1887

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Volume 104, Issue 10

Evolution and diversity of nucleotide and dinucleotide composition in poxviruses Open Access

Abstract

Poxviruses (family ) have long dsDNA genomes and infect a wide range of hosts, including insects, birds, reptiles and mammals. These viruses have substantial incidence, prevalence and disease burden in humans and in other animals. Nucleotide and dinucleotide composition, mostly CpG and TpA, have been largely studied in viral genomes because of their evolutionary and functional implications. We analysed here the nucleotide and dinucleotide composition, as well as codon usage bias, of a set of representative poxvirus genomes, with a very diverse host spectrum. After correcting for overall nucleotide composition, entomopoxviruses displayed low overall GC content, no enrichment in TpA and large variation in CpG enrichment, while chordopoxviruses showed large variation in nucleotide composition, no obvious depletion in CpG and a weak trend for TpA depletion in GC-rich genomes. Overall, intergenome variation in dinucleotide composition in poxviruses is largely accounted for by variation in overall genomic GC levels. Nonetheless, using vaccinia virus as a model, we found that genes expressed at the earliest times in infection are more CpG-depleted than genes expressed at later stages. This observation has parallels in betahepesviruses (also large dsDNA viruses) and suggests an antiviral role for the innate immune system (e.g. via the zinc-finger antiviral protein ZAP) in the early phases of poxvirus infection. We also analysed codon usage bias in poxviruses and we observed that it is mostly determined by genomic GC content, and that stratification after host taxonomy does not contribute to explaining codon usage bias diversity. By analysis of within-species diversity, we show that genomic GC content is the result of mutational biases. Poxvirus genomes that encode a DNA ligase are significantly AT-richer than those that do not, suggesting that DNA repair systems shape mutation biases. Our data shed light on the evolution of poxviruses and inform strategies for their genetic manipulation for therapeutic purposes.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): codon usage bias , CpG , GC content , nucleotide and dinucleotide composition and poxviruses
Funding
This study was supported by the:
  • European Union's Horizon 2020 research and innovation program (Award CODOVIREVOL (ERC-2014-CoG- 647916))
    • Principle Award Recipient: IgnacioGonzalez Bravo
  • Ministero della Salute (Award Ricerca corrente 2023)
    • Principle Award Recipient: ManuelaSironi
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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References

  1. Gyuranecz M, Foster JT, Dán Á, Ip HS, Egstad KF et al. Worldwide phylogenetic relationship of avian poxviruses. J Virol 2013; 87:4938–4951 [View Article] [PubMed]
     [Google Scholar]
  2. Sarker S, Isberg SR, Moran JL, Araujo RD, Elliott N et al. Crocodilepox virus evolutionary genomics supports observed poxvirus infection dynamics on saltwater crocodile (Crocodylus porosus). Viruses 2019; 11:1116 [View Article] [PubMed]
     [Google Scholar]
  3. Alonso RC, Moura PP, Caldeira DF, Mendes MHAF, Pinto MHB et al. Poxviruses diagnosed in cattle from Distrito Federal, Brazil (2015-2018). Transbound Emerg Dis 2020; 67:1563–1573 [View Article] [PubMed]
     [Google Scholar]
  4. Lefkowitz EJ, Wang C, Upton C. Poxviruses: past, present and future. Virus Res 2006; 117:105–118 [View Article] [PubMed]
     [Google Scholar]
  5. Moss B. Poxvirus DNA replication. Cold Spring Harb Perspect Biol 2013; 5:a010199 [View Article] [PubMed]
     [Google Scholar]
  6. McInnes CJ, Damon IK, Smith GL, McFadden G, Isaacs SN et al. 2023; ICTV Virus Taxonomy Profile: Poxviridae 2023. J Gen Virol 104: Epub ahead of print 31 May 2023 [View Article]
     [Google Scholar]
  7. Fenner F, Henderson DA, Arita I, Jezek Z, Ladnyi ID et al. Smallpox and its eradication / F. Fenner… [et al.]; 1988 https://apps.who.int/iris/handle/10665/39485
