Viral genomic methylation and the interspecies evolutionary relationships of ranavirus.

Publisher: Public Library of Science Country of Publication: United States NLM ID: 101238921 Publication Model: eCollection Cited Medium: Internet ISSN: 1553-7374 (Electronic) Linking ISSN: 15537366 NLM ISO Abbreviation: PLoS Pathog Subsets: MEDLINE

Original Publication: San Francisco, CA : Public Library of Science, c2005-

Ranavirus*/genetics ; Genome, Viral* ; Phylogeny*; Animals ; Evolution, Molecular ; DNA Methylation ; DNA Virus Infections/virology ; DNA Virus Infections/genetics ; Fishes/virology ; Fish Diseases/virology ; Virus Replication/genetics

Ranaviruses are capable of infecting both wild and farmed fish, amphibians, and reptiles, leading to significant economic losses and ecological risks. Currently, ranaviruses have been found in at least 175 species spanning six continents. Except for Singapore grouper iridovirus (SGIV), ranavirus genomes are generally regarded as highly methylated. Nevertheless, our comprehension of the methylation characteristics within ranaviruses remains limited. Despite the numerous genomes currently included in the GenBank database, a complete phylogenetic tree for ranaviruses has not yet been determined, and interspecific evolutionary relationships among ranaviruses have not been thoroughly investigated. In this study, the whole-genome methylation profile of mandarin fish ranavirus (MRV; a ranavirus) was investigated, revealing a methylation level of 16.04%, and hypomethylation of the MRV genome was detrimental to viral replication, speculating the genome methylation may play an important role in MRV replication. Furthermore, by combining with whole-genome DNA sequence phylogenetic analyses, we propose the possibility of an interspecies evolutionary relationship among ranaviruses, with the presence of four distinct evolutionary lineages within ranavirus evolution: "SGIV, SCRAV(MRV/LMBV), EHNV/ENARV/ATV, and CMTV/FV3", which might be also supported by the genomic collinearity, natural host range and host habitats. Furthermore, ranavirus genomic methylation levels may provide additional evidence for this hypothesis, but further proof is needed. Our work enhances the understanding of the role of genome methylation in ranaviruses and is beneficial for the prevention and control of ranavirus diseases; simultaneously, the proposed evolutionary hypothesis of ranavirus provides novel insights and ideas for exploring the evolutionary trajectory of viruses.
Competing Interests: The authors have declared that no competing interests exist.
(Copyright: © 2024 Pan et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

Papillomavirus Res. 2019 Jun;7:180-183. (PMID: 30978415)
Mol Biol Evol. 2013 Apr;30(4):772-80. (PMID: 23329690)
Nucleic Acids Res. 2023 Jan 6;51(D1):D29-D38. (PMID: 36370100)
Sci Rep. 2016 Jul 22;6:30160. (PMID: 27444743)
Nucleic Acids Res. 2024 Jul 5;52(W1):W521-W525. (PMID: 38597606)
Nature. 2019 May;569(7755):171. (PMID: 31065101)
Virology. 1987 Nov;161(1):211-7. (PMID: 2445102)
Vet Microbiol. 2017 May;203:28-33. (PMID: 28619157)
Fish Shellfish Immunol. 2019 Sep;92:141-150. (PMID: 31176007)
BMC Bioinformatics. 2009 Dec 15;10:421. (PMID: 20003500)
J Virol. 1984 Dec;52(3):905-12. (PMID: 6092719)
J Wildl Dis. 2013 Apr;49(2):464-7. (PMID: 23568931)
Nucleic Acids Res. 2008 May;36(9):2825-37. (PMID: 18367473)
Bioinformatics. 2009 Jun 1;25(11):1422-3. (PMID: 19304878)
Curr Top Microbiol Immunol. 2009;328:1-42. (PMID: 19216434)
Nucleic Acids Res. 2012 Apr;40(7):e49. (PMID: 22217600)
J Virol. 2010 Mar;84(6):2636-47. (PMID: 20042506)
J Virol. 1985 Mar;53(3):1005-7. (PMID: 3973962)
Front Vet Sci. 2023 Nov 23;10:1291872. (PMID: 38076556)
Virol J. 2007 Jan 19;4:11. (PMID: 17239238)
Bioinformatics. 2014 Aug 1;30(15):2114-20. (PMID: 24695404)
Nucleic Acids Res. 2017 Jan 4;45(D1):D37-D42. (PMID: 27899564)
J Gen Virol. 2017 May;98(5):890-891. (PMID: 28555546)
Viruses. 2023 Jul 28;15(8):. (PMID: 37631990)
J Virol. 2004 Nov;78(22):12576-90. (PMID: 15507645)
PLoS One. 2015 Aug 06;10(8):e0135058. (PMID: 26247357)
Viruses. 2012 Apr;4(4):521-38. (PMID: 22590684)
Virus Res. 2010 Jan;147(1):98-106. (PMID: 19895861)
Commun Biol. 2024 Feb 28;7(1):237. (PMID: 38413759)
Cold Spring Harb Perspect Biol. 2014 May 01;6(5):a019133. (PMID: 24789823)
Nature. 2009 Nov 19;462(7271):315-22. (PMID: 19829295)
Nucleic Acids Res. 2024 Jul 5;52(W1):W78-W82. (PMID: 38613393)
PLoS One. 2013;8(2):e56711. (PMID: 23451072)
Proc Natl Acad Sci U S A. 1976 Nov;73(11):3923-7. (PMID: 1069277)
Front Genet. 2023 Jan 12;13:1088081. (PMID: 36712873)
Oncogene. 2002 Aug 12;21(35):5483-95. (PMID: 12154409)
Comput Struct Biotechnol J. 2022 Jun 27;20:3493-3502. (PMID: 35860404)
Virology. 1980 Nov;107(1):250-7. (PMID: 6255678)
Mol Biol Evol. 2020 May 1;37(5):1530-1534. (PMID: 32011700)
J Virol Methods. 2013 Mar;188(1-2):121-5. (PMID: 23274753)
Syst Biol. 2016 Nov;65(6):997-1008. (PMID: 27121966)
Viruses. 2019 Jan 09;11(1):. (PMID: 30634383)
Mol Biol Evol. 2018 Feb 1;35(2):518-522. (PMID: 29077904)
Virology. 2017 Nov;511:259-271. (PMID: 28648249)
Methods Mol Biol. 2019;1894:181-227. (PMID: 30547463)
Bioinformatics. 2011 Jun 1;27(11):1571-2. (PMID: 21493656)
Philos Trans R Soc Lond B Biol Sci. 2017 Jan 19;372(1712):. (PMID: 27920373)
Virus Res. 2008 Aug;135(2):273-81. (PMID: 18485510)
Mol Biol Evol. 2012 Jun;29(6):1695-701. (PMID: 22319168)
Nat Methods. 2017 Jun;14(6):587-589. (PMID: 28481363)
J Gen Virol. 1995 Aug;76 ( Pt 8):1937-43. (PMID: 7636474)
Nucleic Acids Res. 2023 Jan 6;51(D1):D384-D388. (PMID: 36477806)
Ecol Evol. 2021 Oct 25;11(22):15498-15519. (PMID: 34824771)

Date Created: 20241125 Date Completed: 20241209 Latest Revision: 20241211

20241211

PMC11627377

10.1371/journal.ppat.1012736

39585924