1932

Abstract

The arrival of novel sequencing technologies throughout the past two decades has led to a paradigm shift in our understanding of herpesvirus genomic diversity. Previously, herpesviruses were seen as a family of DNA viruses with low genomic diversity. However, a growing body of evidence now suggests that herpesviruses exist as dynamic populations that possess standing variation and evolve at much faster rates than previously assumed. In this review, we explore how strategies such as deep sequencing, long-read sequencing, and haplotype reconstruction are allowing scientists to dissect the genomic composition of herpesvirus populations. We also discuss the challenges that need to be addressed before a detailed picture of herpesvirus diversity can emerge.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-100422-010336
2024-09-26
2025-04-29
Loading full text...

Full text loading...

/deliver/fulltext/virology/11/1/annurev-virology-100422-010336.html?itemId=/content/journals/10.1146/annurev-virology-100422-010336&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Davison AJ. 2010.. Herpesvirus systematics. . Vet. Microbiol. 143:(1):5269
    [Crossref] [Google Scholar]
  2. 2.
    Cohen JI. 2020.. Herpesvirus latency. . J. Clin. Investig. 130:(7):336169
    [Crossref] [Google Scholar]
  3. 3.
    Davison AJ. 2007.. Comparative analysis of the genomes. . In Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis, ed. AM Arvin, G Campadelli-Fiume, E Mocarski, PS Moore, B Roizman, et al. , pp. 1026. Cambridge, UK:: Cambridge Univ. Press
    [Google Scholar]
  4. 4.
    Krug LT, Pellett PE. 2021.. The family Herpesviridae: a brief introduction. . In Fields Virology: DNA Viruses, ed. PM Howley, DM Knipe, LT Krug, PE Pellett , pp. 21234. Philadelphia:: Wolters Kluwer. , 7th ed..
    [Google Scholar]
  5. 5.
    Wong Y, Meehan MT, Burrows SR, Doolan DL, Miles JJ. 2022.. Estimating the global burden of Epstein–Barr virus-related cancers. . J. Cancer Res. Clin. Oncol. 148:(1):3146
    [Crossref] [Google Scholar]
  6. 6.
    James C, Harfouche M, Welton NJ, Turner KM, Abu-Raddad LJ, et al. 2020.. Herpes simplex virus: global infection prevalence and incidence estimates. , 2016.. Bull. World Health Organ. 98:(5):31529
    [Crossref] [Google Scholar]
  7. 7.
    Zuhair M, Smit GSA, Wallis G, Jabbar F, Smith C, et al. 2019.. Estimation of the worldwide seroprevalence of cytomegalovirus: a systematic review and meta-analysis. . Rev. Med. Virol. 29:(3):e2034
    [Crossref] [Google Scholar]
  8. 8.
    Arvin AM, Gershon AA. 1996.. Live attenuated varicella vaccine. . Annu. Rev. Microbiol. 50::59100
    [Crossref] [Google Scholar]
  9. 9.
    Gabutti G, Bolognesi N, Sandri F, Florescu C, Stefanati A. 2019.. Varicella zoster virus vaccines: an update. . ImmunoTargets Ther. 8::1528
    [Crossref] [Google Scholar]
  10. 10.
    Alfoldi J, Lindblad-Toh K. 2013.. Comparative genomics as a tool to understand evolution and disease. . Genome Res. 23:(7):106368
    [Crossref] [Google Scholar]
  11. 11.
    Wilkinson GWG, Davison AJ, Tomasec P, Fielding CA, Aicheler R, et al. 2015.. Human cytomegalovirus: taking the strain. . Med. Microbiol. Immunol. 204:(3):27384
    [Crossref] [Google Scholar]
  12. 12.
    Renner DW, Szpara ML. 2018.. The impacts of genome-wide analyses on our understanding of human herpesvirus diversity and evolution. . J. Virol. 92:(1):e00908-17
    [Crossref] [Google Scholar]
  13. 13.
    Houldcroft CJ. 2019.. Human herpesvirus sequencing in the genomic era: the growing ranks of the herpetic legion. . Pathogens 8:(4):186
    [Crossref] [Google Scholar]
  14. 14.
    Sanjuán R, Nebot MR, Chirico N, Mansky LM, Belshaw R. 2010.. Viral mutation rates. . J. Virol. 84:(19):973348
    [Crossref] [Google Scholar]
  15. 15.
