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The CRISPR system in bacteria and archaea provides adaptive immunity against mobile genetic elements. Type III CRISPR systems detect viral RNA, resulting in the activation of two regions of the Cas10 protein: an HD nuclease domain (which degrades viral DNA) 1,2 and a cyclase domain (which synthesizes cyclic oligoadenylates from ATP) 3-5 . Cyclic oligoadenylates in turn activate defence enzymes with a CRISPR-associated Rossmann fold domain 6 , sculpting a powerful antiviral response 7-10 that can drive viruses to extinction 7,8 . Cyclic nucleotides are increasingly implicated in host-pathogen interactions 11-13 . Here we identify a new family of viral anti-CRISPR (Acr) enzymes that rapidly degrade cyclic tetra-adenylate (cA 4 ). The viral ring nuclease AcrIII-1 is widely distributed in archaeal and bacterial viruses and in proviruses. The enzyme uses a previously unknown fold to bind cA 4 specifically, and a conserved active site to rapidly cleave this signalling molecule, allowing viruses to neutralize the type III CRISPR defence system. The AcrIII-1 family has a broad host range, as it targets cA 4 signalling molecules rather than specific CRISPR effector proteins. Our findings highlight the crucial role of cyclic nucleotide signalling in the conflict between viruses and their hosts.

Titel:	An anti-CRISPR viral ring nuclease subverts type III CRISPR immunity.
Autor/in / Beteiligte Person:	Athukoralage, JS ; McMahon, SA ; Zhang, C ; Grüschow, S ; Graham, S ; Krupovic, M ; Whitaker, RJ ; Gloster, TM ; White, MF
Link:	Zum Volltext
Zeitschrift:	Nature, Jg. 577 (2020), Heft 7791, S. 572-575
Veröffentlichung:	Basingstoke : Nature Publishing Group ; <i>Original Publication</i>: London, Macmillan Journals ltd., 2020
Medientyp:	academicJournal
ISSN:	1476-4687 (electronic)
DOI:	10.1038/s41586-019-1909-5
Schlagwort:	Adenine Nucleotides chemistry Adenine Nucleotides metabolism CRISPR-Associated Proteins chemistry CRISPR-Associated Proteins metabolism DNA, Viral metabolism Endonucleases chemistry Models, Molecular Nucleotides, Cyclic chemistry Nucleotides, Cyclic metabolism Oligoribonucleotides chemistry Oligoribonucleotides metabolism Phylogeny Signal Transduction Sulfolobus genetics Sulfolobus immunology Sulfolobus metabolism Viral Proteins chemistry Viral Proteins classification Viruses immunology CRISPR-Cas Systems immunology Endonucleases metabolism Host Microbial Interactions immunology Sulfolobus virology Viral Proteins metabolism Viruses enzymology
Sonstiges:	Nachgewiesen in: MEDLINE Sprachen: English Publication Type: Journal Article; Research Support, Non-U.S. Gov't Language: English [Nature] 2020 Jan; Vol. 577 (7791), pp. 572-575. <i>Date of Electronic Publication: </i>2020 Jan 15. MeSH Terms: CRISPR-Cas Systems / immunology ; Endonucleases / metabolism ; Host Microbial Interactions / immunology ; Sulfolobus / virology ; Viral Proteins / metabolism ; Viruses / enzymology ; Adenine Nucleotides / chemistry ; Adenine Nucleotides / metabolism ; CRISPR-Associated Proteins / chemistry ; CRISPR-Associated Proteins / metabolism ; DNA, Viral / metabolism ; Endonucleases / chemistry ; Models, Molecular ; Nucleotides, Cyclic / chemistry ; Nucleotides, Cyclic / metabolism ; Oligoribonucleotides / chemistry ; Oligoribonucleotides / metabolism ; Phylogeny ; Signal Transduction ; Sulfolobus / genetics ; Sulfolobus / immunology ; Sulfolobus / metabolism ; Viral Proteins / chemistry ; Viral Proteins / classification ; Viruses / immunology Comments: Comment