Interdependencies Between the Adaptation and Interference Modules Guide Efficient CRISPR-Cas Immunity

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Evolutionary Biology: Self/Nonself Evolution, Species and Complex Traits Evolution, Methods and Concepts

Abstract

CRISPR-Cas is a common adaptive RNA-guided prokaryotic immunity mechanism that limits the spread of mobile genetic elements such as phages and plasmids. A CRISPR-Cas system is composed of two seemingly independent modules. Cas proteins from the adaptation module are responsible for recording prior encounters with mobile genetic elements by incorporating fragments of foreign DNA into CRISPR array. Small protective RNAs generated after CRISPR array transcription are used by the interference module Cas proteins to locate complementary nucleic acids and destroy them. Here, we discuss how the activities and substrate preferences of these two functional modules must be tightly coordinated to provide efficient defence against foreign DNA.

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References

  • Abudayyeh OO, Gootenberg JS, Konermann S, Joung J, Slaymaker IM, Cox DB, Shmakov S, Makarova KS, Semenova E, Minakhin L, Severinov K, Regev A, Lander ES, Koonin EV, Zhang F (2016) C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science 353(6299):aaf5573. doi:10.1126/science.aaf5573

  • Arslan Z, Hermanns V, Wurm R, Wagner R, Pul U (2014) Detection and characterization of spacer integration intermediates in type I-E CRISPR-Cas system. Nucl Acids Res 42(12):7884–7893. doi:10.1093/nar/gku510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315(5819):1709–1712. doi:10.1126/science.1138140

    Article  CAS  PubMed  Google Scholar 

  • Brouns SJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJ, Snijders AP, Dickman MJ, Makarova KS, Koonin EV, van der Oost J (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321(5891):960–964. doi:10.1126/science.1159689

    Article  CAS  PubMed  Google Scholar 

  • Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y, Pirzada ZA, Eckert MR, Vogel J, Charpentier E (2011) CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471(7340):602–607. doi:10.1038/nature09886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elmore JR, Sheppard NF, Ramia N, Deighan T, Li H, Terns RM, Terns MP (2016) Bipartite recognition of target RNAs activates DNA cleavage by the Type III-B CRISPR-Cas system. Genes Dev 30(4):447–459. doi:10.1101/gad.272153.115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gleditzsch D, Muller-Esparza H, Pausch P, Sharma K, Dwarakanath S, Urlaub H, Bange G, Randau L (2016) Modulating the cascade architecture of a minimal Type I-F CRISPR-Cas system. Nucl Acids Res 44(12):5872–5882. doi:10.1093/nar/gkw469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goren MG, Doron S, Globus R, Amitai G, Sorek R, Qimron U (2016) Repeat size determination by two molecular rulers in the Type I-E CRISPR array. Cell Rep 16(11):2811–2818. doi:10.1016/j.celrep.2016.08.043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hale CR, Zhao P, Olson S, Duff MO, Graveley BR, Wells L, Terns RM, Terns MP (2009) RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 139(5):945–956. doi:10.1016/j.cell.2009.07.040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hatoum-Aslan A, Samai P, Maniv I, Jiang W, Marraffini LA (2013) A ruler protein in a complex for antiviral defense determines the length of small interfering CRISPR RNAs. J Biol Chem 288(39):27888–27897. doi:10.1074/jbc.M113.499244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayes RP, **ao Y, Ding F, van Erp PB, Rajashankar K, Bailey S, Wiedenheft B, Ke A (2016) Structural basis for promiscuous PAM recognition in type I-E Cascade from E. coli. Nature. doi:10.1038/nature16995

  • Hochstrasser ML, Doudna JA (2015) Cutting it close: CRISPR-associated endoribonuclease structure and function. Trends Biochem Sci 40(1):58–66. doi:10.1016/j.tibs.2014.10.007

    Article  CAS  PubMed  Google Scholar 

  • Kazlauskiene M, Tamulaitis G, Kostiuk G, Venclovas C, Siksnys V (2016) Spatiotemporal control of Type III-A CRISPR-Cas immunity: coupling DNA degradation with the target RNA recognition. Mol Cell 62(2):295–306. doi:10.1016/j.molcel.2016.03.024