    Lauring AS. 2020.. Within-host viral diversity: a window into viral evolution. . Annu. Rev. Virol. 7::6381
    [Crossref] [Google Scholar]
  16. 16.
    Tyler SD, Peters GA, Grose C, Severini A, Gray MJ, et al. 2007.. Genomic cartography of varicella-zoster virus: a complete genome-based analysis of strain variability with implications for attenuation and phenotypic differences. . Virology 359:(2):44758
    [Crossref] [Google Scholar]
  17. 17.
    Renzette N, Gibson L, Bhattacharjee B, Fisher D, Schleiss MR, et al. 2013.. Rapid intrahost evolution of human cytomegalovirus is shaped by demography and positive selection. . PLOS Genet. 9:(9):e1003735
    [Crossref] [Google Scholar]
  18. 18.
    Szpara ML, Gatherer D, Ochoa A, Greenbaum B, Dolan A, et al. 2014.. Evolution and diversity in human herpes simplex virus genomes. . J. Virol. 88:(2):120927
    [Crossref] [Google Scholar]
  19. 19.
    Palser AL, Grayson NE, White RE, Corton C, Correia S, et al. 2015.. Genome diversity of Epstein-Barr virus from multiple tumor types and normal infection. . J. Virol. 89:(10):522237
    [Crossref] [Google Scholar]
  20. 20.
    Bryant NA, Wilkie GS, Russell CA, Compston L, Grafham D, et al. 2018.. Genetic diversity of equine herpesvirus 1 isolated from neurological, abortigenic and respiratory disease outbreaks. . Transbound. Emerg. Dis. 65:(3):81732
    [Crossref] [Google Scholar]
  21. 21.
    Sanjuán R, Domingo-Calap P. 2016.. Mechanisms of viral mutation. . Cell. Mol. Life Sci. 73:(23):443348
    [Crossref] [Google Scholar]
  22. 22.
    Peck KM, Lauring AS. 2018.. Complexities of viral mutation rates. . J. Virol. 92:(14):e01031-17
    [Crossref] [Google Scholar]
  23. 23.
    Hall JD, Almy RE. 1982.. Evidence for control of herpes simplex virus mutagenesis by the viral DNA polymerase. . Virology 116:(2):53543
    [Crossref] [Google Scholar]
  24. 24.
    Drake JW, Hwang CBC. 2005.. On the mutation rate of herpes simplex virus type 1. . Genetics 170:(2):96970
    [Crossref] [Google Scholar]
  25. 25.
    Sijmons S, Thys K, Mbong Ngwese M, Van Damme E, Dvorak J, et al. 2015.. High-throughput analysis of human cytomegalovirus genome diversity highlights the widespread occurrence of gene-disrupting mutations and pervasive recombination. . J. Virol. 89:(15):767395
    [Crossref] [Google Scholar]
  26. 26.
    Renzette N, Pokalyuk C, Gibson L, Bhattacharjee B, Schleiss MR, et al. 2015.. Limits and patterns of cytomegalovirus genomic diversity in humans. . PNAS 112:(30):E412028
    [Crossref] [Google Scholar]
  27. 27.
    Brown J. 2004.. Effect of gene location on the evolutionary rate of amino acid substitutions in herpes simplex virus proteins. . Virology 330:(1):20920
    [Crossref] [Google Scholar]
  28. 28.
    Lee K, Kolb AW, Sverchkov Y, Cuellar JA, Craven M, Brandt CR. 2015.. Recombination analysis of herpes simplex virus 1 reveals a bias toward GC content and the inverted repeat regions. . J. Virol. 89:(14):721423
    [Crossref] [Google Scholar]
  29. 29.
    Greenbaum BD, Ghedin E. 2015.. Viral evolution: beyond drift and shift. . Curr. Opin. Microbiol. 26::10915
    [Crossref] [Google Scholar]
  30. 30.
    Kuny CV, Bowen CD, Renner DW, Johnston CM, Szpara ML. 2020.. In vitro evolution of herpes simplex virus 1 (HSV-1) reveals selection for syncytia and other minor variants in cell culture. . Virus Evol. 6:(1):veaa013
    [Crossref] [Google Scholar]
  31. 31.
