Phage anti-CBASS and anti-Pycsar nucleases subvert bacterial immunity

Hobbs, Samuel J.; Wein, Tanita; Lu, Allen; Morehouse, Benjamin R.; Schnabel, Julia; Leavitt, Azita; Yirmiya, Erez; Sorek, Rotem; Kranzusch, Philip J.

doi:10.1038/s41586-022-04716-y

Phage anti-CBASS and anti-Pycsar nucleases subvert bacterial immunity

Journal Article · 01 April 2022 · Nature

DOI:https://doi.org/10.1038/s41586-022-04716-y· OSTI ID:1870906

Hobbs, Samuel J.; Wein, Tanita; Lu, Allen; Morehouse, Benjamin R.; Schnabel, Julia; Leavitt, Azita; Yirmiya, Erez; Sorek, Rotem; Kranzusch, Philip J.

Research Organization:: Advanced Photon Source (APS), Argonne National Laboratory (ANL), Argonne, IL (US)

Sponsoring Organization:: DOE - Office Of Science; FOREIGN; NIH

OSTI ID:: 1870906

Journal Information:: Nature, Journal Name: Nature Vol. 605

Country of Publication:: United States

Language:: ENGLISH

References (51)

Cyclic di-AMP Signaling in Bacteria Stülke, Jörg; Krüger, Larissa Annual Review of Microbiology, Vol. 74, Issue 1 https://doi.org/10.1146/annurev-micro-020518-115943	journal	September 2020
Cyclic di-GMP: second messenger extraordinaire Jenal, Urs; Reinders, Alberto; Lori, Christian Nature Reviews Microbiology, Vol. 15, Issue 5 https://doi.org/10.1038/nrmicro.2016.190	journal	February 2017
Exclusion of Glucosyl-Hydroxymethylcytosine DNA Containing Bacteriophages Is Overcome by the Injected Protein Inhibitor IPI* Bair, Catherine L.; Rifat, Dalin; Black, Lindsay W. Journal of Molecular Biology, Vol. 366, Issue 3 https://doi.org/10.1016/j.jmb.2006.11.049	journal	February 2007
Structures and Strategies of Anti-CRISPR-Mediated Immune Suppression Wiegand, Tanner; Karambelkar, Shweta; Bondy-Denomy, Joseph Annual Review of Microbiology, Vol. 74, Issue 1 https://doi.org/10.1146/annurev-micro-020518-120107	journal	September 2020
3?,5?-Cyclic nucleotide phosphodiesterases class III: Members, structure, and catalytic mechanism Richter, Wito Proteins: Structure, Function, and Genetics, Vol. 46, Issue 3 https://doi.org/10.1002/prot.10049	journal	January 2002
Biology of DNA restriction. Bickle, T. A.; Krüger, D. H. Microbiological Reviews, Vol. 57, Issue 2 https://doi.org/10.1128/mr.57.2.434-450.1993	journal	January 1993
Ancient Origin of cGAS-STING Reveals Mechanism of Universal 2′,3′ cGAMP Signaling Kranzusch, Philip J.; Wilson, Stephen C.; Lee, Amy S. Y. Molecular Cell, Vol. 59, Issue 6 https://doi.org/10.1016/j.molcel.2015.07.022	journal	September 2015
Viral and metazoan poxins are cGAMP-specific nucleases that restrict cGAS–STING signalling Eaglesham, James B.; Pan, Youdong; Kupper, Thomas S. Nature, Vol. 566, Issue 7743 https://doi.org/10.1038/s41586-019-0928-6	journal	February 2019
Structure-based functional mechanisms and biotechnology applications of anti-CRISPR proteins Jia, Ning; Patel, Dinshaw J. Nature Reviews Molecular Cell Biology, Vol. 22, Issue 8 https://doi.org/10.1038/s41580-021-00371-9	journal	June 2021
Dual Specificity and Novel Structural Folding of Yeast Phosphodiesterase-1 for Hydrolysis of Second Messengers Cyclic Adenosine and Guanosine 3′,5′-Monophosphate Tian, Yuanyuan; Cui, Wenjun; Huang, Manna Biochemistry, Vol. 53, Issue 30 https://doi.org/10.1021/bi500406h	journal	July 2014
A cyclic oligonucleotide signaling pathway in type III CRISPR-Cas systems Kazlauskiene, Migle; Kostiuk, Georgij; Venclovas, Česlovas Science, Vol. 357, Issue 6351 https://doi.org/10.1126/science.aao0100	journal	June 2017
Molecular basis for the specific recognition of the metazoan cyclic GMP-AMP by the innate immune adaptor protein STING Shi, Heping; Wu, Jiaxi; Chen, Zhijian J. Proceedings of the National Academy of Sciences, Vol. 112, Issue 29 https://doi.org/10.1073/pnas.1507317112	journal	July 2015
Systematic discovery of antiphage defense systems in the microbial pangenome Doron, Shany; Melamed, Sarah; Ofir, Gal Science, Vol. 359, Issue 6379 https://doi.org/10.1126/science.aar4120	journal	January 2018