in: Mol Cell. 2020 May 21;78(4):568-569. (PMID: 32442502) References: Samai, P. et al. Co-transcriptional DNA and RNA cleavage during type III CRISPR-Cas immunity. Cell 161, 1164–1174 (2015). (PMID: 25959775459484010.1016/j.cell.2015.04.027) ; Tamulaitis, G. et al. Programmable RNA shredding by the type III-A CRISPR-Cas system of Streptococcus thermophilus. Mol. Cell 56, 506–517 (2014). (PMID: 2545884510.1016/j.molcel.2014.09.027) ; Kazlauskiene, M., Kostiuk, G., Venclovas, Č., Tamulaitis, G. & Siksnys, V. A cyclic oligonucleotide signaling pathway in type III CRISPR-Cas systems. Science 357, 605–609 (2017). (PMID: 2866343910.1126/science.aao0100) ; Niewoehner, O. et al. Type III CRISPR-Cas systems produce cyclic oligoadenylate second messengers. Nature 548, 543–548 (2017). (PMID: 2872201210.1038/nature23467) ; Rouillon, C., Athukoralage, J. S., Graham, S., Grüschow, S. & White, M. F. Control of cyclic oligoadenylate synthesis in a type III CRISPR system. eLife 7, e36734 (2018). (PMID: 29963983605330410.7554/eLife.36734) ; Makarova, K. S., Anantharaman, V., Grishin, N. V., Koonin, E. V. & Aravind, L. CARF and WYL domains: ligand-binding regulators of prokaryotic defense systems. Front. Genet. 5, 102 (2014). (PMID: 24817877401220910.3389/fgene.2014.00102) ; Rostøl, J. T. & Marraffini, L. A. Non-specific degradation of transcripts promotes plasmid clearance during type III-A CRISPR-Cas immunity. Nat. Microbiol. 4, 656–662 (2019). (PMID: 30692669643066910.1038/s41564-018-0353-x) ; Pyenson, N. C., Gayvert, K., Varble, A., Elemento, O. & Marraffini, L. A. Broad targeting specificity during bacterial type III CRISPR-Cas immunity constrains viral escape. Cell Host Microbe 22, 343–353 (2017). (PMID: 28826839559936610.1016/j.chom.2017.07.016) ; Deng, L., Garrett, R. A., Shah, S. A., Peng, X. & She, Q. A novel interference mechanism by a type IIIB CRISPR-Cmr module in Sulfolobus. Mol. Microbiol. 87, 1088–1099 (2013). (PMID: 2332056410.1111/mmi.12152) ; Jiang, W., Samai, P. & Marraffini, L. A. Degradation of phage transcripts by CRISPR-associated RNases enables type III CRISPR-Cas immunity. Cell 164, 710–721 (2016). (PMID: 26853474475287310.1016/j.cell.2015.12.053) ; Whiteley, A. T. et al. Bacterial cGAS-like enzymes synthesize diverse nucleotide signals. Nature 567, 194–199 (2019). (PMID: 30787435654437010.1038/s41586-019-0953-5) ; Maelfait, J. & Rehwinkel, J. RECONsidering sensing of cyclic dinucleotides. Immunity 46, 337–339 (2017). (PMID: 2832969710.1016/j.immuni.2017.03.005) ; Cohen, D. et al. Cyclic GMP-AMP signalling protects bacteria against viral infection. Nature 574, 691–695 (2019). (PMID: 3153312710.1038/s41586-019-1605-5) ; Athukoralage, J. S., Rouillon, C., Graham, S., Grüschow, S. & White, M. F. Ring nucleases deactivate type III CRISPR ribonucleases by degrading cyclic oligoadenylate. Nature 562, 277–280 (2018). (PMID: 30232454621970510.1038/s41586-018-0557-5) ; Borges, A. L., Davidson, A. R. & Bondy-Denomy, J. The discovery, mechanisms, and evolutionary impact of anti-CRISPRs. Annu. Rev. Virol. 