    Jaramillo N, Domingo E, Munoz-Egea MC, Tabares E, Gadea I. 2013.. Evidence of Muller's ratchet in herpes simplex virus type 1. . J. Gen. Virol. 94:(Part 2):36675
    [Crossref] [Google Scholar]
  32. 32.
    Firth C, Kitchen A, Shapiro B, Suchard MA, Holmes EC, Rambaut A. 2010.. Using time-structured data to estimate evolutionary rates of double-stranded DNA viruses. . Mol. Biol. Evol. 27:(9):203851
    [Crossref] [Google Scholar]
  33. 33.
    Forni D, Pontremoli C, Clerici M, Pozzoli U, Cagliani R, Sironi M. 2020.. Recent out-of-Africa migration of human herpes simplex viruses. . Mol. Biol. Evol. 37:(5):125971
    [Crossref] [Google Scholar]
  34. 34.
    Depledge DP, Gray ER, Kundu S, Cooray S, Poulsen A, et al. 2014.. Evolution of cocirculating varicella-zoster virus genotypes during a chickenpox outbreak in Guinea-Bissau. . J. Virol. 88:(24):1393646
    [Crossref] [Google Scholar]
  35. 35.
    Bradley AJ, Lurain NS, Ghazal P, Trivedi U, Cunningham C, et al. 2009.. High-throughput sequence analysis of variants of human cytomegalovirus strains Towne and AD169. . J. Gen. Virol. 90::237580
    [Crossref] [Google Scholar]
  36. 36.
    Dargan DJ, Douglas E, Cunningham C, Jamieson F, Stanton RJ, et al. 2010.. Sequential mutations associated with adaptation of human cytomegalovirus to growth in cell culture. . J. Gen. Virol. 91::153546
    [Crossref] [Google Scholar]
  37. 37.
    Charles OJ, Venturini C, Gantt S, Atkinson C, Griffiths P, et al. 2023.. Genomic and geographical structure of human cytomegalovirus. . PNAS 120:(30):e2221797120
    [Crossref] [Google Scholar]
  38. 38.
    Sarisky RT, Nguyen TT, Duffy KE, Wittrock RJ, Leary JJ. 2000.. Difference in incidence of spontaneous mutations between Herpes simplex virus types 1 and 2. . Antimicrob. Agents Chemother. 44:(6):152429
    [Crossref] [Google Scholar]
  39. 39.
    Kuny CV, Szpara ML. 2020.. Alphaherpesvirus genomics: past, present and future. . Curr. Issues Mol. Biol. 42::4180
    [Google Scholar]
  40. 40.
    Cunningham C, Gatherer D, Hilfrich B, Baluchova K, Derrick J, et al. 2010.. Sequences of complete human cytomegalovirus genomes from infected cell cultures and clinical specimens. . J. Gen. Virol. 91::60515
    [Crossref] [Google Scholar]
  41. 41.
    Depledge DP, Yamanishi K, Gomi Y, Gershon AA, Breuer J. 2016.. Deep sequencing of distinct preparations of the live attenuated varicella-zoster virus vaccine reveals a conserved core of attenuating single-nucleotide polymorphisms. . J. Virol. 90:(19):8698704
    [Crossref] [Google Scholar]
  42. 42.
    Ortigas-Vásquez A, Pandey U, Renner D, Bowen CD, Baigent SJ, et al. 2024.. Comparative analysis of multiple consensus genomes of the same strain of Marek's disease virus reveals intrastrain variation. . Virus Evol. 10:veae047
    [Google Scholar]
  43. 43.
    Houldcroft CJ, Beale MA, Breuer J. 2017.. Clinical and biological insights from viral genome sequencing. . Nat. Rev. Microbiol. 15:(3):18392
    [Crossref] [Google Scholar]
  44. 44.
    Burrel S, Deback C, Agut H, Boutolleau D. 2010.. Genotypic characterization of UL23 thymidine kinase and UL30 DNA polymerase of clinical isolates of herpes simplex virus: natural polymorphism and mutations associated with resistance to antivirals. . Antimicrob. Agents Chemother. 54:(11):483342
    [Crossref] [Google Scholar]
  45. 45.
    Sauerbrei A, Deinhardt S, Zell R, Wutzler P. 2010.. Phenotypic and genotypic characterization of acyclovir-resistant clinical isolates of herpes simplex virus. . Antivir. Res. 86:(3):24652
    [Crossref] [Google Scholar]
  46. 46.
