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PreprintCited by 31interferon and immune responsesEvolution and Genetic DynamicsInvertebrate Immune Response Mechanisms

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Viperin immunity evolved across the tree of life through serial innovations on a conserved scaffold

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Shomar, H, Georjon, H, Feng, Y, Olympio, B, Tesson, F, Cury, J, Wu, F, Bernheim, A·2023·Nature Ecology & Evolution
DOI 10.1101/2023.09.13.557418

Preprint — published as 10.1038/s41559-024-02463-z · Paper page

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Abstract

Evolutionary arms races between cells and viruses drive the rapid diversification of antiviral genes in diverse life forms. Recent discoveries have revealed the existence of shared immune genes between prokaryotes and eukaryotes, showing molecular and mechanistic similarities in their response to viruses. However, the underlying evolutionary dynamics that explain the conservation and adaptation of these antiviral genes remain mostly unexplored. Here, we show that viperins constitute a highly conserved family of immune genes across diverse prokaryotes and eukaryotes, and uncover mechanisms by which they diversified in eukaryotes. Our findings indicate that viperins are enriched in Asgard archaea and widely distributed in all major eukaryotic clades, suggesting their presence in the Last Eukaryotic Common Ancestor (LECA). We show that viperins maintain their immune function by producing antiviral nucleotide analogs. We demonstrate that eukaryotic viperins diversified through serial innovations on the viperin gene, such as the emergence and selection of substrate specificity towards pyrimidine nucleotides, and through partnerships with genes maintained through genetic linkage, notably with nucleotide kinases. These findings unveil biochemical and genomic transitions underlying the adaptation of immune genes shared by prokaryotes and eukaryotes. Our study paves the way for the understanding of the conservation of immunity across domains of life.

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Research works printed but not linked: 63

