crRNA complementarity shifts endogenous CRISPR-Cas systems between transcriptional repression and DNA defense

References

• Barrangou R, Fremaux C, Deveau H, et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science. 2007;315(5819):1709–1712.
   PubMed Web of Science ®Google Scholar
• Marraffini LA, Sontheimer EJ. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science. 2008;322(5909):1843–1845.
   PubMed Web of Science ®Google Scholar
• Koonin EV, Makarova KS, Zhang F Diversity, classification and evolution of CRISPR-Cas systems. Curr Opin Microbiol. 2017;37:67–78.
   PubMed Web of Science ®Google Scholar
• Makarova KS, Wolf YI, Iranzo J, et al. Evolutionary classification of CRISPR–Cas systems: a burst of class 2 and derived variants. Nature Rev Microbiol. 2020;18(2):67–83.
   PubMed Web of Science ®Google Scholar
• Ratner HK, Weiss DS. Overview of CRISPR-Cas9 Biology. In: Doudna JAMP, editor. CRISPR-Cas: A laboratory manual. Cold Spring Harbor, New York: Cold Spring Harbor Press; 2016. (12):1025–1038.
   Google Scholar
• Jinek M, Chylinski K, Fonfara I, et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science. 2012;337(6096):816–821.
   PubMed Web of Science ®Google Scholar
• Gasiunas G, Barrangou R, Horvath P, et al. Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci U S A. 2012;109(39):E2579–86.
   PubMed Web of Science ®Google Scholar
• Zetsche B, Gootenberg JS, Abudayyeh OO, et al. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell. 2015;163(3):759–771.
   PubMed Web of Science ®Google Scholar
• Shmakov S, Smargon A, Scott D, et al. Diversity and evolution of class 2 CRISPR-Cas systems. Nat Rev Microbiol. 2017;15(3):169–182.
   PubMed Web of Science ®Google Scholar
• Yan WX, Hunnewell P, Alfonse LE, et al. Functionally diverse type V CRISPR-Cas systems. Science. 2019;363(6422):88–91.
   PubMed Web of Science ®Google Scholar
• Yao R, Liu D, Jia X, et al. Cas9/Cas12a biotechnology and application in bacteria. Synth Syst Biotechnol. 2018;3(3):135–149.
   PubMed Web of Science ®Google Scholar
• Wu WY, Lebbink JHG, Kanaar R, van der Oost J. et al., Genome editing by natural and engineered CRISPR-associated nucleases. Nat Chem Biol. 2018;14(7):642–651.
   PubMed Web of Science ®Google Scholar
• Swarts DC, Jinek M. Cas9 versus Cas12a/Cpf1: structure-function comparisons and implications for genome editing. Wiley Interdiscip Rev RNA 2018:e1481. 9 5
   PubMed Web of Science ®Google Scholar
• Liao C, Slotkowski RA, Achmedov T, et al. The Francisella novicida Cas12a is sensitive to the structure downstream of the terminal repeat in CRISPR arrays. RNA Biol. 2019;16(4):404–412.
   PubMed Web of Science ®Google Scholar
• Schunder E, Rydzewski K, Grunow R, et al. First indication for a functional CRISPR/Cas system in Francisella tularensis. Int J Med Microbiol. 2013;303(2):51–60.
   PubMed Web of Science ®Google Scholar
• Fonfara I, Le Rhun A, Chylinski K, et al. Phylogeny of Cas9 determines functional exchangeability of dual-RNA and Cas9 among orthologous type II CRISPR-Cas systems. Nucleic Acids Res. 2014;42(4):2577–2590.
   PubMed Web of Science ®Google Scholar
• Ratner HK, Weiss DS. Francisella novicida CRISPR-Cas systems can functionally complement each other in DNA defense while providing target flexibility. J Bacteriol. 2020. 202 12 10.1128/JB.00670-19
   PubMedGoogle Scholar
• Chylinski K, Le Rhun A, Charpentier E. The tracrRNA and Cas9 families of type II CRISPR-Cas immunity systems. RNA Biol. 2013;10(5):726–737.