    Houldcroft CJ, Bryant JM, Depledge DP, Margetts BK, Simmonds J, et al. 2016.. Detection of low frequency multi-drug resistance and novel putative maribavir resistance in immunocompromised pediatric patients with cytomegalovirus. . Front. Microbiol. 7::1317
    [Crossref] [Google Scholar]
  47. 47.
    Tweedy JG, Prusty BK, Gompels UA. 2017.. Use of whole genome deep sequencing to define emerging minority variants in virus envelope genes in herpesvirus treated with novel antimicrobial K21. . Antivir. Res. 146::2014
    [Crossref] [Google Scholar]
  48. 48.
    Hage E, Wilkie GS, Linnenweber-Held S, Dhingra A, Suárez NM, et al. 2017.. Characterization of human cytomegalovirus genome diversity in immunocompromised hosts by whole-genome sequencing directly from clinical specimens. . J. Infect. Dis. 215:(11):167383
    [Crossref] [Google Scholar]
  49. 49.
    Depledge DP, Cudini J, Kundu S, Atkinson C, Brown JR, et al. 2018.. High viral diversity and mixed infections in cerebral spinal fluid from cases of varicella zoster virus encephalitis. . J. Infect. Dis. 218:(10):1592601
    [Crossref] [Google Scholar]
  50. 50.
    Mercier-Darty M, Boutolleau D, Lepeule R, Rodriguez C, Burrel S. 2018.. Utility of ultra-deep sequencing for detection of varicella-zoster virus antiviral resistance mutations. . Antivir. Res. 151::2023
    [Crossref] [Google Scholar]
  51. 51.
    Quiñones-Mateu ME, Avila S, Reyes-Teran G, Martinez MA. 2014.. Deep sequencing: becoming a critical tool in clinical virology. . J. Clin. Virol. 61:(1):919
    [Crossref] [Google Scholar]
  52. 52.
    Reuter JA, Spacek DV, Snyder MP. 2015.. High-throughput sequencing technologies. . Mol. Cell 58:(4):58697
    [Crossref] [Google Scholar]
  53. 53.
    Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, et al. 2012.. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. . J. Comput. Biol. 19:(5):45577
    [Crossref] [Google Scholar]
  54. 54.
    Bowen CD, Renner DW, Shreve JT, Tafuri Y, Payne KM, et al. 2016.. Viral forensic genomics reveals the relatedness of classic herpes simplex virus strains KOS, KOS63, and KOS79. . Virology 492::17986
    [Crossref] [Google Scholar]
  55. 55.
    Andino R, Domingo E. 2015.. Viral quasispecies. . Virology 479–480::4651
    [Crossref] [Google Scholar]
  56. 56.
    Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R. 2006.. Quasispecies diversity determines pathogenesis through cooperative interactions within a viral population. . Nature 439:(7074):34448
    [Crossref] [Google Scholar]
  57. 57.
    Moya A, Elena SF, Bracho A, Miralles R, Barrio E. 2000.. The evolution of RNA viruses: a population genetics view. . PNAS 97:(13):696773
    [Crossref] [Google Scholar]
  58. 58.
    Holmes EC, Moya A. 2002.. Is the quasispecies concept relevant to RNA viruses?. J. Virol. 76:(1):46065
    [Crossref] [Google Scholar]
  59. 59.
    McAllister J, Simmonds P, Casino C, Smith DB. 1997.. Virus “quasispecies”: making a mountain out of a molehill?. J. Gen. Virol. 78:(7):151119
    [Crossref] [Google Scholar]
  60. 60.
    Fitzsimmons WJ, Woods RJ, McCrone JT, Woodman A, Arnold JJ, et al. 2018.. A speed-fidelity trade-off determines the mutation rate and virulence of an RNA virus. . PLOS Biol. 16:(6):e2006459
    [Crossref] [Google Scholar]
  61. 61.
    Trimpert J, Groenke N, Kunec D, Eschke K, He S, et al. 2019.. A proofreading-impaired herpesvirus generates populations with quasispecies-like structure. . Nat. Microbiol. 4:(12):217583
    [Crossref] [Google Scholar]
  62. 62.
    López-Muñoz AD, Rastrojo A, Martín R, Alcamí A. 2021.. Herpes simplex virus 2 (HSV-2) evolves faster in cell culture than HSV-1 by generating greater genetic diversity. . PLOS Pathog. 17:(8):e1009541
    [Crossref] [Google Scholar]
  63. 63.