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
progressiveMauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement Darling, Aaron E.; Mau, Bob; Perna, Nicole T. PLoS ONE, Vol. 5, Issue 6 https://doi.org/10.1371/journal.pone.0011147	journal	June 2010
Global indicators of X-ray data quality Weiss, Manfred S. Journal of Applied Crystallography, Vol. 34, Issue 2 https://doi.org/10.1107/S0021889800018227	journal	April 2001
Cutadapt removes adapter sequences from high-throughput sequencing reads Martin, Marcel EMBnet.journal, Vol. 17, Issue 1 https://doi.org/10.14806/ej.17.1.200	journal	May 2011
A phage-encoded anti-CRISPR enables complete evasion of type VI-A CRISPR-Cas immunity Meeske, Alexander J.; Jia, Ning; Cassel, Alice K. Science, Vol. 369, Issue 6499 https://doi.org/10.1126/science.abb6151	journal	July 2020
The arms race between bacteria and their phage foes Hampton, Hannah G.; Watson, Bridget N. J.; Fineran, Peter C. Nature, Vol. 577, Issue 7790 https://doi.org/10.1038/s41586-019-1894-8	journal	January 2020
Linking Crystallographic Model and Data Quality Karplus, P. A.; Diederichs, K. Science, Vol. 336, Issue 6084 https://doi.org/10.1126/science.1218231	journal	May 2012
Discovery of multiple anti-CRISPRs highlights anti-defense gene clustering in mobile genetic elements Pinilla-Redondo, Rafael; Shehreen, Saadlee; Marino, Nicole D. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-19415-3	journal	November 2020
Bacterial cGAS-like enzymes synthesize diverse nucleotide signals Whiteley, Aaron T.; Eaglesham, James B.; de Oliveira Mann, Carina C. Nature, Vol. 567, Issue 7747 https://doi.org/10.1038/s41586-019-0953-5	journal	February 2019
Phage-Encoded Anti-CRISPR Defenses Stanley, Sabrina Y.; Maxwell, Karen L. Annual Review of Genetics, Vol. 52, Issue 1 https://doi.org/10.1146/annurev-genet-120417-031321	journal	November 2018
Structure Reveals Mechanisms of Viral Suppressors that Intercept a CRISPR RNA-Guided Surveillance Complex Chowdhury, Saikat; Carter, Joshua; Rollins, MaryClare F. Cell, Vol. 169, Issue 1 https://doi.org/10.1016/j.cell.2017.03.012	journal	March 2017
Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix Liebschner, Dorothee; Afonine, Pavel V.; Baker, Matthew L. Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 10 https://doi.org/10.1107/S2059798319011471	journal	October 2019
Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 49, Issue W1 https://doi.org/10.1093/nar/gkab301	journal	April 2021
CBASS Immunity Uses CARF-Related Effectors to Sense 3′–5′- and 2′–5′-Linked Cyclic Oligonucleotide Signals and Protect Bacteria from Phage Infection Lowey, Brianna; Whiteley, Aaron T.; Keszei, Alexander F. A. Cell, Vol. 182, Issue 1 https://doi.org/10.1016/j.cell.2020.05.019	journal	July 2020
W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis Trifinopoulos, Jana; Nguyen, Lam-Tung; von Haeseler, Arndt Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw256	journal	April 2016
A Rapid Bacteriophage DNA Extraction Method Jakočiūnė, Džiuginta; Moodley, Arshnee Methods and Protocols, Vol. 1, Issue 3 https://doi.org/10.3390/mps1030027	journal	July 2018
Type III CRISPR–Cas systems produce cyclic oligoadenylate second messengers Niewoehner, Ole; Garcia-Doval, Carmela; Rostøl, Jakob T. Nature, Vol. 548, Issue 7669 https://doi.org/10.1038/nature23467	journal	July 2017
Structural and biochemical analyses of the metallo-β-lactamase fold protein YhfI from Bacillus subtilis Na, Hye-won; Namgung, Byeol; Song, Wan Seok Biochemical and Biophysical Research Communications, Vol. 519, Issue 1 https://doi.org/10.1016/j.bbrc.2019.08.106	journal	October 2019
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
Cyclic GMP–AMP signalling protects bacteria against viral infection Cohen, Daniel; Melamed, Sarah; Millman, Adi Nature, Vol. 574, Issue 7780 https://doi.org/10.1038/s41586-019-1605-5	journal	September 2019