4, 37–59 (2017). (PMID: 28749735603911410.1146/annurev-virology-101416-041616) ; Hwang, S. & Maxwell, K. L. Meet the anti-CRISPRs: widespread protein inhibitors of CRISPR-Cas systems. CRISPR J. 2, 23–30 (2019). (PMID: 3102123410.1089/crispr.2018.0052) ; Oke, M. et al. The Scottish structural proteomics facility: targets, methods and outputs. J. Struct. Funct. Genomics 11, 167–180 (2010). (PMID: 20419351288393010.1007/s10969-010-9090-y) ; Larson, E. T. et al. A new DNA binding protein highly conserved in diverse crenarchaeal viruses. Virology 363, 387–396 (2007). (PMID: 1733636010.1016/j.virol.2007.01.027) ; Wirth, J. F. et al. Development of a genetic system for the archaeal virus Sulfolobus turreted icosahedral virus (STIV). Virology 415, 6–11 (2011). (PMID: 2149685710.1016/j.virol.2011.03.023) ; Bautista, M. A., Zhang, C. & Whitaker, R. J. Virus-induced dormancy in the archaeon Sulfolobus islandicus. MBio 6, e02565-14 (2015). (PMID: 25827422445353710.1128/mBio.02565-14) ; Grüschow, S., Athukoralage, J. S., Graham, S., Hoogeboom, T. & White, M. F. Cyclic oligoadenylate signalling mediates Mycobacterium tuberculosis CRISPR defence. Nucleic Acids Res. 47, 9259–9270 (2019). (PMID: 31392987675508510.1093/nar/gkz676) ; Bondy-Denomy, J. et al. A unified resource for tracking anti-CRISPR names. CRISPR J. 1, 304–305 (2018). (PMID: 3102127310.1089/crispr.2018.0043) ; Auchtung, J. M., Aleksanyan, N., Bulku, A. & Berkmen, M. B. Biology of ICEBs1, an integrative and conjugative element in Bacillus subtilis. Plasmid 86, 14–25 (2016). (PMID: 2738185210.1016/j.plasmid.2016.07.001) ; Yang, W. Nucleases: diversity of structure, function and mechanism. Q. Rev. Biophys. 44, 1–93 (2011). (PMID: 2085471010.1017/S0033583510000181) ; Broo, K. S., Brive, L., Sott, R. S. & Baltzer, L. Site-selective control of the reactivity of surface-exposed histidine residues in designed four-helix-bundle catalysts. Fold. Des. 3, 303–312 (1998). (PMID: 971057610.1016/S1359-0278(98)00041-8) ; Bhoobalan-Chitty, Y., Johansen, T. B., Di Cianni, N. & Peng, X. Inhibition of type III CRISPR-Cas immunity by an archaeal virus-encoded anti-CRISPR protein. Cell 179, 448–458 (2019). (PMID: 3156445410.1016/j.cell.2019.09.003) ; Knott, G. J. et al. Broad-spectrum enzymatic inhibition of CRISPR-Cas12a. Nat. Struct. Mol. Biol. 26, 315–321 (2019). (PMID: 30936531644918910.1038/s41594-019-0208-z) ; Dong, L. et al. An anti-CRISPR protein disables type V Cas12a by acetylation. Nat. Struct. Mol. Biol. 26, 308–314 (2019). (PMID: 3093652610.1038/s41594-019-0206-1) ; Keller, J. et al. Crystal structure of AFV3-109, a highly conserved protein from crenarchaeal viruses. Virol. J. 4, 12 (2007). (PMID: 17241456179686410.1186/1743-422X-4-12) ; Anderson, R. E., Kouris, A., Seward, C. H., Campbell, K. M. & Whitaker, R. J. Structured populations of Sulfolobus acidocaldarius with susceptibility to mobile genetic elements. Genome Biol. Evol. 9, 1699–1710 (2017). (PMID: 28633403555443910.1093/gbe/evx104) ; Held, N. L., Herrera, A. & Whitaker, R. J. Reassortment of CRISPR repeat-spacer loci in Sulfolobus islandicus. Environ. Microbiol. 15, 3065–3076 (2013). (PMID: 23701169) ; Zhang, C. & Whitaker, R. J. Microhomology-mediated high-throughput gene inactivation strategy for the hyperthermophilic crenarchaeon Sulfolobus islandicus. Appl. Environ. Microbiol. 84, e02167-17 (2017). (PMID: 290304455734048) ; Zhang, C., Cooper, T. E., Krause, D. J. & Whitaker, R. J. Augmenting the genetic toolbox for Sulfolobus islandicus with a stringent positive selectable marker for agmatine prototrophy. Appl. Environ. Microbiol. 79, 5539–5549 (2013). (PMID: 23835176375417810.1128/AEM.01608-13) ; Deng, L., Zhu, H., Chen, Z., Liang, Y. X. & She, Q. Unmarked gene deletion and host-vector system for the hyperthermophilic crenarchaeon Sulfolobus islandicus. Extremophiles 13, 735–746 (2009). (PMID: 1951358410.1007/s00792-009-0254-2) ; Rouillon, C., Athukoralage, J. S., Graham, S., Grüschow, S. & White, M. F. Investigation of the cyclic oligoadenylate signaling pathway of type III CRISPR systems. Methods Enzymol. 