    Isakov O, Bordería AV, Golan D, Hamenahem A, Celniker G, et al. 2015.. Deep sequencing analysis of viral infection and evolution allows rapid and detailed characterization of viral mutant spectrum. . Bioinformatics 31:(13):214150
    [Crossref] [Google Scholar]
  64. 64.
    Shipley MM, Renner DW, Ott M, Bloom DC, Koelle DM, et al. 2018.. Genome-wide surveillance of genital herpes simplex virus type 1 from multiple anatomic sites over time. . J. Infect. Dis. 218:(4):595605
    [Crossref] [Google Scholar]
  65. 65.
    Greninger AL, Roychoudhury P, Xie H, Casto A, Cent A, et al. 2018.. Ultrasensitive capture of human herpes simplex virus genomes directly from clinical samples reveals extraordinarily limited evolution in cell culture. . mSphere 3:(3):e00283-18
    [Crossref] [Google Scholar]
  66. 66.
    Prescott J, Feldmann H, Safronetz D. 2017.. Amending Koch's postulates for viral disease: when “growth in pure culture” leads to a loss of virulence. . Antivir. Res. 137::15
    [Crossref] [Google Scholar]
  67. 67.
    Depledge DP, Palser AL, Watson SJ, Lai IY-C, Gray ER, et al. 2011.. Specific capture and whole-genome sequencing of viruses from clinical samples. . PLOS ONE 6:(11):e27805
    [Crossref] [Google Scholar]
  68. 68.
    Shipley MM, Rathbun MM, Szpara ML. 2020.. Oligonucleotide enrichment of HSV-1 genomic DNA from clinical specimens for use in high-throughput sequencing. . In Herpes Simplex Virus, ed. RJ Diefenbach, C Fraefel , pp. 199217. New York:: Springer
    [Google Scholar]
  69. 69.
    Suárez NM, Wilkie GS, Hage E, Camiolo S, Holton M, et al. 2019.. Human cytomegalovirus genomes sequenced directly from clinical material: variation, multiple-strain infection, recombination, and gene loss. . J. Infect. Dis. 220:(5):78191
    [Crossref] [Google Scholar]
  70. 70.
    Kaymaz Y, Oduor CI, Aydemir O, Luftig MA, Otieno JA, et al. 2020.. Epstein Barr virus genomes reveal population structure and type 1 association with endemic Burkitt lymphoma. . J. Virol. 94::e02007-19
    [Crossref] [Google Scholar]
  71. 71.
    Lassalle F, Beale MA, Bharucha T, Williams CA, Williams RJ, et al. 2020.. Whole genome sequencing of Herpes Simplex Virus 1 directly from human cerebrospinal fluid reveals selective constraints in neurotropic viruses. . Virus Evol. 6:(1):veaa012
    [Crossref] [Google Scholar]
  72. 72.
    Huang S-W, Hung S-J, Wang J-R. 2019.. Application of deep sequencing methods for inferring viral population diversity. . J. Virol. Methods 266::95102
    [Crossref] [Google Scholar]
  73. 73.
    Mangul S, Wu NC, Mancuso N, Zelikovsky A, Sun R, Eskin E. 2014.. Accurate viral population assembly from ultra-deep sequencing data. . Bioinformatics 30:(12):i32937
    [Crossref] [Google Scholar]
  74. 74.
    Sims D, Sudbery I, Ilott NE, Heger A, Ponting CP. 2014.. Sequencing depth and coverage: key considerations in genomic analyses. . Nat. Rev. Genet. 15:(2):12132
    [Crossref] [Google Scholar]
  75. 75.
    Deng C, Daley T, Calabrese P, Ren J, Smith AD. 2020.. Predicting the number of bases to attain sufficient coverage in high-throughput sequencing experiments. . J. Comput. Biol. 27:(7):113043
    [Crossref] [Google Scholar]
  76. 76.
    Gweon HS, Shaw LP, Swann J, De Maio N, AbuOun M, et al. 2019.. The impact of sequencing depth on the inferred taxonomic composition and AMR gene content of metagenomic samples. . Environ. Microbiome 14:(1):7
    [Crossref] [Google Scholar]
  77. 77.
    Illingworth CJR, Roy S, Beale MA, Tutill H, Williams R, Breuer J. 2017.. On the effective depth of viral sequence data. . Virus Evol. 3:(2):vex030
    [Crossref] [Google Scholar]
  78. 78.
