed  Article  CAS  Google Scholar 

  72. 72.

    Mandal B (2010) Advances in small isometric multicomponent ssDNA viruses infecting plants. Indian J Virol 21:18–30

    Article  Google Scholar 

  73. 73.

    Mansoor S, Zafar Y, Briddon RW (2006) Geminivirus disease complexes: the threat is spreading. Trends Plant Sci 11:209–212

    PubMed  CAS  Article  Google Scholar 

  74. 74.

    Martin D, Shepherd D (2009) The epidemiology, economic impact and control of maize streak disease. Food Secur 1:305–315

    Article  Google Scholar 

  75. 75.

    Martin DP, Biagini P, Lefeuvre P, Golden M, Roumagnac P, Varsani A (2011) Recombination in eukaryotic single stranded DNA viruses. Viruses 3:1699–1738

    PubMed  CAS  Article  Google Scholar 

  76. 76.

    McDaniel L, Breitbart M, Mobberley J, Long A, Haynes M, Rohwer F, Paul JH (2008) Metagenomic analysis of lysogeny in Tampa Bay: implications for prophage gene expression. PLoS ONE 3:e3263

    PubMed  Article  CAS  Google Scholar 

  77. 77.

    Merits A, Fedorkin ON, Guo D, Kalinina NO, Morozov SY (2000) Activities associated with the putative replication initiation protein of Coconut foliar decay virus, a tentative member of the genus Nanovirus. J Gen Virol 81:3099–3106

    PubMed  CAS  Google Scholar 

  78. 78.

    Nash TE, Dallas MB, Reyes MI, Buhrman GK, Ascencio-Ibanez JT, Hanley-Bowdoin L (2011) Functional analysis of a novel motif conserved across geminivirus Rep proteins. J Virol 85:1182–1192

    PubMed  CAS  Article  Google Scholar 

  79. 79.

    Ng TF, Duffy S, Polston JE, Bixby E, Vallad GE, Breitbart M (2011) Exploring the diversity of plant DNA viruses and their satellites using vector-enabled metagenomics on whiteflies. PLoS One 6:e19050

    PubMed  CAS  Article  Google Scholar 

  80. 80.

    Ng TF, Wheeler E, Greig D, Waltzek TB, Gulland F, Breitbart M (2011) Metagenomic identification of a novel anellovirus in Pacific harbor seal (Phoca vitulina richardsii) lung samples and its detection in samples from multiple years. J Gen Virol 92:1318–1323

    PubMed  CAS  Article  Google Scholar 

  81. 81.

    Ng TFF, Manire C, Borrowman K, Langer T, Ehrhart L, Breitbart M (2009) Discovery of a novel single-stranded DNA virus from a sea turtle fibropapilloma by using viral metagenomics. J Virol 83:2500–2509

    PubMed  CAS  Article  Google Scholar 

  82. 82.

    Ng TFF, Suedmeyer WK, Wheeler E, Gulland F, Breitbart M (2009) Novel anellovirus discovered from a mortality event of captive California sea lions. J Gen Virol 90:1256–1261

    PubMed  CAS  Article  Google Scholar 

  83. 83.

    Ng TFF, Willner DL, Lim YW, Schmieder R, Chau B, Nilsson C, Anthony S, Ruan YJ, Rohwer F, Breitbart M (2011) Broad surveys of DNA viral diversity obtained through viral metagenomics of mosquitoes. PLoS ONE 6:e20579

    PubMed  CAS  Article  Google Scholar 

  84. 84.

    Niagro FD, Forsthoefel AN, Lawther RP, Kamalanathan L, Ritchie BW, Latimer KS, Lukert PD (1998) Beak and feather disease virus and porcine circovirus genomes: intermediates between the geminiviruses and plant circoviruses. Arch Virol 143:1723–1744

    PubMed  CAS  Article  Google Scholar 

  85. 85.

    Niel C, Diniz-Mendes L, Devalle S (2005) Rolling-circle amplification of Torque teno virus (TTV) complete genomes from human and swine sera and identification of a novel swine TTV genogroup. J Gen Virol 86:1343–1347

    PubMed  CAS  Article  Google Scholar 

  86. 86.

    Novick RP (1998) Contrasting lifestyles of rolling-circle phages and plasmids. Trends Biochem Sci 23:434–438

    PubMed  CAS  Article  Google Scholar 

  87. 87.

    Orozco BM, Kong LJ, Batts LA, Elledge S, Hanley-Bowdoin L (2000) The multifunctional character of a geminivirus replication protein is reflected by its complex oligomerization properties. J Biol Chem 275:6114–6122

    PubMed  CAS  Article  Google Scholar 

  88. 88.

    Oshima K, Kakizawa S, Nishigawa H, Kuboyama T, Miyata S, Ugaki M, Namba S (2001) A plasmid of phytoplasma encodes a unique replication protein having both plasmid- and virus-like domains: Clue to viral ancestry or result of virus/plasmid recombination? Virology 285:270–277

    PubMed  CAS  Article  Google Scholar 

  89. 89.

