TAC–TIC, a high-throughput genetics method to identify triggers or blockers of bacterial toxin–antitoxin systems

Jacob Bobonis, Alessio Ling Jie Yang, Carlos Geert Pieter Voogdt, Athanasios Typas

Published: 2024-05-09 DOI: 10.1038/s41596-024-00988-y

Toxin-Antitoxin Systems

TAC-TIC

Gene Overexpression

Bacterial Immunity

Phage-Defending Retron-TAs

AI 解读

Deoxyfluorination of phenols for chemoselective18F-labeling of peptides

Stable isotope tracing to assess tumor metabolism in vivo

Measuring DNA modifications with the comet assay: a compendium of protocols

Detect-seq, a chemical labeling and biotin pull-down approach for the unbiased and genome-wide off-target evaluation of programmable cytosine base editors

A systems-level mass spectrometry-based technique for accurate and sensitive quantification of the RNA cap epitranscriptome

Spooling electrochemiluminescence spectroscopy: development, applications and beyond

Chronic, cortex-wide imaging of specific cell populations during behavior

Chromatin accessibility profiling by ATAC-seq

Global analysis of RNA-binding protein dynamics by comparative and enhanced RNA interactome capture

Pooled genetic perturbation screens with image-based phenotypes

查看全部

Sections

Figures

References

Song, S. & Wood, T. K. A primary physiological role of toxin/antitoxin systems is phage inhibition. Front. Microbiol. 11, 1895 (2020).
LeRoux, M. & Laub, M. T. Toxin–antitoxin systems as phage defense elements. Annu. Rev. Microbiol. 76, 21–43 (2022).
Tal, N. & Sorek, R. SnapShot: bacterial immunity. Cell 185, 578–578.e1 (2022).
Bobonis, J. et al. Bacterial retrons encode phage-defending tripartite toxin–antitoxin systems. Nature 609, 144–150 (2022).
Harms, A., Brodersen, D. E., Mitarai, N. & Gerdes, K. Toxins, targets, and triggers: an overview of toxin–antitoxin biology. Mol. Cell 70, 768–784 (2018).
Fraikin, N., Goormaghtigh, F. & Van Melderen, L. Type II toxin–antitoxin systems: evolution and revolutions. J. Bacteriol. 202, e00763–19 (2020).
Fineran, P. C. et al. The phage abortive infection system, ToxIN, functions as a protein–RNA toxin–antitoxin pair. Proc. Natl Acad. Sci. USA 106, 894–899 (2009).
Otsuka, Y. & Yonesaki, T. Dmd of bacteriophage T4 functions as an antitoxin against Escherichia coli LsoA and RnlA toxins. Mol. Microbiol. 83, 669–681 (2012).
Sberro, H. et al. Discovery of functional toxin/antitoxin systems in bacteria by shotgun cloning. Mol. Cell 50, 136–148 (2013).
Lopatina, A., Tal, N. & Sorek, R. Abortive infection: bacterial suicide as an antiviral immune strategy. Annu. Rev. Virol. 7, 371–384 (2020).
Vassallo, C. N., Doering, C. R., Littlehale, M. L., Teodoro, G. I. C. & Laub, M. T. A functional selection reveals previously undetected anti-phage defence systems in the E. coli pangenome. Nat. Microbiol. 7, 1568–1579 (2022).
Millman, A. et al. An expanded arsenal of immune systems that protect bacteria from phages. Cell Host Microbe 30, 1556–1569.e5 (2022).
Jaskólska, M., Adams, D. W. & Blokesch, M. Two defence systems eliminate plasmids from seventh pandemic Vibrio cholerae. Nature 604, 323–329 (2022).
Millman, A. et al. Bacterial retrons function in anti-phage defense. Cell 183, 1551–1561.e12 (2020).
Gao, L. et al. Diverse enzymatic activities mediate antiviral immunity in prokaryotes. Science 369, 1077–1084 (2020).
Samson, J. E., Magadán, A. H., Sabri, M. & Moineau, S. Revenge of the phages: defeating bacterial defences. Nat. Rev. Microbiol. 11, 675–687 (2013).
Jurėnas, D., Fraikin, N., Goormaghtigh, F. & Van Melderen, L. Biology and evolution of bacterial toxin–antitoxin systems. Nat. Rev. Microbiol. 20, 335–350 (2022).
Schubert, M. G. et al. High-throughput functional variant screens via in vivo production of single-stranded DNA. Proc. Natl Acad. Sci. USA 118, 1–10 (2021).
Farzadfard, F., Gharaei, N., Citorik, R. J. & Lu, T. K. Efficient retroelement-mediated DNA writing in bacteria. Cell Syst. 12, 860–872.e5 (2021).
Lopez, S. C., Crawford, K. D., Lear, S. K., Bhattarai-Kline, S. & Shipman, S. L. Precise genome editing across kingdoms of life using retron-derived DNA. Nat. Chem. Biol. 18, 199–206 (2022).
Mestre, M. R., González-Delgado, A., Gutiérrez-Rus, L. I., Martínez-Abarca, F. & Toro, N. Systematic prediction of genes functionally associated with bacterial retrons and classification of the encoded tripartite systems. Nucleic Acids Res. 48, 12632–12647 (2020).
