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Koonin EV, Dolja VV, Krupovic M, et al. Viruses Defined by the Position of the Virosphere within the Replicator Space. Microbiol Mol Biol Rev. 2021;e0019320doi: 10.1128/MMBR.00193-20.
Koonin, E. V., Dolja, V. V., Krupovic, M., & Kuhn, J. H. (2021). Viruses Defined by the Position of the Virosphere within the Replicator Space. Microbiology and molecular biology reviews : MMBR, e0019320. https://doi.org/10.1128/MMBR.00193-20
Koonin, Eugene V, et al. "Viruses Defined by the Position of the Virosphere within the Replicator Space." Microbiology and molecular biology reviews : MMBR vol. (2021): e0019320. doi: https://doi.org/10.1128/MMBR.00193-20
Koonin EV, Dolja VV, Krupovic M, Kuhn JH. Viruses Defined by the Position of the Virosphere within the Replicator Space. Microbiol Mol Biol Rev. 2021 Sep 01;e0019320. doi: 10.1128/MMBR.00193-20. Epub 2021 Sep 01. PMID: 34468181; PMCID: PMC8483706.
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Microbiol Mol Biol Rev. 2021 Sep 01;e0019320. doi: 10.1128/MMBR.00193-20. Epub 2021 Sep 01.

Viruses Defined by the Position of the Virosphere within the Replicator Space.

Microbiology and molecular biology reviews : MMBR

Eugene V Koonin, Valerian V Dolja, Mart Krupovic, Jens H Kuhn

Affiliations

  1. National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland, USA.
  2. Department of Botany and Plant Pathology, Oregon State Universitygrid.4391.f, Corvallis, Oregon, USA.
  3. Archaeal Virology Unit, Institut Pasteurgrid.428999.7, Paris, France.
  4. Integrated Research Facility at Fort Detrick, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Frederick, Maryland, USA.

PMID: 34468181 PMCID: PMC8483706 DOI: 10.1128/MMBR.00193-20

Abstract

Originally, viruses were defined as miniscule infectious agents that passed through filters that retain even the smallest cells. Subsequently, viruses were considered obligate intracellular parasites whose reproduction depends on their cellular hosts for energy supply and molecular building blocks. However, these features are insufficient to unambiguously define viruses as they are broadly understood today. We outline possible approaches to define viruses and explore the boundaries of the virosphere within the virtual space of replicators and the relationships between viruses and other types of replicators. Regardless of how, exactly, viruses are defined, viruses clearly have evolved on many occasions from nonviral replicators, such as plasmids, by recruiting host proteins to become virion components. Conversely, other types of replicators have repeatedly evolved from viruses. Thus, the virosphere is a dynamic entity with extensive evolutionary traffic across its boundaries. We argue that the virosphere proper, here termed orthovirosphere, consists of a distinct variety of replicators that encode structural proteins encasing the replicators' genomes, thereby providing protection and facilitating transmission among hosts. Numerous and diverse replicators, such as virus-derived but capsidless RNA and DNA elements, or defective viruses occupy the zone surrounding the orthovirosphere in the virtual replicator space. We define this zone as the perivirosphere. Although intense debates on the nature of certain replicators that adorn the internal and external boundaries of the virosphere will likely continue, we present an operational definition of virus that recently has been accepted by the International Committee on Taxonomy of Viruses.

Keywords: MGE; mobile genetic element; orthovirosphere; perivirosphere; replicator; virosphere; virus; virus classification; virus definition; virus taxonomy