  8. Kraemer MUG, Tegally H, Pigott DM, Dasgupta A, Sheldon J et al. Tracking the 2022 monkeypox outbreak with epidemiological data in real-time. Lancet Infect Dis 2022; 22:941–942 [View Article]
     [Google Scholar]
  9. Silva NIO, de Oliveira JS, Kroon EG, Trindade G de S, Drumond BP. Here, there, and everywhere: the wide host range and geographic distribution of zoonotic orthopoxviruses. Viruses 2020; 13:43 [View Article] [PubMed]
     [Google Scholar]
  10. McVey DS. Poxviridae. In McVey DS, Kennedy M, Chengappa MM, Wilkes R. eds Veterinary Microbiology Wiley; 2022 pp 522–532 [View Article]
     [Google Scholar]
  11. Chen X, Anstey AV, Bugert JJ. Molluscum contagiosum virus infection. Lancet Infect Dis 2013; 13:877–888 [View Article] [PubMed]
     [Google Scholar]
  12. Takatsuka J, Nakai M, Shinoda T. A virus carries a gene encoding juvenile hormone acid methyltransferase, a key regulatory enzyme in insect metamorphosis. Sci Rep 2017; 7:13522 [View Article] [PubMed]
     [Google Scholar]
  13. Nakai M, Kinjo H, Takatsuka J, Shiotsuki T, Kamita SG et al. Entomopoxvirus infection induces changes in both juvenile hormone and ecdysteroid levels in larval Mythimna separata. J Gen Virol 2016; 97:225–232 [View Article] [PubMed]
     [Google Scholar]
  14. Palli SR, Ladd TR, Tomkins WL, Shu S, Ramaswamy SB et al. Choristoneura fumiferana entomopoxvirus prevents metamorphosis and modulates juvenile hormone and ecdysteroid titers. Insect Biochem Mol Biol 2000; 30:869–876 [View Article] [PubMed]
     [Google Scholar]
  15. Coffman KA, Hankinson QM, Burke GR. A viral mutualist employs posthatch transmission for vertical and horizontal spread among parasitoid wasps. Proc Natl Acad Sci USA 2022; 119:e2120048119 [View Article] [PubMed]
     [Google Scholar]
  16. Chiu E, Hijnen M, Bunker RD, Boudes M, Rajendran C et al. Structural basis for the enhancement of virulence by viral spindles and their in vivo crystallization. Proc Natl Acad Sci USA 2015; 112:3973–3978 [View Article] [PubMed]
     [Google Scholar]
  17. Woods SA, Streett DA, Henry JE. Temporal patterns of mortality from an entomopoxvirus and strategies for control of the migratory grasshopper (Melanoplus sanguinipes F.). J Invertebr Pathol 1992; 60:33–39 [View Article]
     [Google Scholar]
  18. Hendrickson RC, Wang C, Hatcher EL, Lefkowitz EJ. Orthopoxvirus genome evolution: the role of gene loss. Viruses 2010; 2:1933–1967 [View Article] [PubMed]
     [Google Scholar]
  19. Senkevich TG, Yutin N, Wolf YI, Koonin EV, Moss B. Ancient gene capture and recent gene loss shape the evolution of orthopoxvirus-host interaction genes. mBio 2021; 12:e0149521 [View Article] [PubMed]
     [Google Scholar]
  20. Upton C, Slack S, Hunter AL, Ehlers A, Roper RL. Poxvirus orthologous clusters: toward defining the minimum essential poxvirus genome. J Virol 2003; 77:7590–7600 [View Article] [PubMed]
     [Google Scholar]
  21. Hatcher EL, Hendrickson RC, Lefkowitz EJ. Identification of nucleotide-level changes impacting gene content and genome evolution in orthopoxviruses. J Virol 2014; 88:13651–13668 [View Article] [PubMed]
     [Google Scholar]
  22. Akashi H. Codon bias evolution in Drosophila. Population genetics of mutation-selection drift. Gene 1997; 205:269–278 [View Article]
     [Google Scholar]
  23. Duret L. Evolution of synonymous codon usage in metazoans. Curr Opin Genet Dev 2002; 12:640–649 [View Article] [PubMed]
     [Google Scholar]
  24. Plotkin JB, Kudla G. Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet 2011; 12:32–42 [View Article] [PubMed]
     [Google Scholar]
  25. Mordstein C, Cano L, Morales AC, Young B, Ho AT et al. Transcription, mRNA export, and immune evasion shape the codon usage of viruses. Genome Biol Evol 2021; 13:evab106 [View Article] [PubMed]
     [Google Scholar]
  26. Bulmer M. The selection-mutation-drift theory of synonymous codon usage. Genetics 1991; 129:897–907 [View Article]
     [Google Scholar]
  27. Bahir I, Fromer M, Prat Y, Linial M. Viral adaptation to host: a proteome-based analysis of codon usage and amino acid preferences. Mol Syst Biol 2009; 5:311 [View Article] [PubMed]
     [Google Scholar]
  28. Lucks JB, Nelson DR, Kudla GR, Plotkin JB. Genome landscapes and bacteriophage codon usage. PLoS Comput Biol 2008; 4:e1000001 [View Article] [PubMed]