616, 191–218 (2019). (PMID: 3069164310.1016/bs.mie.2018.10.020) ; Linkert, M. et al. Metadata matters: access to image data in the real world. J. Cell Biol. 189, 777–782 (2010). (PMID: 20513764287893810.1083/jcb.201004104) ; Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012). (PMID: 2274377210.1038/nmeth.2019) ; Sternberg, S. H., Haurwitz, R. E. & Doudna, J. A. Mechanism of substrate selection by a highly specific CRISPR endoribonuclease. RNA 18, 661–672 (2012). (PMID: 22345129331255410.1261/rna.030882.111) ; Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402 (1997). (PMID: 925469414691710.1093/nar/25.17.3389) ; Pei, J. & Grishin, N. V. PROMALS3D: multiple protein sequence alignment enhanced with evolutionary and three-dimensional structural information. Methods Mol. Biol. 1079, 263–271 (2014). (PMID: 24170408450675410.1007/978-1-62703-646-7_17) ; Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009). (PMID: 19505945271234410.1093/bioinformatics/btp348) ; Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010). (PMID: 2052563810.1093/sysbio/syq010) ; Letunic, I. & Bork, P. Interactive tree of life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 47 (W1), W256–W259 (2019). (PMID: 30931475660246810.1093/nar/gkz239) ; Winter, G. xia2: an expert system for macromolecular crystallography data reduction. J. Appl. Crystallogr. 43, 186–190 (2010). (PMID: 10.1107/S0021889809045701) ; Kabsch, W. Xds. Acta Crystallogr. D 66, 125–132 (2010). (PMID: 10.1107/S0907444909047337201246922815665) ; Evans, P. R. An introduction to data reduction: space-group determination, scaling and intensity statistics. Acta Crystallogr. D 67, 282–292 (2011). (PMID: 10.1107/S090744491003982X214604463069743) ; McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007). (PMID: 19461840248347210.1107/S0021889807021206) ; Murshudov, G. N., Vagin, A. A. & Dodson, E. J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D 53, 240–255 (1997). (PMID: 1529992610.1107/S0907444996012255) ; Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D 67, 235–242 (2011). (PMID: 2146044110.1107/S09074449100457493069738) ; Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486–501 (2010). (PMID: 2038300210.1107/S09074449100074932852313) ; Long, F. et al. AceDRG: a stereochemical description generator for ligands. Acta Crystallogr. D 73, 112–122 (2017). (PMID: 10.1107/S2059798317000067) ; Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12–21 (2010). (PMID: 10.1107/S090744490904207320057044) ; Gerlt, J. A. Genomic enzymology: web tools for leveraging protein family sequence-function space and genome context to discover novel functions. Biochemistry 56, 4293–4308 (2017). (PMID: 2882622110.1021/acs.biochem.7b00614) Grant Information: BB/G011400/1 United Kingdom BB_ Biotechnology and Biological Sciences Research Council; BB/R008035/1 United Kingdom BB_ Biotechnology and Biological Sciences Research Council; BB/S000313/1 United Kingdom BB_ Biotechnology and Biological Sciences Research Council Substance Nomenclature: 0 (Adenine Nucleotides) ; 0 (CRISPR-Associated Proteins) ; 0 (DNA, Viral) ; 0 (Nucleotides, Cyclic) ; 0 (Oligoribonucleotides) ; 0 (Viral Proteins) ; 61172-40-5 (2',5'-oligoadenylate) ; EC 3.1.- (Endonucleases) Entry Date(s): Date Created: 20200117 Date Completed: 20200507 Latest Revision: 20220715 Update Code: 20240513 PubMed Central ID: PMC6986909

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An anti-CRISPR viral ring nuclease subverts type III CRISPR immunity.