    Park EJ, Kim KH, Abell GC, Kim MS, Roh SW, Bae JW (2011) Metagenomic analysis of the viral communities in fermented foods. Appl Environ Microbiol 77:1284–1291

    PubMed  CAS  Article  Google Scholar 

  90. 90.

    Phan TG, Kapusinszky B, Wang CL, Rose RK, Lipton HL, Delwart EL (2011) The fecal viral flora of wild rodents. PLoS Pathogens 7:e1002218

    PubMed  CAS  Article  Google Scholar 

  91. 91.

    Pietila 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

    PubMed  CAS  Article  Google Scholar 

  92. 92.

    Prasetyo AA, Kamahora T, Kuroishi A, Murakami K, Hino S (2009) Replication of chicken anemia virus (CAV) requires apoptin and is complemented by VP3 of human torque teno virus (TTV). Virology 385:85–92

    PubMed  CAS  Article  Google Scholar 

  93. 93.

    Rijsewijk FAM, dos Santos HF, Teixeira TF, Cibulski SP, Varela APM, Dezen D, Franco AC, Roehe PM (2011) Discovery of a genome of a distant relative of chicken anemia virus reveals a new member of the genus Gyrovirus. Arch Virol 156:1097–1100

    PubMed  CAS  Article  Google Scholar 

  94. 94.

    Rojas MR, Hagen C, Lucas WJ, Gilbertson RL (2005) Exploiting chinks in the plant’s armor: Evolution and emergence of geminiviruses. Annu Rev Phytopathol 43:361–394

    PubMed  CAS  Article  Google Scholar 

  95. 95.

    Rosario K, Duffy S, Breitbart M (2009) Diverse circovirus-like genome architectures revealed by environmental metagenomics. J Gen Virol 90:2418–2424

    PubMed  CAS  Article  Google Scholar 

  96. 96.

    Rosario K, Nilsson C, Lim YW, Yijun R, Breitbart M (2009) Metagenomic analysis of viruses in reclaimed water. Environ Microbiol 11:2806–2820

    PubMed  CAS  Article  Google Scholar 

  97. 97.

    Rosario K, Breitbart M (2011) Exploring the viral world through metagenomics. Curr Opin Virol 1:289–297

    PubMed  CAS  Article  Google Scholar 

  98. 98.

    Rosario K, Marinov M, Stainton D, Kraberger S, Wiltshire EJ, Collings DA, Walters M, Martin DP, Breitbart M, Varsani A (2011) Dragonfly cyclovirus, a novel single-stranded DNA virus discovered in dragonflies (Odonata: Anisoptera). J Gen Virol 92:1302–1308

    PubMed  CAS  Article  Google Scholar 

  99. 99.

    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

    PubMed  CAS  Article  Google Scholar 

  100. 100.

    Sauvage V, Cheval J, Foulongne V, Gouilh MA, Pariente K, Manuguerra JC, Richardson J, Dereure O, Lecuit M, Burguiere A, Caro V, Eloit M (2011) Identification of the first human Gyrovirus, a virus related to chicken anemia virus. J Virol 85:7948–7950

    PubMed  CAS  Article  Google Scholar 

  101. 101.

    Segales J, Allan GM, Domingo M (2005) Porcine circovirus diseases. Anim Health Res Rev/Conf Res Workers Anim Dis 6:119–142

    Article  Google Scholar 

  102. 102.

    Shan TL, Li LL, Simmonds P, Wang CL, Moeser A, Delwart E (2011) The fecal virome of pigs on a high-density farm. J Virol 85:11697–11708

    PubMed  CAS  Article  Google Scholar 

  103. 103.

    Steinfeldt T, Finsterbusch T, Mankertz A (2001) Rep and Rep ‘ protein of Porcine circovirus type 1 bind to the origin of replication in vitro. Virology 291:152–160

    PubMed  CAS  Article  Google Scholar 

  104. 104.

    Steinfeldt T, Finsterbusch T, Mankertz A (2006) Demonstration of nicking/joining activity at the origin of DNA replication associated with the Rep and Rep’ proteins of porcine circovirus type 1. J Virol 80:6225–6234

    PubMed  CAS  Article  Google Scholar 

  105. 105.

    Steinfeldt T, Finsterbusch T, Mankertz A (2007) Functional analysis of cis- and trans-acting replication factors of porcine circovirus type 1. J Virol 81:5696–5704

    PubMed  CAS  Article  Google Scholar 

  106. 106.

    Stenlund A (2003) Initiation of DNA replication: Lessons from viral initiator proteins. Nat Rev Mol Cell Biol 4:777–785

    PubMed  CAS  Google Scholar 

  107. 107.

    Streck AF, Bonatto SL, Homeier T, Souza CK, Gonçalves KR, Gava D, Canal CW, Truyen U (2011) High rate of viral evolution in the capsid protein of porcine parvovirus. J Gen Virol 92:2628–2636

    PubMed  CAS  Article  Google Scholar 

  108. 108.

    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 28:2731–2739

    PubMed  CAS  Article  Google Scholar 

  109. 109.

