[Viruses and the evolution of modern eukaryotic cells].
Les virus et l’émergence des cellules eucaryotes modernes.
Journal
Medecine sciences : M/S
ISSN: 1958-5381
Titre abrégé: Med Sci (Paris)
Pays: France
ID NLM: 8710980
Informations de publication
Date de publication:
Dec 2022
Dec 2022
Historique:
entrez:
24
1
2023
pubmed:
25
1
2023
medline:
27
1
2023
Statut:
ppublish
Résumé
It is now well accepted that viruses have played an important role in the evolution of modern eukaryotes. In this review, we suggest that interactions between ancient eukaryoviruses and proto-eukaryotes also played a major role in eukaryogenesis. We discuss phylogenetic analyses that highlight the viral origin of several key proteins in the molecular biology of eukaryotes. We also discuss recent observations that, by analogy, could suggest a viral origin of the cellular nucleus. Finally, we hypothesize that mechanisms of cell differentiation in multicellular organisms might have originated from mechanisms implemented by viruses to transform infected cells into virocells. Les virus et l’émergence des cellules eucaryotes modernes. Il est maintenant bien établi que les virus ont joué un rôle important dans l’évolution des eucaryotes modernes. Dans cette revue, nous commentons le rôle qu’ils ont pu jouer dans l’eucaryogenèse. Nous discutons les analyses phylogénétiques qui mettent en évidence l’origine virale de plusieurs protéines clés de la biologie moléculaire des eucaryotes et des observations récentes qui, par analogie, pourraient suggérer une origine virale du noyau cellulaire. Nous mettons en parallèle la complexité des eucaryotes avec l’unicité de leur virosphère et avançons l’hypothèse selon laquelle des mécanismes de la différenciation cellulaire auraient leur source dans ceux mis en œuvre par les virus pour transformer les cellules infectées en cellules virales.
Autres résumés
Type: Publisher
(fre)
Les virus et l’émergence des cellules eucaryotes modernes.
Identifiants
pubmed: 36692278
doi: 10.1051/medsci/2022164
pii: msc220144
doi:
Types de publication
Review
English Abstract
Journal Article
Langues
fre
Sous-ensembles de citation
IM
Pagination
990-998Informations de copyright
© 2022 médecine/sciences – Inserm.
Références
Raoult D, Forterre P. Redefining viruses: Lessons from Mimivirus. Nat Rev Microbiol 2008 ; 6 : 315–319.
Forterre, P. To Be or Not to Be Alive: How Recent Discoveries Challenge the Traditional Definitions of Viruses and Life, Stud Hist Philos Biol Biomed Sci 2016; pii : S1369–8486(16)30008–5.
Nasir A, Romero-Severson E, Claverie JM. Investigating the Concept and Origin of Viruses. Trends Microbiol 2020; 28 : 959–67.
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; 85(4) : e0019320.
Nasir A, Forterre P, Kim KM, et al. The distribution and impact of viral lineages in domains of life. Front Microbiol 2014 ; 5 : 194.
Koonin EV, Dolja VV, Krupovic M, et al. Global organization and proposed megataxonomy of the virus world. Microbiol Mol Biol Rev 2020; 84(2) : e00061–19.
Woo AC, Gaia M, Guglielmini J, et al. Phylogeny of the Varidnaviria morphogenesis module: congruence and incongruence with the tree of life and viral taxonomy. Front Microbiol 2021; 12 : 704052.
Koonin EV, Dolja VV, Krupovic M. Origins and evolution of viruses of eukaryotes: The ultimate modularity. Virology 2015 ; 479–80 : 2–25.
Da Cunha V, Gaia M, Forterre P. The expending Asgard archaea and their elusive relationships with Eukarya. mLife 2022; 1 : 3–12.
Forterre P, Prangishvili D. The great billion-year war between ribosome – and capsid-encoding organisms (cells and viruses) as the major source of evolutionary novelties. Ann N Y Acad Sci 2009 ; 1178 : 65–77.
Decroly E, Ferron F, Lescar J, et al. Conventional and unconventional mechanisms for capping viral mRNA. Nat Rev Microbiol 2012 ; 10 : 51–65.
Bell PJL. Evidence supporting a viral origin of the eukaryotic nucleus. Virus Res 2020; 289 : 198168.
Forterre P, Gaïa M. Giant viruses and the origin of modern eukaryotes. Curr Opin Microbiol 2016 ; 31 : 44–49.
Ochman H, Lawrence JG, Groisman EA. Lateral gene transfer and the nature of bacterial innovation. Nature 2000 ; 405 : 299–304.
Koonin EV. Taming of the shrewd: novel eukaryotic genes from RNA viruses. BMC Biol 2010 ; 8 : 2.
Arneth B. Leftovers of viruses in human physiology. Brain Struct Funct 2021; 226 : 1649–58.
Peltier C, Schmidlin L, Klein E, et al. Expression of the Beet necrotic yellow vein virus p25 protein induces hormonal changes and a root branching phenotype in Arabidopsis thaliana. Transgenic Res 2011 ; 20 : 443–466.
Valansi C, Moi D, Leikina E, et al. Arabidopsis HAP2/GCS1 is a gamete fusion protein homologous to somatic and viral fusogens. J Cell Biol 2017 ; 216 : 571–581.