     [Google Scholar]
  29. Wong EHM, Smith DK, Rabadan R, Peiris M, Poon LLM. Codon usage bias and the evolution of influenza A viruses. Codon Usage Biases of Influenza Virus. BMC Evol Biol 2010; 10:253 [View Article] [PubMed]
     [Google Scholar]
  30. Zhou J, Xing Y, Zhou Z, Wang S. A comprehensive analysis of Usutu virus (USUV) genomes revealed lineage-specific codon usage patterns and host adaptations. Front Microbiol 2023; 13:967999 [View Article]
     [Google Scholar]
  31. Yu C, Li J, Li Q, Chang S, Cao Y et al. Hepatitis B virus (HBV) codon adapts well to the gene expression profile of liver cancer: an evolutionary explanation for HBV’s oncogenic role. J Microbiol 2022; 60:1106–1112 [View Article]
     [Google Scholar]
  32. Qin L, Ding S, Wang Z, Jiang R, He Z. Host plants shape the Codon Usage Pattern of Turnip Mosaic Virus. Viruses 2022; 14:2267 [View Article] [PubMed]
     [Google Scholar]
  33. Kumar N, Kulkarni DD, Lee B, Kaushik R, Bhatia S et al. Evolution of Codon Usage Bias in Henipaviruses is governed by natural selection and is host-specific. Viruses 2018; 10:604 [View Article] [PubMed]
     [Google Scholar]
  34. Wang Q, Lyu X, Cheng J, Fu Y, Lin Y et al. Codon Usage provides insights into the adaptive evolution of Mycoviruses in their associated fungi host. Int J Mol Sci 2022; 23:7441 [View Article] [PubMed]
     [Google Scholar]
  35. Félez-Sánchez M, Trösemeier J-H, Bedhomme S, González-Bravo MI, Kamp C et al. Cancer, Warts, or Asymptomatic infections: clinical presentation matches Codon Usage preferences in human papillomaviruses. Genome Biol Evol 2015; 7:2117–2135 [View Article] [PubMed]
     [Google Scholar]
  36. Chen F, Yang J-R. Distinct codon usage bias evolutionary patterns between weakly and strongly virulent respiratory viruses. iScience 2022; 25:103682 [View Article]
     [Google Scholar]
  37. Lauring AS, Jones JO, Andino R. Rationalizing the development of live attenuated virus vaccines. Nat Biotechnol 2010; 28:573–579 [View Article]
     [Google Scholar]
  38. Le Nouën C, Brock LG, Luongo C, McCarty T, Yang L et al. Attenuation of human respiratory syncytial virus by genome-scale codon-pair deoptimization. Proc Natl Acad Sci USA 2014; 111:13169–13174 [View Article] [PubMed]
     [Google Scholar]
  39. Eschke K, Trimpert J, Osterrieder N, Kunec D, Mocarski E. Attenuation of a very virulent Marek’s disease herpesvirus (MDV) by codon pair bias deoptimization. PLoS Pathog 2018; 14:e1006857 [View Article]
     [Google Scholar]
  40. Cheng BYH, Nogales A, de la Torre JC, Martínez-Sobrido L. Development of live-attenuated arenavirus vaccines based on codon deoptimization of the viral glycoprotein. Virology 2017; 501:35–46 [View Article]
     [Google Scholar]
  41. Martinez MA, Jordan-Paiz A, Franco S, Nevot M. Synonymous virus genome recoding as a tool to impact viral fitness. Trends Microbiol 2016; 24:134–147
     [Google Scholar]
  42. Simón D, Cristina J, Musto H. An overview of dinucleotide and codon usage in all viruses. Arch Virol 2022; 167:1443–1448 [View Article]
     [Google Scholar]
  43. Kunec D, Osterrieder N. Codon pair bias is a direct consequence of dinucleotide bias. Cell Rep 2016; 14:55–67 [View Article] [PubMed]
     [Google Scholar]
  44. Daron J, Bravo IG. Variability in codon usage in coronaviruses is mainly driven by mutational bias and selective constraints on CpG dinucleotide. Viruses 2021; 13:1800 [View Article] [PubMed]
     [Google Scholar]
  45. Cooper DN, Gerber-Huber S. DNA methylation and CpG suppression. Cell Differ 1985; 17:199–205 [View Article] [PubMed]
     [Google Scholar]
  46. Karlin S, Ladunga I, Blaisdell BE. Heterogeneity of genomes: measures and values. Proc Natl Acad Sci USA 1994; 91:12837–12841 [View Article] [PubMed]
     [Google Scholar]
  47. Burge C, Campbell AM, Karlin S. Over- and under-representation of short oligonucleotides in DNA sequences. Proc Natl Acad Sci USA 1992; 89:1358–1362 [View Article]
     [Google Scholar]
  48. Simmen MW. Genome-scale relationships between cytosine methylation and dinucleotide abundances in animals. Genomics 2008; 92:33–40 [View Article]
     [Google Scholar]
  49. Bird AP, Taggart MH. Variable patterns of total DNA and rDNA methylation in animals. Nucl Acids Res 1980; 8:1485–1497 [View Article]