   PubMed Web of Science ®Google Scholar
• Deltcheva E, Chylinski K, Sharma CM, et al. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature. 2011;471(7340):602–607.
   PubMed Web of Science ®Google Scholar
• Stern A, Keren L, Wurtzel O, et al. Self-targeting by CRISPR: gene regulation or autoimmunity? Trends Genet. 2010;26(8):335–340.
   PubMed Web of Science ®Google Scholar
• Sapranauskas R, Gasiunas G, Fremaux C, et al. The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Res. 2011;39(21):9275–9282.
   PubMed Web of Science ®Google Scholar
• Deveau H, Barrangou R, Garneau JE, et al. Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J Bacteriol. 2008;190(4):1390–1400.
   PubMed Web of Science ®Google Scholar
• Mojica FJ, Diez-Villasenor C, Garcia-Martinez J, et al. Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology. 2009;155(Pt 3):733–740.
   PubMed Web of Science ®Google Scholar
• Westra ER, van Erp PB, Kunne T, et al. CRISPR immunity relies on the consecutive binding and degradation of negatively supercoiled invader DNA by Cascade and Cas3. Mol Cell. 2012;46(5):595–605.
   PubMed Web of Science ®Google Scholar
• Shah SA, Erdmann S, Mojica FJM, et al. Protospacer recognition motifs: mixed identities and functional diversity. RNA Biol. 2013;10(5):891–899.
   PubMed Web of Science ®Google Scholar
• Marraffini LA, Sontheimer EJ. Self versus non-self discrimination during CRISPR RNA-directed immunity. Nature. 2010;463(7280):568–571.
   PubMed Web of Science ®Google Scholar
• Vercoe RB, Chang JT, Dy RL, et al. Cytotoxic chromosomal targeting by CRISPR/Cas systems can reshape bacterial genomes and expel or remodel pathogenicity islands. PLoS Genet. 2013;9(4):e1003454.
   PubMed Web of Science ®Google Scholar
• Sampson TR, Saroj SD, Llewellyn AC, et al. A CRISPR/Cas system mediates bacterial innate immune evasion and virulence. Nature. 2013;497(7448):254–257.
   PubMed Web of Science ®Google Scholar
• Ratner HK, Escalera-Maurer A, Le Rhun A, et al. Catalytically active Cas9 mediates transcriptional interference to facilitate bacterial virulence. Mol Cell. 2019;75(3):498–510.e5.
   PubMed Web of Science ®Google Scholar
• Jones CL, Sampson TR, Nakaya HI, et al. Repression of bacterial lipoprotein production by Francisella novicida facilitates evasion of innate immune recognition. Cell Microbiol. 2012;14(10):1531–1543.
   PubMed Web of Science ®Google Scholar
• Ma K, Cao Q, Luo S, et al. Cas9 enhances bacterial virulence by repressing the regR transcriptional regulator in streptococcusagalactiae. Infect Immun 2018;86(3). 3
   Web of Science ®Google Scholar
• Louwen R, Horst-Kreft D, de Boer AG, et al. A novel link between Campylobacter jejuni bacteriophage defence, virulence and Guillain-Barre syndrome. Eur J Clin Microbiol Infect Dis. 2013;32(2):207–226.
   PubMed Web of Science ®Google Scholar
• Guzina J, Chen WH, Stankovic T, et al. In silico analysis suggests common appearance of scaRNAs in type II systems and their association with bacterial virulence. Front Genet 2018;9:474.
   PubMed Web of Science ®Google Scholar
• Ratner HK, Sampson TR, Weiss DS. I can see CRISPR now, even when phage are gone: a view on alternative CRISPR-Cas functions from the prokaryotic envelope. Curr Opin Infect Dis. 2015;28(3):267–274.
   PubMed Web of Science ®Google Scholar
• Spencer BL, Deng L, Patras KA, et al. Cas9 contributes to group B streptococcal colonization and disease. Front Microbiol 2019;10:1930.