    Chateigner A, Bézier A, Labrousse C, Jiolle D, Barbe V, Herniou E. 2015.. Ultra deep sequencing of a baculovirus population reveals widespread genomic variations. . Viruses 7:(7):362546
    [Crossref] [Google Scholar]
  79. 79.
    Chen-Harris H, Borucki MK, Torres C, Slezak TR, Allen JE. 2013.. Ultra-deep mutant spectrum profiling: improving sequencing accuracy using overlapping read pairs. . BMC Genom. 14::96
    [Crossref] [Google Scholar]
  80. 80.
    Posada-Cespedes S, Seifert D, Beerenwinkel N. 2016.. Recent advances in inferring viral diversity from high-throughput sequencing data. . Virus Res. 239::1732
    [Crossref] [Google Scholar]
  81. 81.
    Daly GM, Leggett RM, Rowe W, Stubbs S, Wilkinson M, et al. 2015.. Host subtraction, filtering and assembly validations for novel viral discovery using next generation sequencing data. . PLOS ONE 10:(6):e0129059
    [Crossref] [Google Scholar]
  82. 82.
    Bhaduri A, Qu K, Lee CS, Ungewickell A, Khavari PA. 2012.. Rapid identification of non-human sequences in high-throughput sequencing datasets. . Bioinformatics 28:(8):117475
    [Crossref] [Google Scholar]
  83. 83.
    Rathbun MM, Shipley MM, Bowen CD, Selke S, Wald A, et al. 2022.. Comparison of herpes simplex virus 1 genetic diversity between adult sexual transmission partners with genital infection. . PLOS Pathog. 18:(5):e1010437
    [Crossref] [Google Scholar]
  84. 84.
    Kieft K, Anantharaman K. 2022.. Virus genomics: What is being overlooked?. Curr. Opin. Virol. 53::101200
    [Crossref] [Google Scholar]
  85. 85.
    Watson SJ, Welkers MRA, Depledge DP, Coulter E, Breuer JM, et al. 2013.. Viral population analysis and minority-variant detection using short read next-generation sequencing. . Philos. Trans. R. Soc. B 368:(1614):20120205
    [Crossref] [Google Scholar]
  86. 86.
    Ghasemzadeh A, Ter Haar MM, Shams-Bakhsh M, Pirovano W, Pantaleo V. 2018.. Shannon entropy to evaluate substitution rate variation among viral nucleotide positions in datasets of viral siRNAs. . Methods Mol. Biol. 1746::18795
    [Crossref] [Google Scholar]
  87. 87.
    Nelson CW, Hughes AL. 2015.. Within-host nucleotide diversity of virus populations: insights from next-generation sequencing. . Infect. Genet. Evol. 30::17
    [Crossref] [Google Scholar]
  88. 88.
    Staden R. 1979.. A strategy of DNA sequencing employing computer programs. . Nucleic Acids Res. 6:(7):260110
    [Crossref] [Google Scholar]
  89. 89.
    Treangen TJ, Salzberg SL. 2011.. Repetitive DNA and next-generation sequencing: computational challenges and solutions. . Nat. Rev. Genet. 13:(1):3646
    [Crossref] [Google Scholar]
  90. 90.
    Van Dijk EL, Jaszczyszyn Y, Naquin D, Thermes C. 2018.. The third revolution in sequencing technology. . Trends Genet. 34:(9):66681
    [Crossref] [Google Scholar]
  91. 91.
    López-Muñoz AD, Rastrojo A, Alcamí A. 2018.. Complete genome sequence of herpes simplex virus 2 strain 333. . Microbiol. Resour. Announc. 7:(9):e00870-18
    [Crossref] [Google Scholar]
  92. 92.
    Karamitros T, van Wilgenburg B, Wills M, Klenerman P, Magiorkinis G. 2018.. Nanopore sequencing and full genome de novo assembly of human cytomegalovirus TB40/E reveals clonal diversity and structural variations. . BMC Genom. 19:(1):577
    [Crossref] [Google Scholar]
  93. 93.
    Yajima M, Ikuta K, Kanda T. 2018.. Rapid CRISPR/Cas9-mediated cloning of full-length Epstein-Barr virus genomes from latently infected cells. . Viruses 10:(4):171
    [Crossref] [Google Scholar]
  94. 94.