     [Google Scholar]
  50. Gentles AJ, Karlin S. Genome-scale compositional comparisons in eukaryotes. Genome Res 2001; 11:540–546 [View Article] [PubMed]
     [Google Scholar]
  51. Simmonds P, Xia W, Baillie JK, McKinnon K. Modelling mutational and selection pressures on dinucleotides in eukaryotic phyla--selection against CpG and UpA in cytoplasmically expressed RNA and in RNA viruses. BMC Genome 2013; 14:610 [View Article] [PubMed]
     [Google Scholar]
  52. Provataris P, Meusemann K, Niehuis O, Grath S, Misof B. Signatures of DNA methylation across insects suggest reduced DNA methylation levels in holometabola. Genome Biol Evol 2018; 10:1185–1197 [View Article] [PubMed]
     [Google Scholar]
  53. Gonçalves-Carneiro D, Takata MA, Ong H, Shilton A, Bieniasz PD. Origin and evolution of the zinc finger antiviral protein. PLoS Pathog 2021; 17:e1009545 [View Article] [PubMed]
     [Google Scholar]
  54. Beutler E, Gelbart T, Han JH, Koziol JA, Beutler B. Evolution of the genome and the genetic code: selection at the dinucleotide level by methylation and polyribonucleotide cleavage. Proc Natl Acad Sci USA 1989; 86:192–196 [View Article]
     [Google Scholar]
  55. Karlin S, Mrázek J. Compositional differences within and between eukaryotic genomes. Proc Natl Acad Sci USA 1997; 94:10227–10232 [View Article]
     [Google Scholar]
  56. Bauer AP, Leikam D, Krinner S, Notka F, Ludwig C et al. The impact of intragenic CpG content on gene expression. Nucleic Acids Res 2010; 38:3891–3908 [View Article] [PubMed]
     [Google Scholar]
  57. Krinner S, Heitzer AP, Diermeier SD, Obermeier I, Längst G et al. CpG domains downstream of TSSs promote high levels of gene expression. Nucleic Acids Res 2014; 42:3551–3564 [View Article] [PubMed]
     [Google Scholar]
  58. Takata MA, Gonçalves-Carneiro D, Zang TM, Soll SJ, York A et al. CG dinucleotide suppression enables antiviral defence targeting non-self RNA. Nature 2017; 550:124–127 [View Article]
     [Google Scholar]
  59. Luo X, Wang X, Gao Y, Zhu J, Liu S et al. Molecular mechanism of RNA recognition by zinc-finger antiviral protein. Cell Rep 2020; 30:46–52 [View Article] [PubMed]
     [Google Scholar]
  60. Bowie AG, Unterholzner L. Viral evasion and subversion of pattern-recognition receptor signalling. Nat Rev Immunol 2008; 8:911–922 [View Article] [PubMed]
     [Google Scholar]
  61. Goonawardane N, Nguyen D, Simmonds P, Schwemmle M. Association of zinc finger antiviral protein binding to viral genomic RNA with attenuation of replication of echovirus 7. mSphere 2021; 6:e01138-20 [View Article] [PubMed]
     [Google Scholar]
  62. Odon V, Fros JJ, Goonawardane N, Dietrich I, Ibrahim A et al. The role of ZAP and OAS3/RNAseL pathways in the attenuation of an RNA virus with elevated frequencies of CpG and UpA dinucleotides. Nucleic Acids Res 2019; 47:8061–8083 [View Article] [PubMed]
     [Google Scholar]
  63. Ficarelli M, Neil SJD, Swanson CM. Targeted restriction of viral gene expression and replication by the ZAP antiviral system. Annu Rev Virol 2021; 8:265–283 [View Article] [PubMed]
     [Google Scholar]
  64. Ficarelli M, Wilson H, Pedro Galão R, Mazzon M, Antzin-Anduetza I et al. KHNYN is essential for the zinc finger antiviral protein (ZAP) to restrict HIV-1 containing clustered CpG dinucleotides. Elife 2019; 8:e46767 [View Article] [PubMed]
     [Google Scholar]
  65. Miyazato P, Matsuo M, Tan BJY, Tokunaga M, Katsuya H et al. HTLV-1 contains a high CG dinucleotide content and is susceptible to the host antiviral protein ZAP. Retrovirology 2019; 16:38 [View Article] [PubMed]
     [Google Scholar]
  66. Kmiec D, Nchioua R, Sherrill-Mix S, Stürzel CM, Heusinger E et al. CpG Frequency in the 5’ Third of the env Gene Determines Sensitivity of Primary HIV-1 Strains to the Zinc-Finger Antiviral Protein. mBio 2020; 11:e02903-19 [View Article] [PubMed]
     [Google Scholar]
  67. Gonçalves-Carneiro D, Mastrocola E, Lei X, DaSilva J, Chan YF et al. Rational attenuation of RNA viruses with zinc finger antiviral protein. Nat Microbiol 2022; 7:1558–1567 [View Article] [PubMed]
     [Google Scholar]
