DNA methylation enables recurrent endogenization of giant viruses in an animal relative

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  • dc.contributor.author Sarre, Luke A.
  • dc.contributor.author Kim, Iana V.
  • dc.contributor.author Ovchinnikov, Vladimir
  • dc.contributor.author Olivetta, Marine
  • dc.contributor.author Suga, Hiroshi
  • dc.contributor.author Dudin, Omaya
  • dc.contributor.author Sebé-Pedrós, Arnau
  • dc.contributor.author Mendoza, Alex de
  • dc.date.accessioned 2024-09-20T06:06:41Z
  • dc.date.available 2024-09-20T06:06:41Z
  • dc.date.issued 2024
  • dc.description.abstract 5-Methylcytosine (5mC) is a widespread silencing mechanism that controls genomic parasites. In eukaryotes, 5mC has gained complex roles in gene regulation beyond parasite control, yet 5mC has also been lost in many lineages. The causes for 5mC retention and its genomic consequences are still poorly understood. Here, we show that the protist closely related to animals Amoebidium appalachense features both transposon and gene body methylation, a pattern reminiscent of invertebrates and plants. Unexpectedly, hypermethylated genomic regions in Amoebidium derive from viral insertions, including hundreds of endogenized giant viruses, contributing 14% of the proteome. Using a combination of inhibitors and genomic assays, we demonstrate that 5mC silences these giant virus insertions. Moreover, alternative Amoebidium isolates show polymorphic giant virus insertions, highlighting a dynamic process of infection, endogenization, and purging. Our results indicate that 5mC is critical for the controlled coexistence of newly acquired viral DNA into eukaryotic genomes, making Amoebidium a unique model to understand the hybrid origins of eukaryotic DNA.
  • dc.description.sponsorship This work was supported by European Research Council Starting Grant 950230 (A.d.M., L.A.S., and V.O.), European Research Council Starting Grant 851647 (A.S.-P.), Juan de la Cierva postdoctoral fellowship FJC2020-043131-I (I.V.K.), JSPS KAKENHI Grant Number JP16H06279 (H.S.), JSPS KAKENHI Grant Number JP26891021 (H.S.), Swiss National Science Foundation Ambizione fellowship PZ00P3_185859 (M.O. and O.D.), Spanish Ministry of Science and Innovation grant PID2021-124757NB-I00 (A.S.-P.), and Spanish Ministry’s support to the EMBL partnership, the Centro de Excelencia Severo Ochoa and the CERCA Programme (Generalitat de Catalunya) (A.S.-P.).
  • dc.format.mimetype application/pdf
  • dc.identifier.citation Sarre LA, Kim IV, Ovchinnikov V, Olivetta M, Suga H, Dudin O, et al. DNA methylation enables recurrent endogenization of giant viruses in an animal relative. Sci Adv. 2024 Jul 12;10(28):eado6406. DOI: 10.1126/sciadv.ado6406
  • dc.identifier.doi http://dx.doi.org/10.1126/sciadv.ado6406
  • dc.identifier.issn 2375-2548
  • dc.identifier.uri http://hdl.handle.net/10230/61187
  • dc.language.iso eng
  • dc.publisher American Association for the Advancement of Science (AAAS)
  • dc.relation.ispartof Sci Adv. 2024 Jul 12;10(28):eado6406
  • dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/950230
  • dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/851647
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/3PE/PID2021-124757NB-I00
  • dc.rights Copyright © 2024 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution License 4.0 (CC BY). This is an open-access article distributed under the terms of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
  • dc.rights.accessRights info:eu-repo/semantics/openAccess
  • dc.rights.uri http://creativecommons.org/licenses/by/4.0/
  • dc.subject.other Regulació genètica
  • dc.title DNA methylation enables recurrent endogenization of giant viruses in an animal relative
  • dc.type info:eu-repo/semantics/article
  • dc.type.version info:eu-repo/semantics/publishedVersion

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