    Jiao X, Sui H, Lyons C, Tran B, Sherman BT, Imamichi T. 2019.. Complete genome sequence of herpes simplex virus 1 strain MacIntyre. . Microbiol. Resour. Announc. 8:(37):e00895-19
    [Crossref] [Google Scholar]
  95. 95.
    López-Muñoz AD, Rastrojo A, Kropp KA, Viejo-Borbolla A, Alcamí A. 2021.. Combination of long- and short-read sequencing fully resolves complex repeats of herpes simplex virus 2 strain MS complete genome. . Microb. Genom. 7:(6):000586
    [Google Scholar]
  96. 96.
    Chang W, Jiao X, Sui H, Goswami S, Sherman BT, et al. 2022.. Complete genome sequence of herpes simplex virus 2 strain G. . Viruses 14:(3):536
    [Crossref] [Google Scholar]
  97. 97.
    Chau VQ, Kolb AW, Miller DL, Yannuzzi NA, Brandt CR. 2023.. Phylogenetic and genomic characterization of whole genome sequences of ocular herpes simplex virus type 1 isolates identifies possible virulence determinants in humans. . Investig. Opthalmol. Vis. Sci. 64:(10):16
    [Crossref] [Google Scholar]
  98. 98.
    Mahiet C, Ergani A, Huot N, Alende N, Azough A, et al. 2012.. Structural variability of the herpes simplex virus 1 genome in vitro and in vivo. . J. Virol. 86:(16):8592601
    [Crossref] [Google Scholar]
  99. 99.
    Saranathan R, Asare E, Leung L, De Oliveira AP, Kaugars KE, et al. 2022.. Capturing structural variants of herpes simplex virus genome in full length by Oxford Nanopore Sequencing. . Microbiol. Spectr. 10:(5):e02285-22
    [Crossref] [Google Scholar]
  100. 100.
    Genoyer E, López CB. 2019.. The impact of defective viruses on infection and immunity. . Annu. Rev. Virol. 6::54766
    [Crossref] [Google Scholar]
  101. 101.
    Hayward GS, Ambinder R, Ciufo D, Diane Hayward S, Lafemina RL. 1984.. Structural organization of human herpesvirus DNA molecules. . J. Investig. Dermatol. 83:(1):S2941
    [Crossref] [Google Scholar]
  102. 102.
    Shitrit A, Nisnevich V, Rozenshtein N, Kobo H, Phan HV, et al. 2023.. Shared sequence characteristics identified in non-canonical rearrangements of HSV-1 genomes. . J. Virol. 97:(12):e00955-23
    [Crossref] [Google Scholar]
  103. 103.
    Jain M, Olsen HE, Paten B, Akeson M. 2016.. The Oxford Nanopore MinION: delivery of nanopore sequencing to the genomics community. . Genome Biol. 17:(1):239
    [Crossref] [Google Scholar]
  104. 104.
    Wang L, Qu L, Yang L, Wang Y, Zhu H. 2020.. NanoReviser: an error-correction tool for nanopore sequencing based on a deep learning algorithm. . Front. Genet. 11::900
    [Crossref] [Google Scholar]
  105. 105.
    Wenger AM, Peluso P, Rowell WJ, Chang P-C, Hall RJ, et al. 2019.. Accurate circular consensus long-read sequencing improves variant detection and assembly of a human genome. . Nat. Biotechnol. 37:(10):115562
    [Crossref] [Google Scholar]
  106. 106.
    Castro CJ, Marine RL, Ramos E, Ng TFF. 2020.. The effect of variant interference on de novo assembly for viral deep sequencing. . BMC Genom. 21:(1):421
    [Crossref] [Google Scholar]
  107. 107.
    Deng X, Naccache SN, Ng T, Federman S, Li L, et al. 2015.. An ensemble strategy that significantly improves de novo assembly of microbial genomes from metagenomic next-generation sequencing data. . Nucleic Acids Res. 43:(7):e46
    [Crossref] [Google Scholar]
  108. 108.
    Padovani de Souza K, Setubal JC, de Carvalho A, Oliveira G, Chateau A, Alves R. 2019.. Machine learning meets genome assembly. . Brief. Bioinform. 20:(6):211629
    [Crossref] [Google Scholar]
  109. 109.