  68. Cooper DA, Banerjee S, Chakrabarti A, García-Sastre A, Hesselberth JR et al. RNase L targets distinct sites in influenza A virus RNAs. J Virol 2015; 89:2764–2776 [View Article] [PubMed]
     [Google Scholar]
  69. Lin Y-T, Chiweshe S, McCormick D, Raper A, Wickenhagen A et al. Human cytomegalovirus evades ZAP detection by suppressing CpG dinucleotides in the major immediate early 1 gene. PLoS pathogens 2020; 16:e1008844
     [Google Scholar]
  70. Gonzalez-Perez AC, Stempel M, Wyler E, Urban C, Piras A et al. The zinc finger antiviral protein ZAP restricts human cytomegalovirus and selectively binds and Destabilizes viral Ul4/Ul5 transcripts. mBio 2021; 12:e02683-20
     [Google Scholar]
  71. Peng C, Wyatt LS, Glushakow-Smith SG, Lal-Nag M, Weisberg AS et al. Zinc-finger antiviral protein (ZAP) is a restriction factor for replication of modified vaccinia virus Ankara (MVA) in human cells. PLoS Pathog 2020; 16:e1008845 [View Article] [PubMed]
     [Google Scholar]
  72. Burns CC, Campagnoli R, Shaw J, Vincent A, Jorba J et al. Genetic inactivation of poliovirus infectivity by increasing the frequencies of CpG and UpA dinucleotides within and across synonymous capsid region codons. J Virol 2009; 83:9957–9969 [View Article] [PubMed]
     [Google Scholar]
  73. Gaunt E, Wise HM, Zhang H, Lee LN, Atkinson NJ et al. Elevation of CpG frequencies in influenza A genome attenuates pathogenicity but enhances host response to infection. eLife 2016; 5: [View Article]
     [Google Scholar]
  74. Antzin-Anduetza I, Mahiet C, Granger LA, Odendall C, Swanson CM. Increasing the CpG dinucleotide abundance in the HIV-1 genomic RNA inhibits viral replication. Retrovirology 2017; 14:49 [View Article] [PubMed]
     [Google Scholar]
  75. Fros JJ, Dietrich I, Alshaikhahmed K, Passchier TC, Evans DJ et al. CpG and UpA dinucleotides in both coding and non-coding regions of echovirus 7 inhibit replication initiation post-entry. eLife 2017; 6: [View Article]
     [Google Scholar]
  76. Pereira-Gómez M, Carrau L, Fajardo Á, Moreno P, Moratorio G. Altering compositional properties of viral genomes to design live-attenuated vaccines. Front Microbiol 2021; 12:676582 [View Article] [PubMed]
     [Google Scholar]
  77. Lauring AS, Acevedo A, Cooper SB, Andino R. Codon usage determines the mutational robustness, evolutionary capacity, and virulence of an RNA virus. Cell Host Microbe 2012; 12:623–632 [View Article] [PubMed]
     [Google Scholar]
  78. Gigante CM, Gao J, Tang S, McCollum AM, Wilkins K et al. Genome of Alaskapox virus, a novel orthopoxvirus isolated from Alaska. Viruses 2019; 11:708 [View Article]
     [Google Scholar]
  79. Bourret J, Alizon S, Bravo IG. COUSIN (COdon Usage Similarity INdex): a normalized measure of Codon Usage preferences. Genome Biol Evol 2019; 11:3523–3528 [View Article] [PubMed]
     [Google Scholar]
  80. Charif D, Lobry JR. SeqinR 1.0-2: a contributed package to the R project for statistical computing devoted to biological sequences retrieval and analysis. In Bastolla U, Porto M, Roman HE, Vendruscolo M. eds Structural Approaches to Sequence Evolution: Molecules, Networks, Populations Berlin, Heidelberg: Springer; pp 207–232 [View Article]
     [Google Scholar]
  81. Rohart F, Gautier B, Singh A, Lê Cao K-A. mixOmics: an R package for 'omics feature selection and multiple data integration. PLoS Comput Biol 2017; 13:e1005752 [View Article] [PubMed]
     [Google Scholar]
  82. Emms DM, Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol 2019; 20: [View Article]
     [Google Scholar]
  83. Yang Z, Bruno DP, Martens CA, Porcella SF, Moss B. Simultaneous high-resolution analysis of vaccinia virus and host cell transcriptomes by deep RNA sequencing. Proc Natl Acad Sci USA 2010; 107:11513–11518 [View Article] [PubMed]
     [Google Scholar]
  84. Pohlert T. The Pairwise multiple comparison of mean ranks package (PMCMR). R package 20142004–2006
     [Google Scholar]
  85. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
     [Google Scholar]
  86. Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res 2016; 44:W232–5 [View Article] [PubMed]
     [Google Scholar]
  87. Chernomor O, von Haeseler A, Minh BQ. Terrace aware data structure for phylogenomic inference from supermatrices. Syst Biol 2016; 65:997–1008 [View Article] [PubMed]