An anti-CRISPR viral ring nuclease subverts type III CRISPR immunity Athukoralage, Januka S.; McMahon, Stephen A.; Zhang, Changyi Nature, Vol. 577, Issue 7791 https://doi.org/10.1038/s41586-019-1909-5	journal	January 2020
Molecular mechanisms of the CdnG-Cap5 antiphage defense system employing 3′,2′-cGAMP as the second messenger Fatma, Shirin; Chakravarti, Arpita; Zeng, Xuankun Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-26738-2	journal	November 2021
Assembling Single-Cell Genomes and Mini-Metagenomes From Chimeric MDA Products Nurk, Sergey; Bankevich, Anton; Antipov, Dmitry Journal of Computational Biology, Vol. 20, Issue 10 https://doi.org/10.1089/cmb.2013.0084	journal	October 2013
cGAS-like receptors sense RNA and control 3′2′-cGAMP signalling in Drosophila Slavik, Kailey M.; Morehouse, Benjamin R.; Ragucci, Adelyn E. Nature, Vol. 597, Issue 7874 https://doi.org/10.1038/s41586-021-03743-5	journal	July 2021
Effector-mediated membrane disruption controls cell death in CBASS antiphage defense Duncan-Lowey, Brianna; McNamara-Bordewick, Nora K.; Tal, Nitzan Molecular Cell, Vol. 81, Issue 24 https://doi.org/10.1016/j.molcel.2021.10.020	journal	December 2021
Direct activation of a phospholipase by cyclic GMP-AMP in El Tor Vibrio cholerae Severin, Geoffrey B.; Ramliden, Miriam S.; Hawver, Lisa A. Proceedings of the National Academy of Sciences, Vol. 115, Issue 26 https://doi.org/10.1073/pnas.1801233115	journal	June 2018
Cyclic CMP and cyclic UMP mediate bacterial immunity against phages Tal, Nitzan; Morehouse, Benjamin R.; Millman, Adi Cell, Vol. 184, Issue 23 https://doi.org/10.1016/j.cell.2021.09.031	journal	November 2021
Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system Bondy-Denomy, Joe; Pawluk, April; Maxwell, Karen L. Nature, Vol. 493, Issue 7432 https://doi.org/10.1038/nature11723	journal	December 2012
The dynamic interplay of host and viral enzymes in type III CRISPR-mediated cyclic nucleotide signalling Athukoralage, Januka S.; Graham, Shirley; Rouillon, Christophe eLife, Vol. 9 https://doi.org/10.7554/eLife.55852	journal	April 2020
Structure and Mechanism of a Cyclic Trinucleotide-Activated Bacterial Endonuclease Mediating Bacteriophage Immunity Lau, Rebecca K.; Ye, Qiaozhen; Birkholz, Erica A. Molecular Cell, Vol. 77, Issue 4 https://doi.org/10.1016/j.molcel.2019.12.010	journal	February 2020
Structure of the Human cGAS–DNA Complex Reveals Enhanced Control of Immune Surveillance Zhou, Wen; Whiteley, Aaron T.; de Oliveira Mann, Carina C. Cell, Vol. 174, Issue 2 https://doi.org/10.1016/j.cell.2018.06.026	journal	July 2018
STING cyclic dinucleotide sensing originated in bacteria Morehouse, Benjamin R.; Govande, Apurva A.; Millman, Adi Nature, Vol. 586, Issue 7829 https://doi.org/10.1038/s41586-020-2719-5	journal	September 2020
A Completely Reimplemented MPI Bioinformatics Toolkit with a New HHpred Server at its Core Zimmermann, Lukas; Stephens, Andrew; Nam, Seung-Zin Journal of Molecular Biology, Vol. 430, Issue 15 https://doi.org/10.1016/j.jmb.2017.12.007	journal	July 2018
Daughter cell separation is controlled by cytokinetic ring-activated cell wall hydrolysis Uehara, Tsuyoshi; Parzych, Katherine R.; Dinh, Thuy The EMBO Journal, Vol. 29, Issue 8 https://doi.org/10.1038/emboj.2010.36	journal	March 2010
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
Inexpensive Multiplexed Library Preparation for Megabase-Sized Genomes Baym, Michael; Kryazhimskiy, Sergey; Lieberman, Tami D. PLOS ONE, Vol. 10, Issue 5 https://doi.org/10.1371/journal.pone.0128036	journal	May 2015
Engineering of Bacteriophage T4 Genome Using CRISPR-Cas9 Tao, Pan; Wu, Xiaorong; Tang, Wei-Chun ACS Synthetic Biology, Vol. 6, Issue 10 https://doi.org/10.1021/acssynbio.7b00179	journal	July 2017
Bacteriophage exclusion, a new defense system Barrangou, Rodolphe; van der Oost, John The EMBO Journal, Vol. 34, Issue 2 https://doi.org/10.15252/embj.201490620	journal	December 2014

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