    Dias R, Torkamani A. 2019.. Artificial intelligence in clinical and genomic diagnostics. . Genome Med. 11:(1):70
    [Crossref] [Google Scholar]
  110. 110.
    Van Loo P, Nordgard SH, Lingjærde OC, Russnes HG, Rye IH, et al. 2010.. Allele-specific copy number analysis of tumors. . PNAS 107:(39):1691015
    [Crossref] [Google Scholar]
  111. 111.
    Skums P, Mancuso N, Artyomenko A, Tork B, Mandoiu I, et al. 2013.. Reconstruction of viral population structure from next-generation sequencing data using multicommodity flows. . BMC Bioinform. 14:(Supp. 9):S2
    [Crossref] [Google Scholar]
  112. 112.
    Giallonardo FD, Töpfer A, Rey M, Prabhakaran S, Duport Y, et al. 2014.. Full-length haplotype reconstruction to infer the structure of heterogeneous virus populations. . Nucleic Acids Res. 42:(14):e115
    [Crossref] [Google Scholar]
  113. 113.
    Schirmer M, Sloan WT, Quince C. 2014.. Benchmarking of viral haplotype reconstruction programmes: an overview of the capacities and limitations of currently available programmes. . Brief. Bioinform. 15:(3):43142
    [Crossref] [Google Scholar]
  114. 114.
    Garg S. 2021.. Computational methods for chromosome-scale haplotype reconstruction. . Genome Biol. 22:(1):101
    [Crossref] [Google Scholar]
  115. 115.
    Pulido-Tamayo S, Sánchez-Rodríguez A, Swings T, Van den Bergh B, Dubey A, et al. 2015.. Frequency-based haplotype reconstruction from deep sequencing data of bacterial populations. . Nucleic Acids Res. 43:(16):e105
    [Crossref] [Google Scholar]
  116. 116.
    Venturini C, Pang J, Tamuri AU, Roy S, Atkinson C, et al. 2022.. Haplotype assignment of longitudinal viral deep sequencing data using covariation of variant frequencies. . Virus Evol. 8:(2):veac093
    [Crossref] [Google Scholar]
  117. 117.
    Cai D, Shang J, Sun Y. 2022.. HaploDMF: viral haplotype reconstruction from long reads via deep matrix factorization. . Bioinformatics 38:(24):536067
    [Crossref] [Google Scholar]
  118. 118.
    Cai D, Sun Y. 2022.. Reconstructing viral haplotypes using long reads. . Bioinformatics 38:(8):212734
    [Crossref] [Google Scholar]
  119. 119.
    Cheng H, Concepcion GT, Feng X, Zhang H, Li H. 2021.. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. . Nat. Methods 18:(2):17075
    [Crossref] [Google Scholar]
  120. 120.
    Koren S, Rhie A, Walenz BP, Dilthey AT, Bickhart DM, et al. 2018.. De novo assembly of haplotype-resolved genomes with trio binning. . Nat. Biotechnol. 36:(12):117482
    [Crossref] [Google Scholar]
  121. 121.
    Kronenberg ZN, Rhie A, Koren S, Concepcion GT, Peluso P, et al. 2021.. Extended haplotype-phasing of long-read de novo genome assemblies using Hi-C. . Nat. Commun. 12:(1):1935
    [Crossref] [Google Scholar]
  122. 122.
    Allen LZ, Ishoey T, Novotny MA, McLean JS, Lasken RS, Williamson SJ. 2011.. Single virus genomics: a new tool for virus discovery. . PLOS ONE 6:(3):e17722
    [Crossref] [Google Scholar]
  123. 123.
    Jing W, Han H-S. 2022.. Droplet microfluidics for high-resolution virology. . Anal. Chem. 94:(23):8085100
    [Crossref] [Google Scholar]
  124. 124.
    Martínez Martínez J, Martinez-Hernandez F, Martinez-Garcia M. 2020.. Single-virus genomics and beyond. . Nat. Rev. Microbiol. 18:(12):70516
    [Crossref] [Google Scholar]
  125. 125.
    Martinez-Hernandez F, Fornas O, Lluesma Gomez M, Bolduc B, de la Cruz Peña MJ, et al. 2017.. Single-virus genomics reveals hidden cosmopolitan and abundant viruses. . Nat. Commun. 8::15892
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-virology-100422-010336
Loading
/content/journals/10.1146/annurev-virology-100422-010336
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error