     [Google Scholar]
  88. Pagel M, Meade A, Barker D. Bayesian estimation of ancestral character states on phylogenies. Syst Biol 2004; 53:673–684 [View Article] [PubMed]
     [Google Scholar]
  89. Garland T, Dickerman AW, Janis CM, Jones JA. Phylogenetic analysis of covariance by computer simulation. Syst Biol 1993; 42:265–292 [View Article]
     [Google Scholar]
  90. Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W. GEIGER: investigating evolutionary radiations. Bioinformatics 2008; 24:129–131 [View Article] [PubMed]
     [Google Scholar]
  91. Revell LJ. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 2012; 3:217–223 [View Article]
     [Google Scholar]
  92. Khabbazian M, Kriebel R, Rohe K, Ané C, Hansen T. Fast and accurate detection of evolutionary shifts in Ornstein–Uhlenbeck models. Methods Ecol Evol 2016; 7:811–824 [View Article]
     [Google Scholar]
  93. Didelot X, Wilson DJ. ClonalFrameML: efficient inference of recombination in whole bacterial genomes. PLoS Comput Biol 2015; 11:e1004041 [View Article] [PubMed]
     [Google Scholar]
  94. Karlin S, Cardon LR. Computational DNA sequence analysis. Annu Rev Microbiol 1994; 48:619–654 [View Article] [PubMed]
     [Google Scholar]
  95. Odon V, Fiddaman SR, Smith AL, Simmonds P. Comparison of CpG- and UpA-mediated restriction of RNA virus replication in mammalian and avian cells and investigation of potential ZAP-mediated shaping of host transcriptome compositions. RNA 2022; 28:1089–1109 [View Article] [PubMed]
     [Google Scholar]
  96. Duret L, Galtier N. The covariation between TpA deficiency, CpG deficiency, and G+C content of human isochores is due to a mathematical artifact. Mol Biol Evol 2000; 17:1620–1625 [View Article] [PubMed]
     [Google Scholar]
  97. Emerson GL, Li Y, Frace MA, Olsen-Rasmussen MA, Khristova ML et al. The phylogenetics and ecology of the orthopoxviruses endemic to North America. PLoS One 2009; 4:e7666 [View Article] [PubMed]
     [Google Scholar]
  98. Simón D, Cristina J, Musto H. Nucleotide composition and Codon usage across viruses and their respective hosts. Front Microbiol 2021; 12:646300 [View Article] [PubMed]
     [Google Scholar]
  99. Pagel M. Inferring the historical patterns of biological evolution. Nature 1999; 401:877–884 [View Article] [PubMed]
     [Google Scholar]
  100. Messer PW. Measuring the rates of spontaneous mutation from deep and large-scale polymorphism data. Genetics 2009; 182:1219–1232 [View Article] [PubMed]
     [Google Scholar]
  101. Hershberg R, Petrov DA. Evidence that mutation is universally biased towards AT in bacteria. PLoS Genet 2010; 6:e1001115 [View Article] [PubMed]
     [Google Scholar]
  102. Gigante CM, Korber B, Seabolt MH, Wilkins K, Davidson W et al. Multiple lineages of monkeypox virus detected in the United States, 2021-2022. Science 2022; 378:560–565 [View Article] [PubMed]
     [Google Scholar]
  103. Isidro J, Borges V, Pinto M, Sobral D, Santos JD et al. Phylogenomic characterization and signs of microevolution in the 2022 multi-country outbreak of monkeypox virus. Nat Med 2022; 28:1569–1572 [View Article] [PubMed]
     [Google Scholar]
  104. O’Toole Á, Neher RA, Ndodo N, Borges V, Gannon B et al. Putative APOBEC3 deaminase editing in MPXV as evidence for sustained human transmission since at least 2016. Evol Biol 2023 [View Article]
     [Google Scholar]
  105. Forni D, Cagliani R, Pozzoli U, Sironi M. An APOBEC3 mutational signature in the genomes of human-infecting orthopoxviruses. mSphere 2023; 8:e0006223 [View Article] [PubMed]
     [Google Scholar]
  106. Damaso CR. Revisiting Jenner’s mysteries, the role of the Beaugency lymph in the evolutionary path of ancient smallpox vaccines. Lancet Infect Dis 2018; 18:e55–e63 [View Article] [PubMed]
     [Google Scholar]
  107. Kerr PJ, Liu J, Cattadori I, Ghedin E, Read AF et al. Myxoma virus and the Leporipoxviruses: an evolutionary paradigm. Viruses 2015; 7:1020–1061 [View Article] [PubMed]
     [Google Scholar]
  108. Sanjuán R, Domingo-Calap P. Mechanisms of viral mutation. Cell Mol Life Sci 2016; 73:4433–4448 [View Article] [PubMed]
     [Google Scholar]
