Deciphering the Origin and Evolution of Hepatitis B Viruses by Means of a Family of Non-enveloped Fish Viruses

Cell Host and Microbe

Volumn 22, Issue 3, 2017, Pages 387-399.e6

  Lauber, Chris ^a   Seitz, Stefan ^b   Mattei, Simone ^c   Suh, Alexander ^d   Beck, Jürgen ^e   Herstein, Jennifer ^f   Börold, Jacob ^b   Salzburger, Walter ^g   Kaderali, Lars ^a,h   Briggs, John A G ^c   Bartenschlager, Ralf ^b,i  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d UPPSALA UNIVERSITY   (Sweden)

^e UNIVERSITY OF FREIBURG   (Germany)

^f UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^g UNIVERSITY OF BASEL   (Switzerland)

^h UNIVERSITY MEDICINE GREIFSWALD   (Germany)

ⁱ GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

hepadnaviruses; hepatitis B virus; overlapping open reading frames; viral gene evolution; virus discovery; virus origins; virus host long term co evolution

Indexed keywords

ENVELOPE PROTEIN; VIRUS ENVELOPE PROTEIN;

ARTICLE; ENVELOPE GENE; GEOLOGICAL TIME; HEPADNAVIRIDAE; HEPATITIS B VIRUS; MOLECULAR EVOLUTION; NACKEDNAVIRUS; NONHUMAN; OPEN READING FRAME; OVERLAPPING GENE; PHYLOGENY; PRIORITY JOURNAL; TELEOST; ULTRASTRUCTURE; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS REPLICATION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CLASSIFICATION; FISH; FISH DISEASE; GENETICS; HEPATITIS B; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; SEQUENCE ALIGNMENT; VIROLOGY; VIRUS GENOME;

AMINO ACID SEQUENCE; ANIMALS; CAPSID; EVOLUTION, MOLECULAR; FISH DISEASES; FISHES; GENOME, VIRAL; HEPADNAVIRIDAE; HEPATITIS B; HEPATITIS B VIRUS; HUMANS; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE ALIGNMENT; VIRAL ENVELOPE PROTEINS;

EID: 85028503322     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2017.07.019     Document Type: Article

References (93)