    Thurber RV (2011) Methods in Viral Metagenomics. In: de Bruijn FJ (ed) Handbook of molecular microbial ecology II. Wiley, New York, pp 15–24

    Google Scholar 

  110. 110.

    Timchenko T, de Kouchkovsky F, Katul L, David C, Vetten HJ, Gronenborn B (1999) A single Rep protein initiates replication of multiple genome components of faba bean necrotic yellows virus, a single-stranded DNA virus of plants. J Virol 73:10173–10182

    PubMed  CAS  Google Scholar 

  111. 111.

    Todd D, Hino S, Mankertz A, Mishiro S, Raidal S, Ritchie BW, Biagini P, Okamoto H, Niel C, Bendinelli M, Teo CG (2005) Family Circoviridae. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds) Virus taxonomy: eighth report of the international committee on taxonomy of viruses. Academic Press, San Diego, pp 327–341

    Google Scholar 

  112. 112.

    Varsani A, Shepherd D, Dent K, Monjane A, Rybicki E, Martin D (2009) A highly divergent South African geminivirus species illuminates the ancient evolutionary history of this family. Virol J 6:36

    PubMed  Article  CAS  Google Scholar 

  113. 113.

    Vega-Rocha S, Gronenborn B, Gronenborn AM, Campos-Olivas R (2007) Solution structure of the endonuclease domain from the master replication initiator protein of the nanovirus Faba bean necrotic yellows virus and comparison with the corresponding geminivirus and circovirus structures. Biochemistry 46:6201–6212

    PubMed  CAS  Article  Google Scholar 

  114. 114.

    Vega Thurber RL, Barott KL, Hall D, Liu H, Rodriguez-Mueller B, Desnues C, Edwards RA, Haynes M, Angly FE, Wegley L, Rohwer FL (2008) Metagenomic analysis indicates that stressors induce production of herpes-like viruses in the coral Porites compressa. Proc Natl Acad Sci USA 105:18413–18418

    PubMed  CAS  Article  Google Scholar 

  115. 115.

    Wen LB, He KW, Yang HC, Ni YX, Zhang XH, Guo RL, Pan QX (2008) Complete nucleotide sequence of a novel porcine circo-virus-like agent and its infectivity in vitro. Sci China Ser C 51:453–458

    CAS  Article  Google Scholar 

  116. 116.

    Wen LB, He KW, Yu ZY, Mao AH, Ni YX, Zhang XH, Guo RL, Li B, Wang XM, Zhou JM, Lv LX (2012) Complete genome sequence of a novel porcine circovirus-like agent. J Virol 86:639

    PubMed  CAS  Article  Google Scholar 

  117. 117.

    Willner D, Furlan M, Haynes M, Schmieder R, Angly FE, Silva J, Tammadoni S, Nosrat B, Conrad D, Rohwer F (2009) Metagenomic analysis of respiratory tract DNA viral communities in cystic fibrosis and non-cystic fibrosis individuals. PLoS ONE 4:e7370

    PubMed  Article  CAS  Google Scholar 

  118. 118.

    Yazdi HRB, Heydarnejad J, Massumi H (2008) Genome characterization and genetic diversity of beet curly top Iran virus: a geminivirus with a novel nonanucleotide. Virus Genes 36:539–545

    PubMed  CAS  Article  Google Scholar 

  119. 119.

    Yoon HS, Price DC, Stepanauskas R, Rajah VD, Sieracki ME, Wilson WH, Yang EC, Duffy S, Bhattacharya D (2011) Single-cell genomics reveals organismal interactions in uncultivated marine protists. Science 332:714–717

    PubMed  CAS  Article  Google Scholar 

  120. 120.

    Yu X, Li B, Fu YP, Jiang DH, Ghabrial SA, Li GQ, Peng YL, Xie JT, Cheng JS, Huang JB, Yi XH (2010) A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc Natl Acad Sci USA 107:8387–8392

    PubMed  CAS  Article  Google Scholar 

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Acknowledgments

The authors were supported by grants from the National Science Foundation Biodiversity Inventories program (DEB-1025915 to MB and DEB-1026095 to SD). Thanks to Yahayra Rosario-Cora for providing illustrations.

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Affiliations

  1. College of Marine Science, University of South Florida, Saint Petersburg, FL, 33701, USA

    Karyna Rosario & Mya Breitbart

  2. Department of Ecology, Evolution and Natural Resources, Rutgers, The State University of New Jersey, New Brunswick, NJ, 08901, USA

    Siobain Duffy

Authors
  1. Karyna Rosario
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  2. Siobain Duffy
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  3. Mya Breitbart
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Correspondence to Karyna Rosario.

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Rosario, K., Duffy, S. & Breitbart, M. A field guide to eukaryotic circular single-stranded DNA viruses: insights gained from metagenomics. Arch Virol 157, 1851–1871 (2012). https://doi.org/10.1007/s00705-012-1391-y

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Keywords

  • Rolling Circle Amplification
  • Circular Genome
  • Roll Circle Replication
  • ssDNA Virus
  • Circular ssDNA