  109. Greseth MD, Traktman P. The life cycle of the vaccinia virus genome. Annu Rev Virol 2022; 9:239–259 [View Article] [PubMed]
     [Google Scholar]
  110. Templeton CW, Traktman P. UV irradiation of vaccinia virus-infected cells impairs cellular functions, introduces lesions into the viral genome, and uncovers repair capabilities for the viral replication machinery. J Virol 2022; 96:e0213721 [View Article] [PubMed]
     [Google Scholar]
  111. Culyba MJ, Minkah N, Hwang Y, Benhamou O-MJ, Bushman FD. DNA branch nuclease activity of vaccinia A22 resolvase. J Biol Chem 2007; 282:34644–34652 [View Article] [PubMed]
     [Google Scholar]
  112. Senkevich TG, Koonin EV, Moss B. Predicted poxvirus FEN1-like nuclease required for homologous recombination, double-strand break repair and full-size genome formation. Proc Natl Acad Sci USA 2009; 106:17921–17926 [View Article] [PubMed]
     [Google Scholar]
  113. Colinas RJ, Goebel SJ, Davis SW, Johnson GP, Norton EK et al. A DNA ligase gene in the copenhagen strain of vaccinia virus is nonessential for viral replication and recombination. Virology 1990; 179:267–275 [View Article]
     [Google Scholar]
  114. Kerr SM, Smith GL. Vaccinia virus DNA ligase is nonessential for virus replication: recovery of plasmids from virus-infected cells. Virology 1991; 180:625–632 [View Article] [PubMed]
     [Google Scholar]
  115. Parks RJ, Winchcombe-Forhan C, DeLange AM, Xing X, Evans DH. DNA ligase gene disruptions can depress viral growth and replication in poxvirus-infected cells. Virus Res 1998; 56:135–147 [View Article] [PubMed]
     [Google Scholar]
  116. Pouyet F, Mouchiroud D, Duret L, Sémon M. Recombination, meiotic expression and human codon usage. Elife 2017; 6: [View Article]
     [Google Scholar]
  117. Melamed-Bessudo C, Shilo S, Levy AA. Meiotic recombination and genome evolution in plants. Curr Opin Plant Biol 2016; 30:82–87 [View Article] [PubMed]
     [Google Scholar]
  118. Lassalle F, Périan S, Bataillon T, Nesme X, Duret L et al. GC-content evolution in bacterial genomes: the biased gene conversion hypothesis expands. PLoS Genet 2015; 11:e1004941 [View Article] [PubMed]
     [Google Scholar]
  119. Figuet E, Ballenghien M, Romiguier J, Galtier N. Biased gene conversion and GC-content evolution in the coding sequences of reptiles and vertebrates. Genome Biol Evol 2014; 7:240–250 [View Article] [PubMed]
     [Google Scholar]
  120. Karlin S, Burge C. Dinucleotide relative abundance extremes: a genomic signature. Trends Genet 1995; 11:283–290 [View Article] [PubMed]
     [Google Scholar]
  121. Hershberg R, Petrov DA, Nachman MW. General rules for optimal codon choice. PLoS Genet 2009; 5:e1000556 [View Article] [PubMed]
     [Google Scholar]
  122. de Jong MJ, van Oosterhout C, Hoelzel AR, Janke A. Moderating the neutralist-selectionist debate: exactly which propositions are we debating, and which arguments are valid?. Biol Rev Camb Philos Soc 2023 [View Article] [PubMed]
     [Google Scholar]
  123. Picard MAL, Leblay F, Cassan C, Willemsen A, Daron J et al. Transcriptomic, proteomic, and functional consequences of codon usage bias in human cells during heterologous gene expression. Protein Sci 2023; 32:e4576 [View Article] [PubMed]
     [Google Scholar]
  124. Li M, Kao E, Gao X, Sandig H, Limmer K et al. Codon-usage-based inhibition of HIV protein synthesis by human schlafen 11. Nature 2012; 491:125–128 [View Article]
     [Google Scholar]
  125. Stabell AC, Hawkins J, Li M, Gao X, David M et al. Non-human primate schlafen11 inhibits production of both host and viral proteins. PLoS Pathog 2016; 12:e1006066 [View Article] [PubMed]
     [Google Scholar]
  126. Greenbaum BD, Levine AJ, Bhanot G, Rabadan R. Patterns of evolution and host gene mimicry in influenza and other RNA viruses. PLoS Pathog 2008; 4:e1000079 [View Article] [PubMed]
     [Google Scholar]
  127. Tulloch F, Atkinson NJ, Evans DJ, Ryan MD, Simmonds P. RNA virus attenuation by codon pair deoptimisation is an artefact of increases in CpG/UpA dinucleotide frequencies. Elife 2014; 3:e04531 [View Article] [PubMed]
     [Google Scholar]
  128. Di Giallonardo F, Schlub TE, Shi M, Holmes EC. Dinucleotide composition in animal RNA viruses is shaped more by virus family than by host species. J Virol 2017; 91:e02381-16 [View Article] [PubMed]