References

  1. Virology. 1995 Dec 20;214(2):571-83 - PubMed
  2. Nat Commun. 2018 Feb 27;9(1):749 - PubMed
  3. Adv Virus Res. 2019;103:167-202 - PubMed
  4. Stud Hist Philos Biol Biomed Sci. 2016 Oct;59:125-34 - PubMed
  5. Proc Natl Acad Sci U S A. 2020 Feb 18;117(7):3779-3788 - PubMed
  6. Cells. 2020 Nov 28;9(12): - PubMed
  7. Biosystems. 1974 Oct;6(2):113-32 - PubMed
  8. Mob DNA. 2017 Dec 6;8:19 - PubMed
  9. Adv Virus Res. 2013;86:109-47 - PubMed
  10. Nat Rev Microbiol. 2012 Jun 11;10(7):472-82 - PubMed
  11. Nat Commun. 2018 Jun 11;9(1):2285 - PubMed
  12. Parasitology. 2018 May;145(6):713-723 - PubMed
  13. J Theor Biol. 1983 Dec 21;105(4):591-602 - PubMed
  14. Curr Biol. 2020 Oct 5;30(19):R1108-R1110 - PubMed
  15. Nat Rev Microbiol. 2009 Apr;7(4):306-11 - PubMed
  16. Front Microbiol. 2012 Jul 27;3:262 - PubMed
  17. ISME J. 2017 Apr;11(4):1029-1042 - PubMed
  18. Nat Commun. 2020 Jun 15;11(1):3034 - PubMed
  19. Genome Biol Evol. 2016 Sep 26;8(9):2856-2869 - PubMed
  20. Philos Trans R Soc Lond B Biol Sci. 2013 Aug 12;368(1626):20130051 - PubMed
  21. Bioessays. 2020 Dec;42(12):e2000114 - PubMed
  22. Virus Evol. 2016 Jun 12;2(1):vew019 - PubMed
  23. Science. 2017 Apr 7;356(6333):82-85 - PubMed
  24. Curr Opin Microbiol. 2005 Aug;8(4):488-94 - PubMed
  25. Front Microbiol. 2021 Jan 14;11:604048 - PubMed
  26. J Extracell Vesicles. 2019 Jul 23;8(1):1643214 - PubMed
  27. Arch Virol. 2020 Jun;165(6):1267-1278 - PubMed
  28. Viruses. 2018 Dec 17;10(12): - PubMed
  29. Biol Direct. 2017 Dec 04;12(1):31 - PubMed
  30. Nat Commun. 2017 Sep 15;8(1):551 - PubMed
  31. Nucleic Acids Res. 2021 Mar 18;49(5):2655-2673 - PubMed
  32. Front Microbiol. 2018 Nov 27;9:2668 - PubMed
  33. Virus Res. 2015 Nov 2;209:136-45 - PubMed
  34. Res Microbiol. 2003 May;154(4):231-6 - PubMed
  35. Mol Biol Evol. 2021 May 4;38(5):1731-1743 - PubMed
  36. J Virol. 2015 Oct 21;90(2):659-69 - PubMed
  37. Photosynth Res. 2015 Oct;126(1):71-97 - PubMed
  38. Stud Hist Philos Biol Biomed Sci. 2016 Oct;59:100-8 - PubMed
  39. Virus Evol. 2021 Feb 19;7(1):veab015 - PubMed
  40. Nat Rev Microbiol. 2015 Feb;13(2):105-15 - PubMed
  41. Cell. 1989 Jul 28;58(2):399-408 - PubMed
  42. Nature. 1961 Apr 22;190:302-5 - PubMed
  43. RNA Biol. 2016 Dec;13(12):1218-1222 - PubMed
  44. Curr Top Microbiol Immunol. 1999;239:81-105 - PubMed
  45. Trends Neurosci. 2021 Apr;44(4):248-259 - PubMed
  46. Curr Opin Virol. 2017 Aug;25:41-48 - PubMed
  47. J Adv Res. 2019 Apr 23;19:75-84 - PubMed
  48. J Bacteriol. 2020 Apr 9;202(9): - PubMed
  49. Proc Natl Acad Sci U S A. 2017 Mar 21;114(12):E2401-E2410 - PubMed
  50. Virus Evol. 2019 Jul 15;5(2):vez021 - PubMed
  51. Virology. 1961 Nov;15:348-73 - PubMed
  52. J Gen Virol. 2003 Aug;84(Pt 8):1951-1960 - PubMed
  53. Crit Rev Biochem Mol Biol. 2017 Oct;52(5):583-594 - PubMed
  54. Virology. 1959 May;8(1):99-115 - PubMed
  55. Nat Commun. 2018 Aug 22;9(1):3360 - PubMed
  56. Proc Natl Acad Sci U S A. 2011 Sep 20;108(38):15931-5 - PubMed
  57. BMC Biol. 2015 Nov 11;13:95 - PubMed
