Journal of Molecular Evolution

, Volume 66, Issue 3, pp 292–297

Bayesian Coalescent Analysis Reveals a High Rate of Molecular Evolution in GB Virus C

  • Camila M. Romano
  • Paolo M. de A. Zanotto
  • Edward C. Holmes
Article

Abstract

GB virus C/hepatitis G (GBV-C) is an RNA virus of the family Flaviviridae. Despite replicating with an RNA-dependent RNA polymerase, some previous estimates of rates of evolutionary change in GBV-C suggest that it fixes mutations at the anomalously low rate of ∼10−7 nucleotide substitution per site, per year. However, these estimates were largely based on the assumption that GBV-C and its close relative GBV-A (New World monkey GB viruses) codiverged with their primate hosts over millions of years. Herein, we estimated the substitution rate of GBV-C using the largest set of dated GBV-C isolates compiled to date and a Bayesian coalescent approach that utilizes the year of sampling and so is independent of the assumption of codivergence. This revealed a rate of evolutionary change approximately four orders of magnitude higher than that estimated previously, in the range of 10−2 to 10−3 sub/site/year, and hence in line with those previously determined for RNA viruses in general and the Flaviviridae in particular. In addition, we tested the assumption of host-virus codivergence in GBV-A by performing a reconciliation analysis of host and virus phylogenies. Strikingly, we found no statistical evidence for host-virus codivergence in GBV-A, indicating that substitution rates in the GB viruses should not be estimated from host divergence times.

Keywords

GB virus C Molecular clock Substitution rate Codivergence Phylogeny Coalescent theory 

