Asgard archaea defense systems and their roles in the origin of eukaryotic immunity.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
31 Jul 2024
31 Jul 2024
Historique:
received:
16
04
2024
accepted:
28
06
2024
medline:
1
8
2024
pubmed:
1
8
2024
entrez:
31
7
2024
Statut:
epublish
Résumé
Dozens of new antiviral systems have been recently characterized in bacteria. Some of these systems are present in eukaryotes and appear to have originated in prokaryotes, but little is known about these defense mechanisms in archaea. Here, we explore the diversity and distribution of defense systems in archaea and identify 2610 complete systems in Asgardarchaeota, a group of archaea related to eukaryotes. The Asgard defense systems comprise 89 unique systems, including argonaute, NLR, Mokosh, viperin, Lassamu, and CBASS. Asgard viperin and argonaute proteins have structural homology to eukaryotic proteins, and phylogenetic analyses suggest that eukaryotic viperin proteins were derived from Asgard viperins. We show that Asgard viperins display anti-phage activity when heterologously expressed in bacteria. Eukaryotic and bacterial argonaute proteins appear to have originated in Asgardarchaeota, and Asgard argonaute proteins have argonaute-PIWI domains, key components of eukaryotic RNA interference systems. Our results support that Asgardarchaeota played important roles in the origin of antiviral defense systems in eukaryotes.
Identifiants
pubmed: 39085212
doi: 10.1038/s41467-024-50195-2
pii: 10.1038/s41467-024-50195-2
doi:
Substances chimiques
Archaeal Proteins
0
Argonaute Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
6386Subventions
Organisme : Simons Foundation
ID : 73592LPI
Organisme : Welch Foundation
ID : F-1808
Informations de copyright
© 2024. The Author(s).
Références
Mayo-Muñoz, D., Pinilla-Redondo, R., Birkholz, N. & Fineran, P. C. A host of armor: Prokaryotic immune strategies against mobile genetic elements. Cell Rep. 42, 112672 (2023).
doi: 10.1016/j.celrep.2023.112672
pubmed: 37347666
Roux, S., Hallam, S. J., Woyke, T. & Sullivan, M. B. Viral dark matter and virus-host interactions resolved from publicly available microbial genomes. elife 4, e08490 (2015).
doi: 10.7554/eLife.08490
pubmed: 26200428
pmcid: 4533152
Bernheim, A. & Sorek, R. The pan-immune system of bacteria: antiviral defence as a community resource. Nat. Rev. Microbiol. 18, 113–119 (2020).
doi: 10.1038/s41579-019-0278-2
pubmed: 31695182
Cury, J. et al. Conservation of antiviral systems across domains of life reveals novel immune mechanisms in humans. Preprint at bioRxiv https://doi.org/10.1101/2022.12.12.520048 (2022).
Doron, S. et al. Systematic discovery of antiphage defense systems in the microbial pangenome. Science 359, eaar4120 (2018).
doi: 10.1126/science.aar4120
pubmed: 29371424
pmcid: 6387622
Tesson, F. et al. Systematic and quantitative view of the antiviral arsenal of prokaryotes. Nat. Commun. 13, 2561 (2022).
doi: 10.1038/s41467-022-30269-9
pubmed: 35538097
pmcid: 9090908
Millman, A. et al. An expanded arsenal of immune systems that protect bacteria from phages. Cell host-microbe 30, 1556–1569 (2022).
doi: 10.1016/j.chom.2022.09.017
pubmed: 36302390
Eme, L. et al. Inference and reconstruction of the heimdallarchaeial ancestry of eukaryotes. Nature 618, 1–8 (2023).
Zaremba-Niedzwiedzka, K. et al. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541, 353–358 (2017).
doi: 10.1038/nature21031
pubmed: 28077874
Makarova, K. S. et al. Evolutionary classification of CRISPR–Cas systems: a burst of class 2 and derived variants. Nat. Rev. Microbiol. 18, 67–83 (2020).
doi: 10.1038/s41579-019-0299-x
pubmed: 31857715
Chin, K. C. & Cresswell, P. Viperin (cig5), an IFN-inducible antiviral protein directly induced by human cytomegalovirus. Proc. Natl Acad. Sci. 98, 15125–15130 (2001).