1. Abascal, F., Zardoya, R., Posada, D., ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21 (2005), 2104–2105.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J., Basic local alignment search tool. J. Mol. Biol. 215 (1990), 403–410.
3. Andrews, S. (2010). FastQC. A quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc.
4. Baele, G., Lemey, P., Bedford, T., Rambaut, A., Suchard, M.A., Alekseyenko, A.V., Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol. Biol. Evol. 29 (2012), 2157–2167.
5. Baldo, L., Santos, M.E., Salzburger, W., Comparative transcriptomics of Eastern African cichlid fishes shows signs of positive selection and a large contribution of untranslated regions to genetic diversity. Genome Biol. Evol. 3 (2011), 443–455.
6. Bankevich, A., Nurk, S., Antipov, D., Gurevich, A.A., Dvorkin, M., Kulikov, A.S., Lesin, V.M., Nikolenko, S.I., Pham, S., Prjibelski, A.D., et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19 (2012), 455–477.
7. Bardens, A., Döring, T., Stieler, J., Prange, R., Alix regulates egress of hepatitis B virus naked capsid particles in an ESCRT-independent manner. Cell Microbiol. 13 (2011), 602–619.
8. Bartenschlager, R., Schaller, H., The amino-terminal domain of the hepadnaviral P-gene encodes the terminal protein (genome-linked protein) believed to prime reverse transcription. EMBO J. 7 (1988), 4185–4192.
9. Beck, J., Nassal, M., Hepatitis B virus replication. World J. Gastroenterol. 13 (2007), 48–64.
10. Begun, D.R., Planet of the apes. Sci. Am. 289 (2003), 74–83.
11. Betancur, R., Broughton, R.E., Wiley, E.O., Carpenter, K., Lopez, J.A., Li, C., Holcroft, N.I., Arcila, D., Sanciangco, M., Cureton Ii, J.C., et al. The tree of life and a new classification of bony fishes. PLoS Curr., 5, 2013, 10.1371/currents.tol.53ba26640df0ccaee75bb165c8c26288.
12. Bininda-Emonds, O.R., Cardillo, M., Jones, K.E., MacPhee, R.D., Beck, R.M., Grenyer, R., Price, S.A., Vos, R.A., Gittleman, J.L., Purvis, A., The delayed rise of present-day mammals. Nature 446 (2007), 507–512.
13. Castoe, T.A., Gu, W., de Koning, A.P., Daza, J.M., Jiang, Z.J., Parkinson, C.L., Pollock, D.D., Dynamic nucleotide mutation gradients and control region usage in squamate reptile mitochondrial genomes. Cytogenet. Genome Res. 127 (2009), 112–127.
14. Chauhan, R., Churchill, N.D., Mulrooney-Cousins, P.M., Michalak, T.I., Initial sites of hepadnavirus integration into host genome in human hepatocytes and in the woodchuck model of hepatitis B-associated hepatocellular carcinoma. Oncogenesis, 6, 2017, e317.
15. Chirico, N., Vianelli, A., Belshaw, R., Why genes overlap in viruses. Proc. Biol. Sci. 277 (2010), 3809–3817.
16. Claramunt, S., Cracraft, J., A new time tree reveals Earth history's imprint on the evolution of modern birds. Sci. Adv., 1, 2015, e1501005.
17. Conow, C., Fielder, D., Ovadia, Y., Libeskind-Hadas, R., Jane: a new tool for the cophylogeny reconstruction problem. Algorithms. Mol. Biol., 5, 2010, 16.
18. Crowther, R.A., Kiselev, N.A., Bottcher, B., Berriman, J.A., Borisova, G.P., Ose, V., Pumpens, P., Three-dimensional structure of hepatitis B virus core particles determined by electron cryomicroscopy. Cell 77 (1994), 943–950.
19. Dill, J.A., Camus, A.C., Leary, J.H., Di, G.F., Holmes, E.C., Ng, T.F., Distinct viral lineages from fish and amphibians reveal the complex evolutionary history of hepadnaviruses. J. Virol. 90 (2016), 7920–7933.
20. Drexler, J.F., Geipel, A., König, A., Corman, V.M., van Riel, D., Leijten, L.M., Bremer, C.M., Rasche, A., Cottontail, V.M., Maganga, G.D., et al. Bats carry pathogenic hepadnaviruses antigenically related to hepatitis B virus and capable of infecting human hepatocytes. Proc. Natl. Acad. Sci. USA 110 (2013), 16151–16156.
21. Drozdetskiy, A., Cole, C., Procter, J., Barton, G.J., JPred4: a protein secondary structure prediction server. Nucleic Acids Res. 43 (2015), W389–W394.
22. Drummond, A.J., Ho, S.Y., Phillips, M.J., Rambaut, A., Relaxed phylogenetics and dating with confidence. PLoS Biol., 4, 2006, e88.