  58. Mol Microbiol. 2018 Apr;108(1):6-15 - PubMed
  59. Philos Trans R Soc Lond B Biol Sci. 2006 Oct 29;361(1474):1761-76 - PubMed
  60. Nat Rev Microbiol. 2019 Jun;17(6):355-370 - PubMed
  61. Nat Commun. 2019 May 8;10(1):2098 - PubMed
  62. Nat Rev Microbiol. 2019 Jul;17(7):449-458 - PubMed
  63. J Virol. 2019 Feb 19;93(5): - PubMed
  64. Pathogens. 2020 Sep 18;9(9): - PubMed
  65. J Virol. 2021 Feb 3;: - PubMed
  66. Antonie Van Leeuwenhoek. 2014 Jul;106(1):27-41 - PubMed
  67. Microbiol Mol Biol Rev. 2014 Jun;78(2):278-303 - PubMed
  68. Ann N Y Acad Sci. 2009 Oct;1178:65-77 - PubMed
  69. Trends Biochem Sci. 2015 Nov;40(11):648-661 - PubMed
  70. Nature. 2012 Nov 15;491(7424):413-7 - PubMed
  71. Clin Infect Dis. 2017 Aug 15;65(suppl_1):S74-S79 - PubMed
  72. Rev Biol Trop. 2011 Sep;59(3):993-8 - PubMed
  73. Adv Virus Res. 2019;103:71-133 - PubMed
  74. Arch Gesamte Virusforsch. 1967;22(1):273-9 - PubMed
  75. Nat Commun. 2019 Jul 31;10(1):3425 - PubMed
  76. mBio. 2018 Nov 27;9(6): - PubMed
  77. J Virol. 2017 May 26;91(12): - PubMed
  78. Philos Trans R Soc Lond B Biol Sci. 2009 Aug 12;364(1527):2263-74 - PubMed
  79. Trends Microbiol. 2020 Dec;28(12):959-967 - PubMed
  80. Science. 2015 May 22;348(6237):914-7 - PubMed
  81. Science. 1935 Jun 28;81(2113):644-5 - PubMed
  82. Trends Plant Sci. 2006 May;11(5):209-12 - PubMed
  83. Virus Evol. 2017 Dec 07;3(2):vex036 - PubMed
  84. Proc Natl Acad Sci U S A. 2021 Jan 19;118(3): - PubMed
  85. Proc Natl Acad Sci U S A. 2011 Dec 20;108(51):20311-6 - PubMed
  86. Environ Microbiol. 2009 Nov;11(11):2771-4 - PubMed
  87. Viruses. 2015 Jul 17;7(7):3937-53 - PubMed
  88. Curr Opin Virol. 2013 Oct;3(5):578-86 - PubMed
  89. Annu Rev Virol. 2017 Sep 29;4(1):87-104 - PubMed
  90. J Virol. 2020 Jun 1;94(12): - PubMed
  91. Nat Microbiol. 2016 Apr 26;1:16056 - PubMed
  92. Curr Opin Virol. 2013 Oct;3(5):587-94 - PubMed
  93. PLoS One. 2013;8(1):e49044 - PubMed
  94. Viruses. 2019 Oct 31;11(11): - PubMed
  95. Nucleic Acids Res. 2016 Jun 2;44(10):4551-64 - PubMed
  96. Proc Soc Exp Biol Med. 1963 Apr;112:1040-50 - PubMed
  97. Adv Virus Res. 2018;100:99-116 - PubMed
  98. J Virol. 2021 Jul 12;95(15):e0067321 - PubMed
  99. Virus Evol. 2021 Feb 12;7(1):veab003 - PubMed
  100. Nat Microbiol. 2016 Jan 25;1:15024 - PubMed
  101. Proc Natl Acad Sci U S A. 2020 Jul 28;117(30):17977-17983 - PubMed
  102. Curr Opin Virol. 2013 Oct;3(5):546-57 - PubMed
  103. Cell Mol Life Sci. 2009 Dec;66(23):3727-42 - PubMed
  104. Cold Spring Harb Symp Quant Biol. 1962;27:1-24 - PubMed
  105. Virus Genes. 2021 Feb;57(1):1-22 - PubMed
  106. Bacteriol Rev. 1971 Sep;35(3):235-41 - PubMed
  107. RNA Biol. 2011 Mar-Apr;8(2):200-6 - PubMed
  108. Gene. 2007 Apr 1;390(1-2):3-17 - PubMed
  109. Annu Rev Phytopathol. 2020 Aug 25;58:23-53 - PubMed
  110. Virus Genes. 2019 Apr;55(2):165-173 - PubMed
  111. Nature. 2009 May 14;459(7244):207-12 - PubMed
  112. Virus Evol. 2020 Nov 30;6(2):veaa059 - PubMed
  113. Front Microbiol. 2018 Jan 22;8:2643 - PubMed
  114. J Virol. 2010 Dec;84(23):12100-9 - PubMed