doi: 10.1073/pnas.011593298
pubmed: 11752458
pmcid: 64994
Fenwick, M. K., Li, Y., Cresswell, P., Modis, Y. & Ealick, S. E. Structural studies of viperin, an antiviral radical SAM enzyme. Proc. Natl Acad. Sci. 114, 6806–6811 (2017).
doi: 10.1073/pnas.1705402114
pubmed: 28607080
pmcid: 5495270
Bernheim, A. et al. Prokaryotic viperins produce diverse antiviral molecules. Nature 589, 120–124 (2021).
doi: 10.1038/s41586-020-2762-2
pubmed: 32937646
Meeks, J. C. Physiological adaptations in nitrogen-fixing Nostoc–plant symbiotic associations. In Prokaryotic Symbionts in Plants (pp. 181–205). Berlin, Heidelberg: Springer Berlin Heidelberg (2007).
Li, F. W. et al. Fern genomes elucidate land plant evolution and cyanobacterial symbioses. Nat. plants 4, 460–472 (2018).
doi: 10.1038/s41477-018-0188-8
pubmed: 29967517
pmcid: 6786969
Lachowicz, J. C., Gizzi, A. S., Almo, S. C. & Grove, T. L. Structural insight into the substrate scope of viperin and viperin-like enzymes from three domains of life. Biochemistry 60, 2116–2129 (2021).
doi: 10.1021/acs.biochem.0c00958
pubmed: 34156827
Shomar, H. et al. Viperin immunity evolved across the tree of life through serial innovations on a conserved scaffold. Nature Ecology & Evolution, 1–13 (2024).
Rivera-Serrano, E. E. et al. Viperin reveals its true function. Annu. Rev. Virol. 7, 421–446 (2020).
doi: 10.1146/annurev-virology-011720-095930
pubmed: 32603630
pmcid: 8191541
Penev, P. I. et al. Supersized ribosomal RNA expansion segments in Asgard archaea. Genome Biol. Evol. 12, 1694–1710 (2020).
doi: 10.1093/gbe/evaa170
pubmed: 32785681
pmcid: 7594248
Bartel, D. P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281–297 (2004).
doi: 10.1016/S0092-8674(04)00045-5
pubmed: 14744438
Hammond, S. M., Bernstein, E., Beach, D. & Hannon, G. J. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404, 293–296 (2000).
doi: 10.1038/35005107
pubmed: 10749213
Cerutti, L., Mian, N. & Bateman, A. Domains in gene silencing and cell differentiation proteins: the novel PAZ domain and redefinition of the Piwi domain. Trends Biochem. Sci. 25, 481–482 (2000).
doi: 10.1016/S0968-0004(00)01641-8
pubmed: 11050429
Shabalina, S. A. & Koonin, E. V. Origins and evolution of eukaryotic RNA interference. Trends Ecol. Evol. 23, 578–587 (2008).
doi: 10.1016/j.tree.2008.06.005
pubmed: 18715673
pmcid: 2695246
Makarova, K. S., Wolf, Y. I., van der Oost, J. & Koonin, E. V. Prokaryotic homologs of Argonaute proteins are predicted to function as key components of a novel system of defense against mobile genetic elements. Biol. Direct 4, 1–15 (2009).
doi: 10.1186/1745-6150-4-29
Willkomm, S., Makarova, K. S. & Grohmann, D. DNA silencing by prokaryotic Argonaute proteins adds a new layer of defense against invading nucleic acids. FEMS Microbiol. Rev. 42, 376–387 (2018).
doi: 10.1093/femsre/fuy010
pubmed: 29579258
pmcid: 5995195
Song, J. J., Smith, S. K., Hannon, G. J. & Joshua-Tor, L. Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305, 1434–1437 (2004).
doi: 10.1126/science.1102514
pubmed: 15284453
Sheu-Gruttadauria, J. & MacRae, I. J. Structural foundations of RNA silencing by argonaute. J. Mol. Biol. 429, 2619–2639 (2017).
doi: 10.1016/j.jmb.2017.07.018
pubmed: 28757069
pmcid: 5576611
Ryazansky, S., Kulbachinskiy, A. & Aravin, A. A. The expanded universe of prokaryotic Argonaute proteins. MBio 9, 10–1128 (2018).