23. Drummond, A.J., Suchard, M.A., Xie, D., Rambaut, A., Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29 (2012), 1969–1973.
24. Edgar, R.C., MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32 (2004), 1792–1797.
25. Feschotte, C., Gilbert, C., Endogenous viruses: insights into viral evolution and impact on host biology. Nat. Rev. Genet. 13 (2012), 283–296.
26. Geoghegan, J.L., Duchene, S., Holmes, E.C., Comparative analysis estimates the relative frequencies of co-divergence and cross-species transmission within viral families. PLoS Pathog., 13, 2017, e1006215.
27. Gilbert, C., Feschotte, C., Genomic fossils calibrate the long-term evolution of hepadnaviruses. PLoS Biol., 8, 2010, 10.1371/journal.pbio.1000495.
28. Gilbert, C., Meik, J.M., Dashevsky, D., Card, D.C., Castoe, T.A., Schaack, S., Endogenous hepadnaviruses, bornaviruses and circoviruses in snakes. Proc. Biol. Sci., 281, 2014, 20141122.
29. Glebe, D., Urban, S., Viral and cellular determinants involved in hepadnaviral entry. World J. Gastroenterol. 13 (2007), 22–38.
30. Godoy, B.A., Alvarado-Mora, M.V., Gomes-Gouvea, M.S., Pinho, J.R., Fagundes, N. Jr., Origin of HBV and its arrival in the Americas—the importance of natural selection on time estimates. Antivir. Ther. 18 (2013), 505–512.
31. Gouy, M., Guindon, S., Gascuel, O., SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 27 (2010), 221–224.
32. Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W., Gascuel, O., New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59 (2010), 307–321.
33. Hahn, C.M., Iwanowicz, L.R., Cornman, R.S., Conway, C.M., Winton, J.R., Blazer, V.S., Characterization of a novel hepadnavirus in the white sucker (Catostomus commersonii) from the Great Lakes Region of the United States. J. Virol. 89 (2015), 11801–11811.
34. Hedges, S.B., Marin, J., Suleski, M., Paymer, M., Kumar, S., Tree of life reveals clock-like speciation and diversification. Mol. Biol. Evol. 32 (2015), 835–845.
35. Hong, M., Sandalova, E., Low, D., Gehring, A.J., Fieni, S., Amadei, B., Urbani, S., Chong, Y.S., Guccione, E., Bertoletti, A., Trained immunity in newborn infants of HBV-infected mothers. Nat. Commun., 6, 2015, 6588.
36. Jarvis, E.D., Mirarab, S., Aberer, A.J., Li, B., Houde, P., Li, C., Ho, S.Y., Faircloth, B.C., Nabholz, B., Howard, J.T., et al. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346 (2014), 1320–1331.
37. Jones, D.T., Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 292 (1999), 195–202.
38. Keese, P.K., Gibbs, A., Origins of genes: “big bang” or continuous creation?. Proc. Natl. Acad. Sci. USA 89 (1992), 9489–9493.
39. Kim, F.J., Battini, J.L., Manel, N., Sitbon, M., Emergence of vertebrate retroviruses and envelope capture. Virology 318 (2004), 183–191.
40. Koonin, E.V., Gorbalenya, A.E., Evolution of RNA genomes: does the high mutation rate necessitate high rate of evolution of viral proteins?. J. Mol. Evol. 28 (1989), 524–527.
41. Kyriazi, P., Kornilios, P., Nagy, Z.T., Poulakakis, N., Kumlutaş, Y., Ilgaz, Ç., Avcı, A., Göçmen, B., Lymberakis, P., Comparative phylogeography reveals distinct colonization patterns of Cretan snakes. J. Biogeogr. 40 (2013), 1143–1155.
42. Legendre, P., Desdevises, Y., Bazin, E., A statistical test for host-parasite coevolution. Syst. Biol. 51 (2002), 217–234.
43. Lin, Y.Y., Liu, C., Chien, W.H., Wu, L.L., Tao, Y., Wu, D., Lu, X., Hsieh, C.H., Chen, P.J., Wang, H.Y., et al. New insights into the evolutionary rate of hepatitis B virus at different biological scales. J. Virol. 89 (2015), 3512–3522.
44. Littlejohn, M., Locarnini, S., Yuen, L., Origins and evolution of hepatitis B virus and hepatitis D virus. Cold Spring Harb. Perspect. Med., 6, 2016, a021360.
45. Liu, W., Pan, S., Yang, H., Bai, W., Shen, Z., Liu, J., Xie, Y., The first full-length endogenous hepadnaviruses: identification and analysis. J. Virol. 86 (2012), 9510–9513.
46. Malik, H.S., Henikoff, S., Eickbush, T.H., Poised for contagion: evolutionary origins of the infectious abilities of invertebrate retroviruses. Genome Res. 10 (2000), 1307–1318.