  1. 2023, The virome of the last eukaryotic common ancestor and eukaryogenesis, Nature microbiology, 8, 1008, 10.1038/s41564-023-01378-y · DOI
  2. 10.1038/s41579-020-0408-x · DOI
  3. 2020, The pan-immune system of bacteria: antiviral defence as a community resource, Nat Rev Microbiol, 18, 113, 10.1038/s41579-019-0278-2 · DOI
  4. 10.1038/nri2807 · DOI
  5. 10.1093/gbe/evz266 · DOI
  6. 2023, Origins and diversification of animal innate immune responses against viral infections, Nature ecology & evolution, 7, 182, 10.1038/s41559-022-01951-4 · DOI
  7. 10.1016/j.chom.2016.01.006 · DOI
  8. 2023, The evolution of plant NLR immune receptors and downstream signal components, Current opinion in plant biology, 73, 102363, 10.1016/j.pbi.2023.102363 · DOI
  9. Green, T. J. & Speck, P. Antiviral Defense and Innate Immune Memory in the Oyster. Viruses 10, (2018). · DOI
  10. 2022, Evolution of the interferon response: lessons from ISGs of diverse mammals, Current opinion in virology, 53, 101202, 10.1016/j.coviro.2022.101202 · DOI
  11. 10.1038/s41577-022-00705-4 · DOI
  12. 2020, STING cyclic dinucleotide sensing originated in bacteria, Nature, 586, 429, 10.1038/s41586-020-2719-5 · DOI
  13. 2019, Cyclic GMP-AMP signalling protects bacteria against viral infection, Nature, 574, 691, 10.1038/s41586-019-1605-5 · DOI
  14. 10.1038/s41586-021-04098-7 · DOI
  15. 2023, A conserved family of immune effectors cleaves cellular ATP upon viral infection, Cell, 186, 3619, 10.1016/j.cell.2023.07.020 · DOI
  16. 10.1126/science.abm4096 · DOI
  17. 10.1101/2022.12.12.520048 · DOI
  18. 2020, Viperin Reveals Its True Function, Annu Rev Virol, 7, 421, 10.1146/annurev-virology-011720-095930 · DOI
  19. 10.1038/s41586-018-0238-4 · DOI
  20. 2021, Prokaryotic viperins produce diverse antiviral molecules, Nature, 589, 120, 10.1038/s41586-020-2762-2 · DOI
  21. 2021, Structural Insight into the Substrate Scope of Viperin and Viperin-like Enzymes from Three Domains of Life, Biochemistry, 60, 2116, 10.1021/acs.biochem.0c00958 · DOI
  22. 10.1021/acs.biochem.9b00741 · DOI
  23. 10.1073/pnas.1705402114 · DOI
  24. 10.1038/nature21031 · DOI · Paper page
  25. 10.1038/s41467-022-30269-9 · DOI
  26. 10.1038/s41586-023-06186-2 · DOI
  27. 2021, Expanded diversity of Asgard archaea and their relationships with eukaryotes, Nature, 593, 553, 10.1038/s41586-021-03494-3 · DOI
  28. 2022, Unique mobile elements and scalable gene flow at the prokaryote-eukaryote boundary revealed by circularized Asgard archaea genomes, Nature microbiology, 7, 200, 10.1038/s41564-021-01039-y · DOI
  29. Shujairi, W.-H. A. et al. Viperin is anti-viral in vitro but is dispensable for restricting dengue virus replication or induction of innate and inflammatory responses in vivo. The Journal of general virology 102, (2021). · DOI
  30. 10.1074/jbc.M807261200 · DOI
  31. 10.1101/cshperspect.a013250 · DOI
  32. 2023, CMPK2 is a host restriction factor that inhibits infection of multiple coronaviruses in a cell-intrinsic manner, PLoS biology, 21, e3002039, 10.1371/journal.pbio.3002039 · DOI
  33. 10.1074/jbc.RA119.007719 · DOI
  34. 2021, G. The Antiviral Enzyme, Viperin, Activates Protein Ubiquitination by the E3 Ubiquitin Ligase, TRAF6, Journal of the American Chemical Society, 143, 4910, 10.1021/jacs.1c01045 · DOI
  35. 2023, CMPK2 restricts Zika virus replication by inhibiting viral translation, PLoS pathogens, 19, e1011286, 10.1371/journal.ppat.1011286 · DOI
  36. 2021, cGAS-like receptors sense RNA and control 3’2’-cGAMP signalling in Drosophila, Nature, 597, 109, 10.1038/s41586-021-03743-5 · DOI
  37. 2023, cGLRs are a diverse family of pattern recognition receptors in innate immunity, Cell, 186, 3261, 10.1016/j.cell.2023.05.038 · DOI
  38. 10.1101/2023.06.27.546753 · DOI · Paper page
  39. 10.1073/pnas.1219381110 · DOI
  40. 2022, Evolution of polygenic traits under global vs local adaptation, Genetics, 220, iyab134, 10.1093/genetics/iyab134 · DOI
  41. 10.1126/science.aar4120 · DOI
  42. 10.1371/journal.pone.0110726 · DOI
  43. 2022, GTDB: an ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy, Nucleic acids research, 50, D785, 10.1093/nar/gkab776 · DOI · Paper page
  44. 2011, Accelerated Profile HMM Searches, PLoS computational biology, 7, e1002195, 10.1371/journal.pcbi.1002195 · DOI · Paper page
  45. 10.1093/molbev/msaa015 · DOI · Paper page
  46. 10.1093/bioinformatics/bts565 · DOI · Paper page
  47. 10.1093/bioinformatics/bty121 · DOI
  48. 2022, EukProt: A database of genome-scale predicted proteins across the diversity of eukaryotes, Peer Community Journal, 2, e56, 10.24072/pcjournal.173 · DOI
  49. 10.1093/bioinformatics/btp348 · DOI
  50. 10.1186/s12859-018-2164-8 · DOI
  51. 10.1093/molbev/msx281 · DOI · Paper page
  52. 10.1093/NAR/GKAB301 · DOI
  53. 2022, ColabFold: making protein folding accessible to all, Nature methods, 19, 679, 10.1038/s41592-022-01488-1 · DOI · Paper page
  54. 10.1093/nar/28.1.235 · DOI · Paper page
  55. 10.1093/nar/gkn072 · DOI
  56. 10.1021/acs.analchem.8b02100 · DOI
  57. 2005, The 5′-nucleotidases as regulators of nucleotide and drug metabolism, Pharmacology & Therapeutics, 107, 1, 10.1016/j.pharmthera.2005.01.003 · DOI
  58. Price, M. N. , Dehal, P. S. & Arkin, A. P. FastTree 2 - Approximately maximum-likelihood trees for large alignments. PLoS ONE 5, (2010). · DOI · Paper page
  59. 10.1093/sysbio/syx068 · DOI · Paper page
  60. 10.1093/bioinformatics/16.2.135 · DOI
  61. 10.26508/lsa.201900429 · DOI
  62. 10.1186/s12859-019-3019-7 · DOI · Paper page
  63. 10.1093/NAR/GKAA1018 · DOI

Metadata

Authors
Shomar, H., Georjon, H., Feng, Y., Olympio, B., Tesson, F., Cury, J., Wu, F., & Bernheim, A.
Affiliations
  • Inserm (FR)
  • Eastern Institute of Technology, Ningbo (CN)
Corresponding author
  • Wu, F
  • Bernheim, A
ORCID
Venue
Nature Ecology & Evolution
Publisher
openRxiv
Published
2023-09-13
Volume
8
Issue
9
Pages
1667-1679
ISSN
2397-334X (ISSN-L)
DOI
10.1101/2023.09.13.557418
OpenAlex
W4400325003
Cited by
31
References
1
Citations by year
2026: 10 · 2025: 12 · 2024: 7 · 2023: 2
FWCI
4.85
Type
journal article
Language
en
Open access
Licence
cc-by-nc
Locations
  • Nature Ecology & Evolution (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, cc-by-nc)
Funders
  • Institut Français de Bioinformatique (ANR-11-INBS-0013)
  • European Commission (HORIZON2020, 945298)
  • Agence Nationale de la Recherche (ANR-11-INBS, ANR-11-INBS-0013)
  • Institut National de la Santé et de la Recherche Médicale (R21042KS/RSE22002KSA, R21042KS)
  • Fondation Bettencourt Schueller
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
  • Life Sciences › Immunology and Microbiology › Immunology › Invertebrate Immune Response Mechanisms
Keywords
viperin, antiviral immunity, evolutionary arms race, Asgard archaea, horizontal gene transfer, last eukaryotic common ancestor, nucleotide analogues, nucleotide kinase, genetic linkage, eukaryotic evolution
MeSH terms
Archaea, Phylogeny, Evolution, Molecular, Eukaryota

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