Saka, K. A complete set of escherichia coli open reading frames in mobile plasmids facilitating genetic studies. DNA Res. 12, 63–68 (2005).
Otsuka, Y. et al. GenoBase: Comprehensive resource database of Escherichia coli K-12. Nucleic Acids Res. 43, D606–D617 (2015).
Depardieu, F. et al. A eukaryotic-like serine/threonine kinase protects Staphylococci against phages. Cell Host Microbe 20, 471–481 (2016).
Snyder, L. & McWilliams, K. The rex genes of bacteriophage lambda can inhibit cell function without phage superinfection. Gene 81, 17–24 (1989).
Meeske, A. J., Nakandakari-Higa, S. & Marraffini, L. A. Cas13-induced cellular dormancy prevents the rise of CRISPR-resistant bacteriophage. Nature 570, 241–245 (2019).
Stokar-Avihail, A. et al. Discovery of phage determinants that confer sensitivity to bacterial immune systems. Cell 186, 1863–1876.e16 (2023).
Zhang, T. et al. Direct activation of a bacterial innate immune system by a viral capsid protein. Nature 612, 132–140 (2022).
Maier, L. et al. Extensive impact of non-antibiotic drugs on human gut bacteria. Nature 555, 623–628 (2018).
Paradis-Bleau, C., Kritikos, G., Orlova, K., Typas, A. & Bernhardt, T. G. A genome-wide screen for bacterial envelope biogenesis mutants identifies a novel factor involved in cell wall precursor metabolism. PLoS Genet. 10, e1004056 (2014).
Gao, L. A. et al. Prokaryotic innate immunity through pattern recognition of conserved viral proteins. Science 377, eabm4096 (2022).
Amitsur, M., Levitz, R. & Kaufmann, G. Bacteriophage T4 anticodon nuclease, polynucleotide kinase and RNA ligase reprocess the host lysine tRNA. EMBO J. 6, 2499–2503 (1987).
Ferrières, L. et al. Silent mischief: bacteriophage Mu insertions contaminate products of Escherichia coli random mutagenesis performed using suicidal transposon delivery plasmids mobilized by broad-host-range RP4 conjugative machinery. J. Bacteriol. 192, 6418–6427 (2010).
Simon, R., Priefer, U. & Pühler, A. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Nat. Biotechnol. 1, 784–791 (1983).
Thomason, L. C., Costantino, N. & Court, D. L. E. coli genome manipulation by P1 transduction. Curr. Protoc. Mol. Biol. 79, 1–8 (2007).
Sharan, S. K., Thomason, L. C., Kuznetsov, S. G. & Court, D. L. Recombineering: a homologous recombination-based method of genetic engineering. Nat. Protoc. 4, 206–223 (2009).
Shiver, A. L., Culver, R., Deutschbauer, A. M. & Huang, K. C. Rapid ordering of barcoded transposon insertion libraries of anaerobic bacteria. Nat. Protoc. 16, 3049–3071 (2021).
Engler, C., Kandzia, R. & Marillonnet, S. A one pot, one step, precision cloning method with high throughput capability. PLoS ONE 3, e3647 (2008).
Yong, H. T. et al. Development of a system for discovery of genetic interactions for essential genes in Escherichia coli K-12. Genes Genet. Syst. 88, 233–240 (2013).
Babic, A., Guérout, A.-M. & Mazel, D. Construction of an improved RP4 (RK2)-based conjugative system. Res. Microbiol. 159, 545–549 (2008).
Haase, J., Lurz, R., Grahn, A. M., Bamford, D. H. & Lanka, E. Bacterial conjugation mediated by plasmid RP4: RSF1010 mobilization, donor-specific phage propagation, and pilus production require the same Tra2 core components of a proposed DNA transport complex. J. Bacteriol. 177, 4779–4791 (1995).
Jahn, M., Vorpahl, C., Hübschmann, T., Harms, H. & Müller, S. Copy number variability of expression plasmids determined by cell sorting and droplet digital PCR. Microb. Cell Fact. 15, 211 (2016).
Guzman, L. M., Belin, D., Carson, M. J. & Beckwith, J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose P(BAD) promoter. J. Bacteriol. 177, 4121–4130 (1995).
Baba, T. et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2, 2006:2–2006.0008 (2006).
Kritikos, G. et al. A tool named Iris for versatile high-throughput phenotyping in microorganisms. Nat. Microbiol. 2, 17014 (2017).
Chung, C. T., Niemela, S. L. & Miller, R. H. One-step preparation of competent Escherichia coli: transformation and storage of bacterial cells in the same solution. Proc. Natl Acad. Sci. USA 86, 2172–2175 (1989).
Doherty, H. M., Kritikos, G., Galardini, M., Banzhaf, M. & Moradigaravand, D. ChemGAPP: a tool for chemical genomics analysis and phenotypic profiling. Bioinformatics 39, 2023.01.05.522861 (2023).

TAC–TIC, a high-throughput genetics method to identify triggers or blockers of bacterial toxin–antitoxin systems

Extended

Supplementary information

推荐阅读