  115. Arch Virol. 2016 Jan;161(1):233-47 - PubMed
  116. Mob DNA. 2020 Sep 17;11:29 - PubMed
  117. Curr Opin Virol. 2018 Aug;31:1-8 - PubMed
  118. Cancer Sci. 2017 May;108(5):824-830 - PubMed
  119. Virology. 2007 Jun 20;363(1):124-33 - PubMed
  120. Nucleic Acids Res. 2003 Nov 15;31(22):6481-92 - PubMed
  121. Sci Adv. 2016 Oct 12;2(10):e1600492 - PubMed
  122. Curr Opin Microbiol. 2016 Jun;31:25-33 - PubMed
  123. Proc Natl Acad Sci U S A. 2012 Oct 30;109(44):18078-83 - PubMed
  124. Proc Natl Acad Sci U S A. 2021 Mar 9;118(10): - PubMed
  125. Trends Microbiol. 2010 Jan;18(1):11-9 - PubMed
  126. Mol Microbiol. 1999 Oct;34(2):217-26 - PubMed
  127. J Mol Evol. 2007 Dec;65(6):668-86 - PubMed
  128. Curr Opin Microbiol. 2017 Aug;38:36-43 - PubMed
  129. J Virol. 1994 Oct;68(10):6363-71 - PubMed
  130. Nat Microbiol. 2017 Oct;2(10):1350-1357 - PubMed
  131. J Gen Microbiol. 1957 Oct;17(2):239-53 - PubMed
  132. J Virol. 2016 Nov 28;90(24):11043-11055 - PubMed
  133. Open Biol. 2013 Dec 11;3(12):130160 - PubMed
  134. Science. 2004 Mar 12;303(5664):1626-32 - PubMed
  135. Curr Opin Insect Sci. 2019 Apr;32:47-53 - PubMed
  136. Annu Rev Virol. 2015 Nov;2(1):181-201 - PubMed
  137. Nat Microbiol. 2017 Mar 06;2:17029 - PubMed
  138. Environ Microbiol. 2014 Apr;16(4):1167-75 - PubMed
  139. Nat Rev Microbiol. 2017 Feb;15(2):69-82 - PubMed
  140. Nat Rev Genet. 2020 Feb;21(2):119-131 - PubMed
  141. Proc Natl Acad Sci U S A. 2014 Oct 7;111(40):14542-7 - PubMed
  142. J Bacteriol. 2013 Mar;195(5):941-50 - PubMed
  143. Virus Evol. 2020 Apr 29;6(1):veaa023 - PubMed
  144. Nat Microbiol. 2017 Oct;2(10):1446-1455 - PubMed
  145. Clin Microbiol Infect. 2019 Feb;25(2):147-154 - PubMed
  146. Viruses. 2018 Dec 31;11(1): - PubMed
  147. Biol Direct. 2014 Apr 29;9:6 - PubMed
  148. Trends Microbiol. 2015 Oct;23(10):587-590 - PubMed
  149. PeerJ. 2017 Sep 27;5:e3841 - PubMed
  150. Virology. 2012 Dec 20;434(2):210-21 - PubMed
  151. Nucleic Acids Res. 2018 Nov 16;46(20):10563-10576 - PubMed
  152. Nat Rev Microbiol. 2019 Mar;17(3):181-192 - PubMed
  153. Microbiome. 2021 Jan 12;9(1):13 - PubMed
  154. Virus Res. 2006 Apr;117(1):133-44 - PubMed
  155. Curr Biol. 2017 May 8;27(9):1362-1368 - PubMed
  156. Virus Res. 2021 Jan 2;291:198205 - PubMed
  157. Annu Rev Virol. 2016 Sep 29;3(1):197-214 - PubMed
  158. Virus Evol. 2021 Feb 18;7(1):veab016 - PubMed
  159. ISME J. 2013 Feb;7(2):233-6 - PubMed
  160. Adv Virus Res. 2013;86:59-85 - PubMed
  161. C R Hebd Seances Acad Sci. 1962 Jun 13;254:4225-7 - PubMed
  162. Arch Virol. 2006 Jun;151(6):1249-50 - PubMed
  163. J Virol. 2018 Jun 13;92(13): - PubMed
  164. Curr Opin Virol. 2021 Apr;47:32-37 - PubMed
  165. Microbiol Mol Biol Rev. 2020 Mar 4;84(2): - PubMed
  166. Hist Philos Life Sci. 2012;34(3):391-406 - PubMed
  167. Curr Top Microbiol Immunol. 2006;307:113-31 - PubMed
  168. ISME J. 2020 Mar;14(3):727-739 - PubMed
  169. J Gen Virol. 2011 Nov;92(Pt 11):2674-2678 - PubMed
  170. PLoS One. 2013;8(1):e55102 - PubMed