doi: 10.1128/mBio.01935-18
Sachs, A. B., Sarnow, P. & Hentze, M. W. Starting at the beginning, middle, and end: translation initiation in eukaryotes. Cell 89, 831–838 (1997).
doi: 10.1016/S0092-8674(00)80268-8
pubmed: 9200601
Erickson, F. L., Nika, J., Rippel, S. & Hannig, E. M. Minimum requirements for the function of eukaryotic translation initiation factor 2. Genetics 158, 123–132 (2001).
doi: 10.1093/genetics/158.1.123
pubmed: 11333223
pmcid: 1461651
Wang, S. et al. Electron transport chains in organohalide-respiring bacteria and bioremediation implications. Biotechnol. Adv. 36, 1194–1206 (2018).
doi: 10.1016/j.biotechadv.2018.03.018
pubmed: 29631017
Wang, X. et al. Structural insights into mechanisms of Argonaute protein-associated NADase activation in bacterial immunity. Cell Res. 33, 1–13 (2023).
Swarts, D. C. et al. The evolutionary journey of Argonaute proteins. Nat. Struct. Mol. Biol. 21, 743–753 (2014).
doi: 10.1038/nsmb.2879
pubmed: 25192263
pmcid: 4691850
Bastiaanssen, C. et al. RNA-guided RNA silencing by an Asgard archaeal Argonaute. Nat Commun 15, 5499 (2024).
Kibby, E. M. et al. Bacterial NLR-related proteins protect against phage. Cell 186, 2410–2424 (2023).
doi: 10.1016/j.cell.2023.04.015
pubmed: 37160116
pmcid: 10294775
Appler, K. E. et al. Oxygen metabolism in descendants of the archaeal-eukaryotic ancestor. Preprint at bioRxiv https://doi.org/10.1101/2024.07.04.601786v1 (2024).
Buchfink, B., Reuter, K. & Drost, H. G. Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat. methods 18, 366–368 (2021).
doi: 10.1038/s41592-021-01101-x
pubmed: 33828273
pmcid: 8026399
Richter, D. J. et al. EukProt: a database of genome-scale predicted proteins across the diversity of eukaryotes. Peer Community J. 2, e56 (2022).
Shen, W., Le, S., Li, Y. & Hu, F. SeqKit: a cross-platform and ultrafast toolkit for FASTA/Q file manipulation. PloS one 11, e0163962 (2016).
doi: 10.1371/journal.pone.0163962
pubmed: 27706213
pmcid: 5051824
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
doi: 10.1093/molbev/mst010
pubmed: 23329690
pmcid: 3603318
Steenwyk, J. L. et al. ClipKIT: a multiple sequence alignment trimming software for accurate phylogenomic inference. PLoS Biol. 18, e3001007 (2020).
doi: 10.1371/journal.pbio.3001007
pubmed: 33264284
pmcid: 7735675
Minh, B. Q. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530–1534 (2020).
doi: 10.1093/molbev/msaa015
pubmed: 32011700
pmcid: 7182206
Mirdita, M. et al. ColabFold: making protein folding accessible to all. Nat. methods 19, 679–682 (2022).
doi: 10.1038/s41592-022-01488-1
pubmed: 35637307
pmcid: 9184281
Dong, R., Peng, Z., Zhang, Y. & Yang, J. mTM-align: an algorithm for fast and accurate multiple protein structure alignment. Bioinformatics 34, 1719–1725 (2018).
doi: 10.1093/bioinformatics/btx828
pubmed: 29281009
Pettersen, E. F. et al. UCSF ChimeraX: Structure visualization for researchers, educators, and developers. Protein Sci. 30, 70–82 (2021).
doi: 10.1002/pro.3943
pubmed: 32881101
Jones, P. et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236–1240 (2014).
doi: 10.1093/bioinformatics/btu031
pubmed: 24451626
pmcid: 3998142
Clokie, M. R. & Kropinski, A., 2009. Methods and protocols, volume 1: Isolation, Characterization, and Interactions. Methods Mol. Biol. Humana press, pp.69–81.
Baba, T. et al. Construction of Escherichia coli K‐12 in‐frame, single‐gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2, 2006–0008 (2006).
doi: 10.1038/msb4100050
pmcid: 1681482
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. methods 9, 676–682 (2012).
doi: 10.1038/nmeth.2019
pubmed: 22743772