Barreat JCN, Katzourakis A. Paleovirology of the DNA viruses of eukaryotes. Trends in Microbiol 2022; 30 : 281–92.
Filée J. Multiple occurrences of mimivirus core genes acquired by eukaryotic genomes. Virology 2014 ; 466–7 : 53–59.
Moniruzzaman M, Weinheimer AR, Martinez-Gutierrez CA, et al., Widespread endogenization of giant viruses shapes genomes of green algae. Nature 2020; 588 : 141–5.
Irwin NAT, Pittis AA, Richard TA, et al. Systematic evaluation of horizontal gene transfer between eukaryotes and viruses. Nature microbiol 2022; 7 : 327–36.
La Scola B, Audic S, Robert C, et al. A giant virus in amoebae. Science 2003 ; 299 : 2033.
Takemura M. Poxviruses and the origin of the eukaryotic nucleus. J Mol Evol 2001 ; 52 : 419–425.
Bell PJ. Viral eukaryogenesis: was the ancestor of the nucleus a complex DNA virus?. J Mol Evol 2001 ; 53 : 251–256.
Takemura M. Medusavirus Ancestor in a Proto-Eukaryotic Cell: Updating the Hypothesis for the Viral Origin of the Nucleus. Front Microbiol 2020; 11 : 571831.
Forterre P, Gaia M. Giant viruses and the origin of eukaryotic RNA polymerases. Med Sci (Paris) 2021; 37 : 230–3.
Koonin EV, Yutin N. Evolution of the Large Nucleocytoplasmic DNA Viruses of Eukaryotes and Convergent Origins of Viral Gigantism. Adv Virus Res 2019 ; 103 : 167–202.
Guglielmini J, Woo AC, Krupovic M, et al. Diversification of giant and large eukaryotic dsDNA viruses predated the origin of modern eukaryotes. Proc Natl Acad Sci USA 2019 ; 116 : 19585–19592.
Liu Y, Bisio H, Toner CM, et al. Virus-encoded histone doublets are essential and form nucleosome-like structures. Cell 2021; 184 : 4237–50.e19.
Kijima S, Delmont TO, Miyazaki U, et al. Discovery of Viral Myosin Genes With Complex Evolutionary History Within Plankton. Front Microbiol 2021; 12 : 683294.
Da Cunha V, Gaia M, Ogata H, et al. Giant Viruses Encode Actin-Related Proteins. Mol Biol Evol 2022; 39(2) : msac022.
Khalifeh D, Neveu E, Fasshauer D. Megaviruses contain various genes encoding for eukaryotic vesicle trafficking factors. Traffic 2022; 23 : 414–25.
Villarreal LP, DeFilippis VR. A hypothesis for DNA viruses as the origin of eukaryotic replication proteins. J Virol 2000 ; 74 : 7079–7084.
Forterre P. Why are there so many diverse replication machineries?. J Mol Biol 2013 ; 425 : 4714–4726.
Takemura M, Yokobori S, Ogata H. Evolution of Eukaryotic DNA Polymerases via Interaction Between Cells and Large DNA Viruses. J Mol Evol 2015 ; 81 : 24–33.
Kazlauskas D, Krupovic M, Guglielmini J, et al. Diversity and evolution of B-family DNA polymerases. Nucleic Acids Res 2020; 48 : 10142–56.
Guglielmini J, Gaia M, Da Cunha V, et al. Viral origin of eukaryotic type IIA DNA topoisomerases. Virus evolution 2022; sous presse.
Mondal N, Parvin JD. DNA topoisomerase II alpha is required for RNA polymerase II transcription on chromatin templates. Nature 2001 ; 413 : 435–438.
Sperling AS, Jeong KS, Kitada T, et al. Topoisomerase II binds nucleosome-free DNA and acts redundantly with topoisomerase I to enhance recruitment of RNA Pol II in budding yeast. Proc Nat Acad Sci USA 2011 ; 108 : 12693–12698.
Netherton CL, Wileman T. Virus factories, double membrane vesicles and viroplasm generated in animal cells. Curr Opin Virol 2011 ; 1 : 381–387.
Chaikeeratisak V, Nguyen K, Khanna K, et al. Assembly of a nucleus-like structure during viral replication in bacteria. Science 2017 ; 355 : 194–197.
Mendoza SD, Nieweglowska ES, Govindarajan S, et al. A bacteriophage nucleus-like compartment shields DNA from CRISPR nucleases. Nature 2020; 577 : 244–8.
Wolff G, Limpens RWAL, Zevenhoven-Dobbe JC, et al. A molecular pore spans the double membrane of the coronavirus replication organelle Science 2020; 369 : 1395–8.
Sanderson M, Way M, Smith GL. Virus-induced cell motility. J Virol 1998 ; 72 : 1235–1243.
Buchrieser J, Dufloo J, Hubert M, et al. Syncytia formation by SARS-CoV-2-infected cells. EMBO J 2020; 39 : e106267.
Liu J, Cvirkaite-Krupovic V, Baquero DP, et al. Virus-induced cell gigantism and asymmetric cell division in archaea. Proc Natl Acad Sci USA 2021; 118 : e2022578118.
Forterre P. The virocell concept and environmental microbiology. ISME J 2013 ; 7 : 233–236.
Heisserer C, Selosse MA, Drezen JM. Des virus bénéfiques pour les plantes et les animaux. Med Sci (Paris) 2022; 38 : ???.