     [Google Scholar]
  129. Upadhyay M, Vivekanandan P, Burk RD. Depletion of CpG dinucleotides in papillomaviruses and polyomaviruses: a role for divergent evolutionary pressures. PLoS One 2015; 10:e0142368 [View Article] [PubMed]
     [Google Scholar]
  130. King K, Larsen BB, Gryseels S, Richet C, Kraberger S et al. Coevolutionary analysis implicates toll-like receptor 9 in papillomavirus restriction. mBio 2022; 13:e0005422 [View Article] [PubMed]
     [Google Scholar]
  131. White MK, Safak M, Khalili K. Regulation of gene expression in primate polyomaviruses. J Virol 2009; 83:10846–10856 [View Article] [PubMed]
     [Google Scholar]
  132. Lin Y-T, Chau L-F, Coutts H, Mahmoudi M, Drampa V et al. Does the zinc finger antiviral protein (ZAP) shape the evolution of herpesvirus genomes?. Viruses 2021; 13:1857 [View Article] [PubMed]
     [Google Scholar]
  133. Kerr SM, Johnston LH, Odell M, Duncan SA, Law KM et al. Vaccinia DNA ligase complements Saccharomyces cerevisiae cdc9, localizes in cytoplasmic factories and affects virulence and virus sensitivity to DNA damaging agents. EMBO J 1991; 10:4343–4350 [View Article] [PubMed]
     [Google Scholar]
  134. Teng W, Liao B, Chen M, Shu W, Faucher SP. Genomic legacies of ancient adaptation illuminate GC-content evolution in bacteria. Microbiol Spectr 2023; 11:e0214522 [View Article] [PubMed]
     [Google Scholar]
  135. Lind PA, Andersson DI. Whole-genome mutational biases in bacteria. Proc Natl Acad Sci USA 2008; 105:17878–17883 [View Article]
     [Google Scholar]
  136. Weissman JL, Fagan WF, Johnson PLF. Linking high GC content to the repair of double strand breaks in prokaryotic genomes. PLoS Genet 2019; 15:e1008493 [View Article] [PubMed]
     [Google Scholar]
  137. Luteijn RD, Drexler I, Smith GL, Lebbink RJ, Wiertz EJHJ. Mutagenic repair of double-stranded DNA breaks in vaccinia virus genomes requires cellular DNA ligase IV activity in the cytosol. J Gen Virol 2018; 99:790–804 [View Article]
     [Google Scholar]
  138. Paran N, De Silva FS, Senkevich TG, Moss B. Cellular DNA ligase I is recruited to cytoplasmic vaccinia virus factories and masks the role of the vaccinia ligase in viral DNA replication. Cell Host Microbe 2009; 6:563–569 [View Article] [PubMed]
     [Google Scholar]
  139. Delamonica B, Davalos L, Larijani M, Anthony SJ, Liu J et al. Evolutionary potential of the monkeypox genome arising from interactions with human APOBEC3 enzymes. Virus Evol 2023; 9:vead047 [View Article] [PubMed]
     [Google Scholar]
  140. Molteni C, Forni D, Cagliani R, Arrigoni F, Pozzoli U et al. Selective events at individual sites underlie the evolution of monkeypox virus clades. Virus Evol 2023; 9: [View Article]
     [Google Scholar]
  141. Molteni C, Forni D, Cagliani R, Mozzi A, Clerici M et al. Evolution of the orthopoxvirus core genome. Virus Res 2022; 323:198975 [View Article] [PubMed]
     [Google Scholar]
  142. Zhao G, Droit L, Tesh RB, Popov VL, Little NS et al. The genome of Yoka poxvirus. J Virol 2011; 85:10230–10238 [View Article] [PubMed]
     [Google Scholar]
  143. Gruber CEM, Giombini E, Selleri M, Tausch SH, Andrusch A et al. Whole genome characterization of Orthopoxvirus (OPV) abatino, a zoonotic virus representing a putative novel clade of old world Orthopoxviruses. Viruses 2018; 10:546 [View Article] [PubMed]
     [Google Scholar]
  144. Esparza J, Schrick L, Damaso CR, Nitsche A. Equination (inoculation of horsepox): an early alternative to vaccination (inoculation of cowpox) and the potential role of horsepox virus in the origin of the smallpox vaccine. Vaccine 2017; 35:7222–7230 [View Article] [PubMed]
     [Google Scholar]
  145. Forni D, Cagliani R, Molteni C, Clerici M, Sironi M. Monkeypox virus: the changing facets of a zoonotic pathogen. Infect Genet Evol 2022; 105:105372 [View Article] [PubMed]
     [Google Scholar]
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Evolution and diversity of nucleotide and dinucleotide composition in poxviruses
J. Gen. Virol. 104, 001897 (2023); https://doi.org/10.1099/jgv.0.001897
/content/journal/jgv/10.1099/jgv.0.001897
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