   PubMed Web of Science ®Google Scholar
• Gao NJ, Al-Bassam MM, Poudel S, et al. Functional and proteomic analysis of Streptococcus pyogenes virulence upon loss of its native Cas9 nuclease. Front Microbiol 2019;10(1967).
   PubMed Web of Science ®Google Scholar
• Bikard D, Marraffini LA Control of gene expression by CRISPR-Cas systems. F1000prime Reports. 2013;5:47.
   PubMedGoogle Scholar
• Wimmer F, Beisel CL CRISPR-Cas systems and the paradox of self-targeting spacers. Front Microbiol 2020;10:3078.
   PubMed Web of Science ®Google Scholar
• Heussler GE, O’Toole GA. Friendly fire: biological functions and consequences of chromosomal targeting by CRISPR-Cas systems. J Bacteriol. 2016;198(10):1481–1486.
   PubMed Web of Science ®Google Scholar
• Sternberg SH, LaFrance B, Kaplan M, et al. Conformational control of DNA target cleavage by CRISPR-Cas9. Nature. 2015;527(7576):110–113.
   PubMed Web of Science ®Google Scholar
• Bikard D, Jiang W, Samai P, et al. Programmable repression and activation of bacterial gene expression using an engineered CRISPR-Cas system. Nucleic Acids Res. 2013;41(15):7429–7437.
   PubMed Web of Science ®Google Scholar
• Fu Y, Sander JD, Reyon D, et al. Cas nuclease specificity using truncated guide RNAs. Nat Biotechnol. 2014;32(3):279–284.
   PubMed Web of Science ®Google Scholar
• Kiani S, Chavez A, Tuttle M, et al. Cas9 gRNA engineering for genome editing, activation and repression. Nat Methods. 2015;12(11):1051–1054.
   PubMed Web of Science ®Google Scholar
• Wu X, Scott DA, Kriz AJ, et al. Genome-wide binding of the CRISPR endonuclease Cas9 in mammalian cells. Nat Biotechnol. 2014;32(7):670–676.
   PubMed Web of Science ®Google Scholar
• Breinig M, Schweitzer AY, Herianto AM, et al. Multiplexed orthogonal genome editing and transcriptional activation by Cas12a. Nat Methods. 2019;16(1):51–54.
   PubMed Web of Science ®Google Scholar
• McWhinnie RL, Nano FE. Synthetic promoters functional in Francisella novicida and Escherichia coli. Appl Environ Microbiol. 2014;80(1):226–234.
   PubMed Web of Science ®Google Scholar
• Fonfara I, Richter H, Bratovič M, et al. The CRISPR-associated DNA-cleaving enzyme Cpf1 also processes precursor CRISPR RNA. Nature. 2016;532(7600):517–521.
   PubMed Web of Science ®Google Scholar
• Zetsche B, Heidenreich M, Mohanraju P, et al. Multiplex gene editing by CRISPR-Cpf1 using a single crRNA array. Nat Biotechnol. 2017;35(1):31–34.
   PubMed Web of Science ®Google Scholar
• Dugar G, Leenay RT, Eisenbart SK, et al. CRISPR RNA-dependent binding and cleavage of endogenous RNAs by the Campylobacter jejuni Cas9. Mol Cell. 2018;69(5):893–905.e7.
   PubMed Web of Science ®Google Scholar
• Strutt SC, Torrez RM, Kaya E, et al. RNA-dependent RNA targeting by CRISPR-Cas9. Elife. 2018;7. 10.7554/eLife.32724
   Web of Science ®Google Scholar
• Rousseau BA, Hou Z, Gramelspacher MJ, et al. Programmable RNA cleavage and recognition by a natural CRISPR-Cas9 system from Neisseria meningitidis. Mol Cell. 2018;69(5):906–14.e4.
   PubMed Web of Science ®Google Scholar
• Bozic B, Repac J, Djordjevic M. Endogenous gene regulation as a predicted main function of type I-E CRISPR/Cas system in E. Coli. Molecules. 2019;24(4).