References

  1. Abe K (2001) GB virus-C/hepatiitis G virus. Japan J Infect Dis 54:55–63Google Scholar
  2. Adams NJ, Prescott LE, Jarvis LM, Lewis JC, McClure MO, Smith DB, Simmonds P (1998) Detection in chimpanzees of a novel flavivirus related to GB virus-C/hepatitis G virus. J Gen Virol 79:1871–1877PubMedGoogle Scholar
  3. Birkenmeyer LG, Desai SM, Muerhoff AS, Leary TP, Simons JN, Montes CC, Mushahwar IK (1998) Isolation of a GB virus-related genome from a chimpanzee. J Med Virol 56:44–51PubMedCrossRefGoogle Scholar
  4. Bukh J, Apgar CL (1997) Five new or recently discovered (GBV–A) virus species are indigenous to New World monkeys and may constitute a separate genus of the Flaviviridae. Virology 17:429–436CrossRefGoogle Scholar
  5. Canavez FC, Moreira MAM, Ladasky JJ, Pissinatti A, Parham P, Seuanez HN (1999) Molecular phylogeny of New World primates (Platyrrhini) based on β2-microglobulin DNA sequences. Mol Phylogenet Evol 12:74–82PubMedCrossRefGoogle Scholar
  6. Charleston MA (1998) Jungles: a new solution to the host/parasite phylogeny reconciliation problem. Math Biosci 149:191–223PubMedCrossRefGoogle Scholar
  7. Charleston MA, Page RDM (2002) Treemap, version 20 Available at: http://www.taxonomy.zoology.gla.ac.uk/mac/treemap/index.html
  8. Charleston MA, Robertson DL (2002) Preferential host switching by primate lentiviruses can account for phylogenetic similarity with the primate phylogeny. Syst Biol 51:528–535PubMedCrossRefGoogle Scholar
  9. Charrel RM, De Micco P, de Lamballerie X (1999) Phylogenetic analysis of GB viruses A and C: evidence for codivergence between virus isolates and their primate hosts. J Gen Virol 80:2329–2335PubMedGoogle Scholar
  10. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214PubMedCrossRefGoogle Scholar
  11. Hanada K, Suzuki Y, Gojobori T (2004) A large variation in the rates of synonymous substitution for RNA viruses and its relationship to a diversity of viral infection and transmission modes. Mol Biol Evol 21:1074–1080PubMedCrossRefGoogle Scholar
  12. Hershkovitz P (1977) Living New World monkeys (Platyrrhini). University of Chicago Press, ChicagoGoogle Scholar
  13. Jacobs SC, Larson A, Cheverud JM (1995) Phylogenetic relationships and orthogenetic evolution of coat color among tamarins (genus Saguinus). Syst Biol 44:515–532CrossRefGoogle Scholar
  14. Jenkins GM, Rambaut A, Pybus OG, Holmes EC (2002) Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. J Mol Evol 54:152–161CrossRefGoogle Scholar
  15. Katayama Y, Apichartpiyakul C, Handajani R, Ishido S, Hotta H (1997) GB virus C/hepatitis G virus (GBV-C/HGV) infection in Chiang Mai, Thailand, and identification of variants on the basis of 5′-untranslated region sequences. Arch Virol 142:2433–2445PubMedCrossRefGoogle Scholar
  16. Kosakovsky Pond SL, Frost SD (2005) Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531–2533CrossRefGoogle Scholar
  17. Kuiken T, Holmes EC, McCauley J, Rimmelzwaan GF, Williams CS, Grenfell BT (2006) Host species barriers to influenza virus infections. Science 312:394–397PubMedCrossRefGoogle Scholar
  18. Leary TP, Muerhoff AS, Simons JN, Pilot-Matias TJ, Erker JC, Chalmers ML, Schlauder GG, Dawson GJ, Desai SM, Mushahwar IK (1996) Sequence and genomic organization of GBV-C: a novel member of the flaviviridae associated with human non–A-E hepatitis. J Med Virol 48:60–67PubMedCrossRefGoogle Scholar
  19. Linnen J, Wages J Jr, Zhang-Keck ZY, Fry KE, Krawczynski KZ, Alter H, Koonin E, Gallagher M, Alter M, Hadziyannis S, Karayiannis P, Fung K, Nakatsuji Y, Shih JW, Young L, Piatak M Jr, Hoover C, Fernandez J, Chen S, Zou JC, Morris T, Hyams KC, Ismay S, Lifson JD, Hess G, Foung SK, Thomas H, Bradley D, Margolis H, Kim JP (1996) Molecular cloning and disease association of hepatitis G virus: a transfusion-transmissible agent. Science 26:505–508CrossRefGoogle Scholar
  20. Moaven LD, Hyland CA, Young IF, Bowden DS, McCaw R, Mison L, Locarnini SA (1996) Prevalence of hepatitis G virus in Queensland blood donors. Med J Aust 7:369–371Google Scholar
  21. Nakai K, Win KM, Oo SS, Arakawa Y, Abe K (2001) Molecular characteristic-based epidemiology of hepatitis B, C, and E viruses and GB virus C/hepatitis G virus in Myanmar. J Clin Microbiol 39:1536–1539PubMedCrossRefGoogle Scholar
  22. Nakao H, Okomoto H, Fukuda M, Tsuda F, Mitsui T, Masuko K, Iizuka H, Miyakawa Y, Mayumi M (1997) Mutation rate of GB virus C/hepatitis G virus over the entire genome and in subgenomic regions. Virology 233:43–50PubMedCrossRefGoogle Scholar
  23. Pavesi A (2001) Origin and evolution of GBV-C/hepatitis G virus and relationships with ancient human migrations. J Mol Evol 53:104–113PubMedGoogle Scholar
  24. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  25. Sarrazin C, Rüster B, Lee JH, Kronenberger B, Roth WK, Zeuzem S (2000) Prospective follow-up of patients with GBV-C/HGV infection: specific mutational patterns, clinical outcome, and genetic diversity. J Med Virol 62:191–198PubMedCrossRefGoogle Scholar
  26. Seipp S, Wahl R, Mueller H, Stremmel W, Theilmann L, Goeser T (1996) Sequence analysis of hepatitis GB virus C (GBV-C) isolates from 14 patients. Virus Res 46:81–88PubMedCrossRefGoogle Scholar
  27. Shao L, Shinzawa H, Zhang X, Smith DB, Watanabe H, Mitsuhashi H, Saito K, Saito T, Togashi H, Takahashi T (2000) Diversity of hepatitis G virus within a single infected individual. Virus Genes 21:215–221PubMedCrossRefGoogle Scholar
  28. Simmonds P (2001) 2000 Fleming Lecture. The origin and evolution of hepatitis viruses in humans. J Gen Virol 82:693–712PubMedGoogle Scholar
  29. Simmonds P, Smith DB (1999) Structural constraints on RNA virus evolution. J Virol 73:5787–5794PubMedGoogle Scholar
  30. Simons JN, Leary TP, Dawson GJ, Pilot-Matias TJ, Muerhoff AS, Schlauder GG, Desai SM, Mushahwar IK (1995) Isolation of novel virus-like sequences associated with human hepatitis. Nat Med 1:564–569PubMedCrossRefGoogle Scholar
  31. Suzuki Y, Katayama K, Fukushi S, Kageyama T, Oya A, Okamura H, Tanaka Y, Mizokami Y, Gojobori T (1999) Slow evolutionary rate of GB virus C/hepatitis G virus. J Mol Evol 48:383–389PubMedCrossRefGoogle Scholar
  32. Swofford DL (2003) PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods) Version 4. Sinauer Associates, Sunderland, MAGoogle Scholar
  33. Tacke M, Kiyosawa K, Stark K, Schlueter V, Ofenloch-Haehnle B, Hess G, Engel AM (1997) Detection of antibodies to a putative hepatitis G virus envelope protein. Lancet 1:318–320CrossRefGoogle Scholar
  34. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  35. Wertheim JO, Worobey M (2007) A challenge to the ancient origin of SIVagm based on African green monkey mitochondrial genomes. PLoS Pathog 3:e95PubMedCrossRefGoogle Scholar
  36. Worobey M, Holmes EC (2001) Homolgous recombination in GB virus C/hepatitis G virus. Mol Biol Evol 18:254–261PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Camila M. Romano
    • 1
    • 2
  • Paolo M. de A. Zanotto
    • 1
  • Edward C. Holmes
    • 2
    • 3
  1. 1.Laboratory of Molecular Evolution and Bioinformatics, Department of MicrobiologyBiomedical Sciences Institute–ICBII, University of São PauloSão PauloBrazil
  2. 2.Center for Infectious Disease Dynamics, Department of BiologyThe Pennsylvania State University, Mueller LaboratoryUniversity ParkUSA
  3. 3.Fogarty International Center, National Institutes of HealthBethesdaUSA

Personalised recommendations