47. Martin, M., Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17 (2011), 10–12.
48. Mason, W.S., Gill, U.S., Litwin, S., Zhou, Y., Peri, S., Pop, O., Hong, M.L., Naik, S., Quaglia, A., Bertoletti, A., Kennedy, P.T., HBV DNA integration and clonal hepatocyte expansion in chronic hepatitis B patients considered immune tolerant. Gastroenterology 151 (2016), 986–998.
49. Mindell, J.A., Grigorieff, N., Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142 (2003), 334–347.
50. Mizokami, M., Orito, E., Molecular evolution of hepatitis viruses. Intervirology 42 (1999), 159–165.
51. Nassal, M., Hepatitis B viruses: reverse transcription a different way. Virus Res. 134 (2008), 235–249.
52. Nguyen, D.H., Ludgate, L., Hu, J., Hepatitis B virus-cell interactions and pathogenesis. J. Cell Physiol. 216 (2008), 289–294.
53. Ni, Y., Sonnabend, J., Seitz, S., Urban, S., The pre-s2 domain of the hepatitis B virus is dispensable for infectivity but serves a spacer function for L-protein-connected virus assembly. J. Virol. 84 (2010), 3879–3888.
54. Orito, E., Mizokami, M., Ina, Y., Moriyama, E.N., Kameshima, N., Yamamoto, M., Gojobori, T., Host-independent evolution and a genetic classification of the hepadnavirus family based on nucleotide sequences. Proc. Natl. Acad. Sci. USA 86 (1989), 7059–7062.
55. Patel, M.R., Emerman, M., Malik, H.S., Paleovirology—ghosts and gifts of viruses past. Curr. Opin. Virol. 1 (2011), 304–309.
56. Pavesi, A., Different patterns of codon usage in the overlapping polymerase and surface genes of hepatitis B virus suggest a de novo origin by modular evolution. J. Gen. Virol. 96 (2015), 3577–3586.
57. Pavesi, A., Magiorkinis, G., Karlin, D.G., Viral proteins originated de novo by overprinting can be identified by codon usage: application to the “gene nursery” of Deltaretroviruses. PLoS Comput. Biol., 9, 2013, e1003162.
58. Prum, R.O., Berv, J.S., Dornburg, A., Field, D.J., Townsend, J.P., Lemmon, E.M., Lemmon, A.R., A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526 (2015), 569–573.
59. Pyron, R.A., Burbrink, F.T., Extinction, ecological opportunity, and the origins of global snake diversity. Evolution 66 (2012), 163–178.
60. Rambaut, A. (2016). FigTree. http://tree.bio.ed.ac.uk/software/figtree.
61. Rambaut, A., Suchard, M.A., and Drummond, A.J. (2016a). Tracer. http://tree.bio.ed.ac.uk/software/tracer.
62. Rambaut, A., Lam, T.T., Max, C.L., Pybus, O.G., Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol., 2, 2016, vew007.
63. Rancurel, C., Khosravi, M., Dunker, A.K., Romero, P.R., Karlin, D., Overlapping genes produce proteins with unusual sequence properties and offer insight into de novo protein creation. J. Virol. 83 (2009), 10719–10736.
64. Ranwez, V., Harispe, S., Delsuc, F., Douzery, E.J., MACSE: multiple alignment of coding SEquences accounting for frameshifts and stop codons. PLoS One, 6, 2011, e22594.
65. Remmert, M., Biegert, A., Hauser, A., Soding, J., HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment. Nat. Methods 9 (2012), 173–175.
66. Schaefer, S., Hepatitis B virus taxonomy and hepatitis B virus genotypes. World J. Gastroenterol. 13 (2007), 14–21.
67. Scheres, S.H., RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180 (2012), 519–530.
68. Seeger, C., Mason, W.S., Hepatitis B virus biology. Microbiol. Mol. Biol. Rev. 64 (2000), 51–68.
69. Sharp, P.M., Simmonds, P., Evaluating the evidence for virus/host co-evolution. Curr. Opin. Virol. 1 (2011), 436–441.
70. Simpson, J.T., Wong, K., Jackman, S.D., Schein, J.E., Jones, S.J., Birol, I., ABySS: a parallel assembler for short read sequence data. Genome Res. 19 (2009), 1117–1123.
71. Springer, M.S., Meredith, R.W., Gatesy, J., Emerling, C.A., Park, J., Rabosky, D.L., Stadler, T., Steiner, C., Ryder, O.A., Janecka, J.E., et al. Macroevolutionary dynamics and historical biogeography of primate diversification inferred from a species supermatrix. PLoS One, 7, 2012, e49521.