   Web of Science ®Google Scholar
• Luo ML, Jackson RN, Denny SR, et al. The CRISPR RNA-guided surveillance complex in Escherichia coli accommodates extended RNA spacers. Nucleic Acids Res. 2016;44(15):7385–7394.
   PubMed Web of Science ®Google Scholar
• Li R, Fang L, Tan S, et al. Type I CRISPR-Cas targets endogenous genes and regulates virulence to evade mammalian host immunity. Cell Res. 2016;26(12):1273–1287.
   PubMed Web of Science ®Google Scholar
• Heussler GE, Cady KC, Koeppen K, et al. Clustered regularly interspaced short palindromic repeat-dependent, biofilm-specific death of Pseudomonas aeruginosa mediated by increased expression of phage-related genes. MBio. 2015;6(3):e00129–15.
   PubMed Web of Science ®Google Scholar
• Zhang F, Zhao S, Ren C, et al. CRISPRminer is a knowledge base for exploring CRISPR-Cas systems in microbe and phage interactions. Commun Biol. 2018;1(1):180.
   PubMedGoogle Scholar
• Shmakov SA, Sitnik V, Makarova KS, et al. The CRISPR spacer space is dominated by sequences from species-specific mobilomes. mBio. 2017;8(5):e01397–17.
   PubMed Web of Science ®Google Scholar
• Almendros C, Guzmán NM, García-Martínez J, et al. Anti-cas spacers in orphan CRISPR4 arrays prevent uptake of active CRISPR–Cas I-F systems. Nat Microbiol. 2016;1(8):16081.
   PubMed Web of Science ®Google Scholar
• Milicevic O, Repac J, Bozic B, et al. A simple criterion for inferring CRISPR array direction. Front Microbiol 2019;10(2054).
   PubMed Web of Science ®Google Scholar
• Biswas A, Staals RHJ, Morales SE, et al. CRISPRDetect: A flexible algorithm to define CRISPR arrays. BMC Genomics. 2016;17(1):356.
   PubMedGoogle Scholar
• Couvin D, Bernheim A, Toffano-Nioche C, et al. CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins. Nucleic Acids Res. 2018;46(W1):W246–w51.
   PubMed Web of Science ®Google Scholar
• Leenay Ryan T, Maksimchuk Kenneth R, Slotkowski Rebecca A, et al. Identifying and visualizing functional PAM diversity across CRISPR-Cas systems. Mol Cell. 2016;62(1):137–147.
   PubMed Web of Science ®Google Scholar
• Farasat I, Salis HM. A biophysical Model of CRISPR/Cas9 activity for rational design of genome editing and gene regulation. PLoS Comput Biol. 2016;12(1):e1004724.
   PubMed Web of Science ®Google Scholar
• Vigouroux A, Oldewurtel E, Cui L, et al. Tuning dCas9’s ability to block transcription enables robust, noiseless knockdown of bacterial genes. Mol Syst Biol. 2018;14(3):e7899.
   PubMed Web of Science ®Google Scholar
• Llewellyn AC, Jones CL, Napier BA, et al. Macrophage replication screen identifies a novel Francisella hydroperoxide resistance protein involved in virulence. PLoS ONE. 2011;6(9):e24201.
   PubMed Web of Science ®Google Scholar
• Gallagher LA, McKevitt M, Ramage ER, et al. Genetic dissection of the Francisella novicida restriction barrier. J Bacteriol. 2008;190(23):7830–7837.
   PubMed Web of Science ®Google Scholar
• Weiss DS, Brotcke A, Henry T, et al. In vivo negative selection screen identifies genes required for Francisella virulence. Proc Natl Acad Sci U S A. 2007;104(14):6037–6042.
   PubMed Web of Science ®Google Scholar
• Bryksin AV, Matsumura I, Mokrousov I. Rational design of a plasmid origin that replicates efficiently in both gram-positive and gram-negative bacteria. PLoS One. 2010;5(10):e13244
   PubMed Web of Science ®Google Scholar