    Article  CAS  PubMed  Google Scholar 

  • Koonin EV, Zhang F (2017) Coupling immunity and programmed cell suicide in prokaryotes: life-or-death choices. BioEssays 39(1):1–9. doi:10.1002/bies.201600186

    Article  CAS  PubMed  Google Scholar 

  • Krupovic M, Makarova KS, Forterre P, Prangishvili D, Koonin EV (2014) Casposons: a new superfamily of self-synthesizing DNA transposons at the origin of prokaryotic CRISPR-Cas immunity. BMC Biol 12:36. doi:10.1186/1741-7007-12-36

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuznedelov K, Mekler V, Lemak S, Tokmina-Lukaszewska M, Datsenko KA, Jain I, Savitskaya E, Mallon J, Shmakov S, Bothner B, Bailey S, Yakunin AF, Severinov K, Semenova E (2016) Altered stoichiometry Escherichia coli cascade complexes with shortened CRISPR RNA spacers are capable of interference and primed adaptation. Nucl Acids Res 44(22):10849–10861. doi:10.1093/nar/gkw914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo ML, Jackson RN, Denny SR, Tokmina-Lukaszewska M, Maksimchuk KR, Lin W, Bothner B, Wiedenheft B, Beisel CL (2016) The CRISPR RNA-guided surveillance complex in Escherichia coli accommodates extended RNA spacers. Nucl Acids Res. doi:10.1093/nar/gkw421

    Google Scholar 

  • Maier LK, Stachler AE, Saunders SJ, Backofen R, Marchfelder A (2015) An active immune defense with a minimal CRISPR (clustered regularly interspaced short palindromic repeats) RNA and without the Cas6 protein. J Biol Chem 290(7):4192–4201. doi:10.1074/jbc.M114.617506

    Article  CAS  PubMed  Google Scholar 

  • Makarova KS, Wolf YI, Alkhnbashi OS, Costa F, Shah SA, Saunders SJ, Barrangou R, Brouns SJ, Charpentier E, Haft DH, Horvath P, Moineau S, Mojica FJ, Terns RM, Terns MP, White MF, Yakunin AF, Garrett RA, van der Oost J, Backofen R, Koonin EV (2015) An updated evolutionary classification of CRISPR-Cas systems. Nat Rev Microbiol 13(11):722–736. doi:10.1038/nrmicro3569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marraffini LA, Sontheimer EJ (2008) CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322(5909):1843–1845. doi:10.1126/science.1165771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marraffini LA, Sontheimer EJ (2010) Self versus non-self discrimination during CRISPR RNA-directed immunity. Nature 463(7280):568–571. doi:10.1038/nature08703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moch C, Fromant M, Blanquet S, Plateau P (2016) DNA binding specificities of Escherichia coli Cas1-Cas2 integrase drive its recruitment at the CRISPR locus. Nucl Acids Res. doi:10.1093/nar/gkw1309

    PubMed Central  Google Scholar 

  • Mohanraju P, Makarova KS, Zetsche B, Zhang F, Koonin EV, van der Oost J (2016) Diverse evolutionary roots and mechanistic variations of the CRISPR-Cas systems. Science 353(6299):aad5147. doi:10.1126/science.aad5147

  • Nunez JK, Harrington LB, Kranzusch PJ, Engelman AN, Doudna JA (2015a) Foreign DNA capture during CRISPR-Cas adaptive immunity. Nature 527(7579):535–538. doi:10.1038/nature15760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nunez JK, Lee AS, Engelman A, Doudna JA (2015b) Integrase-mediated spacer acquisition during CRISPR-Cas adaptive immunity. Nature 519(7542):193–198. doi:10.1038/nature14237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nunez JK, Bai L, Harrington LB, Hinder TL, Doudna JA (2016) CRISPR immunological memory requires a host factor for specificity. Mol Cell 62(6):824–833. doi:10.1016/j.molcel.2016.04.027

    Article  CAS  PubMed  Google Scholar 

  • Olovnikov I, Chan K, Sachidanandam R, Newman DK, Aravin AA (2013) Bacterial argonaute samples the transcriptome to identify foreign DNA. Mol Cell 51(5):594–605. doi:10.1016/j.molcel.2013.08.014