72. Stevens, N.J., Seiffert, E.R., O'Connor, P.M., Roberts, E.M., Schmitz, M.D., Krause, C., Gorscak, E., Ngasala, S., Hieronymus, T.L., Temu, J., Palaeontological evidence for an Oligocene divergence between Old World monkeys and apes. Nature 497 (2013), 611–614.
73. Suh, A., Brosius, J., Schmitz, J., Kriegs, J.O., The genome of a Mesozoic paleovirus reveals the evolution of hepatitis B viruses. Nat. Commun., 4, 2013, 1791.
74. Suh, A., Weber, C.C., Kehlmaier, C., Braun, E.L., Green, R.E., Fritz, U., Ray, D.A., Ellegren, H., Early mesozoic coexistence of amniotes and Hepadnaviridae. PLoS Genet., 10, 2014, e1004559.
75. Sung, W.K., Zheng, H., Li, S., Chen, R., Liu, X., Li, Y., Lee, N.P., Lee, W.H., Ariyaratne, P.N., Tennakoon, C., et al. Genome-wide survey of recurrent HBV integration in hepatocellular carcinoma. Nat. Genet. 44 (2012), 765–769.
76. Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30 (2013), 2725–2729.
77. Tang, G., Peng, L., Baldwin, P.R., Mann, D.S., Jiang, W., Rees, I., Ludtke, S.J., EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157 (2007), 38–46.
78. The Timetree of Life. (2016); http://www.timetree.org/.
79. van Heel, M., Harauz, G., Orlova, E.V., Schmidt, R., Schatz, M., A new generation of the IMAGIC image processing system. J. Struct. Biol. 116 (1996), 17–24.
80. van Hemert, F.J., van de Klundert, M.A., Lukashov, V.V., Kootstra, N.A., Berkhout, B., Zaaijer, H.L., Protein X of hepatitis B virus: origin and structure similarity with the central domain of DNA glycosylase. PLoS One, 6, 2011, e23392.
81. van Tuinen, M., Torres, C.R., Potential for bias and low precision in molecular divergence time estimation of the Canopy of Life: an example from aquatic bird families. Front. Genet., 6, 2015, 203.
82. Vogel, M., Vorreiter, J., Nassal, M., Quaternary structure is critical for protein display on capsid-like particles (CLPs): efficient generation of hepatitis B virus CLPs presenting monomeric but not dimeric and tetrameric fluorescent proteins. Proteins 58 (2005), 478–488.
83. Wang, Z., Pascual-Anaya, J., Zadissa, A., Li, W., Niimura, Y., Huang, Z., Li, C., White, S., Xiong, Z., Fang, D., et al. The draft genomes of soft-shell turtle and green sea turtle yield insights into the development and evolution of the turtle-specific body plan. Nat. Genet. 45 (2013), 701–706.
84. Waterhouse, A.M., Procter, J.B., Martin, D.M., Clamp, M., Barton, G.J., Jalview version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25 (2009), 1189–1191.
85. Weber, M., Bronsema, V., Bartos, H., Bosserhoff, A., Bartenschlager, R., Schaller, H., Hepadnavirus P protein utilizes a tyrosine residue in the TP domain to prime reverse transcription. J. Virol. 68 (1994), 2994–2999.
86. WHO. (2017). Hepatitis B. http://www.who.int/mediacentre/factsheets/fs204/en/.
87. Wynne, S.A., Crowther, R.A., Leslie, A.G., The crystal structure of the human hepatitis B virus capsid. Mol. Cell 3 (1999), 771–780.
88. Yang, J.D., Roberts, L.R., Hepatocellular carcinoma: a global view. Nat. Rev. Gastroenterol. Hepatol. 7 (2010), 448–458.
89. Yu, X., Jin, L., Jih, J., Shih, C., Zhou, Z.H., 3.5A cryoEM structure of hepatitis B virus core assembled from full-length core protein. PLoS One, 8, 2013, e69729.
90. Zaaijer, H.L., van Hemert, F.J., Koppelman, M.H., Lukashov, V.V., Independent evolution of overlapping polymerase and surface protein genes of hepatitis B virus. J. Gen. Virol. 88 (2007), 2137–2143.
91. Zehender, G., Ebranati, E., Gabanelli, E., Sorrentino, C., Lo, P.A., Tanzi, E., Ciccozzi, M., Galli, M., Enigmatic origin of hepatitis B virus: an ancient travelling companion or a recent encounter?. World J. Gastroenterol. 20 (2014), 7622–7634.
92. Zhang, G., Li, C., Li, Q., Li, B., Larkin, D.M., Lee, C., Storz, J.F., Antunes, A., Greenwold, M.J., Meredith, R.W., et al. Comparative genomics reveals insights into avian genome evolution and adaptation. Science 346 (2014), 1311–1320.
93. Zheng, Y., Wiens, J.J., Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species. Mol. Phylogenet. Evol. 94 (2016), 537–547.