  171. Public Health Pap Rep. 1900;26:37-53 - PubMed
  172. Annu Rev Microbiol. 1966;20:45-74 - PubMed
  173. Adv Virus Res. 2020;108:127-164 - PubMed
  174. Arch Virol. 2018 Sep;163(9):2587-2600 - PubMed
  175. Nucleic Acids Res. 2010 Jul;38(13):4207-17 - PubMed
  176. Nat Rev Microbiol. 2008 Apr;6(4):315-9 - PubMed
  177. PeerJ. 2015 Apr 09;3:e876 - PubMed
  178. ISME J. 2021 Oct;15(10):2892-2905 - PubMed
  179. Trends Microbiol. 2014 Oct;22(10):554-8 - PubMed
  180. Genome Biol. 2006;7(6):110 - PubMed
  181. Science. 1967 Oct 20;158(3799):378-81 - PubMed
  182. Proc Natl Acad Sci U S A. 2021 Feb 9;118(6): - PubMed
  183. New Phytol. 2016 Nov;212(3):680-692 - PubMed
  184. Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1285-9 - PubMed
  185. J R Microsc Soc. 1965 Sep;84(3):257-316 - PubMed
  186. Nature. 2016 Dec 22;540(7634):539-543 - PubMed
  187. Virus Res. 2016 Jul 2;219:92-99 - PubMed
  188. Proc Natl Acad Sci U S A. 2020 Aug 18;117(33):19643-19652 - PubMed
  189. Nat Rev Microbiol. 2020 Nov;18(11):661-670 - PubMed
  190. Nucleic Acids Res. 2011 Jan;39(Database issue):D70-4 - PubMed
  191. Cold Spring Harb Symp Quant Biol. 1962;27:51-5 - PubMed
  192. Adv Virus Res. 2018;102:89-117 - PubMed
  193. Nat Commun. 2019 Feb 14;10(1):752 - PubMed
  194. Annu Rev Phytopathol. 2004;42:13-34 - PubMed
  195. J Theor Biol. 2020 Feb 7;486:110096 - PubMed
  196. Stud Hist Philos Biol Biomed Sci. 2016 Oct;59:89-99 - PubMed
  197. Virology. 1971 Aug;45(2):411-28 - PubMed
  198. Annu Rev Phytopathol. 2013;51:357-81 - PubMed
  199. PLoS One. 2014 Nov 25;9(11):e114083 - PubMed
  200. Virology. 2015 May;479-480:356-68 - PubMed
  201. Adv Exp Med Biol. 2018;1045:209-226 - PubMed
  202. Virol J. 2018 Apr 10;15(1):67 - PubMed
  203. J Virol. 2018 May 29;92(12): - PubMed
  204. J Gen Virol. 2020 Nov;101(11):1131-1132 - PubMed
  205. Annu Rev Virol. 2017 Sep 29;4(1):61-85 - PubMed
  206. BMC Biol. 2014 May 19;12:36 - PubMed
  207. Proc Natl Acad Sci U S A. 1999 Mar 2;96(5):2192-7 - PubMed
  208. Curr Opin Virol. 2017 Aug;25:7-15 - PubMed
  209. Elife. 2017 Jun 22;6: - PubMed
  210. Virus Genes. 2020 Feb;56(1):16-26 - PubMed
  211. Curr Issues Mol Biol. 2020;34:163-182 - PubMed
  212. Sci Rep. 2016 Jul 25;6:30204 - PubMed
  213. Ann Inst Pasteur (Paris). 1959 Sep;97:281-9 - PubMed
  214. Science. 2013 Jul 19;341(6143):281-6 - PubMed
  215. J Gen Virol. 2021 Mar;102(3): - PubMed
  216. Intervirology. 2013;56(6):349-53 - PubMed
  217. Proc Natl Acad Sci U S A. 2014 Mar 18;111(11):4274-9 - PubMed
  218. J Theor Biol. 1997 Aug 21;187(4):555-71 - PubMed
  219. Sci Rep. 2018 Apr 9;8(1):5698 - PubMed
  220. Nat Rev Microbiol. 2017 Mar;15(3):161-168 - PubMed
  221. Virus Res. 2006 Apr;117(1):38-51 - PubMed
  222. Curr Opin Virol. 2021 Apr;47:86-94 - PubMed
  223. Proc Natl Acad Sci U S A. 2006 Mar 21;103(12):4540-5 - PubMed
  224. ISME J. 2021 Sep 23;: - PubMed
  225. Microbiol Spectr. 2015 Feb;3(1):MDNA3-0009-2014 - PubMed
  226. Science. 2007 Jan 26;315(5811):513-5 - PubMed

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