    Article  CAS  PubMed  Google Scholar 

  • Rouillon C, Zhou M, Zhang J, Politis A, Beilsten-Edmands V, Cannone G, Graham S, Robinson CV, Spagnolo L, White MF (2013) Structure of the CRISPR interference complex CSM reveals key similarities with cascade. Mol Cell 52(1):124–134. doi:10.1016/j.molcel.2013.08.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samai P, Pyenson N, Jiang W, Goldberg GW, Hatoum-Aslan A, Marraffini LA (2015) Co-transcriptional DNA and RNA cleavage during Type III CRISPR-Cas immunity. Cell 161(5):1164–1174. doi:10.1016/j.cell.2015.04.027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Semenova E, Kuznedelov K, Datsenko KA, Boudry PM, Savitskaya EE, Medvedeva S, Beloglazova N, Logacheva M, Yakunin AF, Severinov K (2015) The Cas6e ribonuclease is not required for interference and adaptation by the E. coli type I-E CRISPR-Cas system. Nucl Acids Res 43(12):6049–6061. doi:10.1093/nar/gkv546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shmakov S, Smargon A, Scott D, Cox D, Pyzocha N, Yan W, Abudayyeh OO, Gootenberg JS, Makarova KS, Wolf YI, Severinov K, Zhang F, Koonin EV (2017) Diversity and evolution of class 2 CRISPR-Cas systems. Nat Rev Microbiol 15(3):169–182. doi:10.1038/nrmicro.2016.184

    Article  CAS  PubMed  Google Scholar 

  • Swarts DC, Jore MM, Westra ER, Zhu Y, Janssen JH, Snijders AP, Wang Y, Patel DJ, Berenguer J, Brouns SJ, van der Oost J (2014) DNA-guided DNA interference by a prokaryotic Argonaute. Nature 507(7491):258–261. doi:10.1038/nature12971

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swarts DC, Szczepaniak M, Sheng G, Chandradoss SD, Zhu Y, Timmers EM, Zhang Y, Zhao H, Lou J, Wang Y, Joo C, van der Oost J (2017) Autonomous generation and loading of DNA guides by bacterial argonaute. Mol Cell 65(6):985–998. doi:10.1016/j.molcel.2017.01.033

  • Vogel J, Luisi BF (2011) Hfq and its constellation of RNA. Nat Rev Microbiol 9(8):578–589. doi:10.1038/nrmicro2615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Li J, Zhao H, Sheng G, Wang M, Yin M, Wang Y (2015) Structural and mechanistic basis of PAM-dependent spacer acquisition in CRISPR-Cas systems. Cell 163(4):840–853. doi:10.1016/j.cell.2015.10.008

    Article  CAS  PubMed  Google Scholar 

  • Yoganand KN, Sivathanu R, Nimkar S, Anand B (2017) Asymmetric positioning of Cas1-2 complex and integration host factor induced DNA bending guide the unidirectional homing of protospacer in CRISPR-Cas type I-E system. Nucl Acids Res 45(1):367–381. doi:10.1093/nar/gkw1151

    Article  CAS  PubMed  Google Scholar 

  • Yosef I, Goren MG, Qimron U (2012) Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli. Nucl Acids Res 40(12):5569–5576. doi:10.1093/nar/gks216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Rouillon C, Kerou M, Reeks J, Brugger K, Graham S, Reimann J, Cannone G, Liu H, Albers SV, Naismith JH, Spagnolo L, White MF (2012) Structure and mechanism of the CMR complex for CRISPR-mediated antiviral immunity. Mol Cell 45(3):303–313. doi:10.1016/j.molcel.2011.12.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work is supported by an NIH grant GM10407.

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Correspondence to Ekaterina Semenova or Konstantin Severinov .

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Semenova, E., Severinov, K. (2017). Interdependencies Between the Adaptation and Interference Modules Guide Efficient CRISPR-Cas Immunity. In: Pontarotti, P. (eds) Evolutionary Biology: Self/Nonself Evolution, Species and Complex Traits Evolution, Methods and Concepts. Springer, Cham. https://doi.org/10.1007/978-3-319-61569-1_3

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