Selective and hyperactive uptake of foreign DNA by adaptive immune systems of an archaeon via two distinct mechanisms

Abstract

Summary Central to the disparate adaptive immune systems of archaea and bacteria are clustered regularly interspaced short palindromic repeats (CRISPR). The spacer regions derive from invading genetic elements and, via RNA intermediates and associated proteins, target and cleave nucleic acids of the invader. Here we demonstrate the hyperactive uptake of hundreds of unique spacers within CRISPR loci associated with type I and IIIB immune systems of a hyperthermophilic archaeon. Infection with an environmental virus mixture resulted in the exclusive uptake of protospacers from a co‐infecting putative conjugative plasmid. Spacer uptake occurred by two distinct mechanisms in only one of two CRISPR loci subfamilies present. In two loci, insertions, often multiple, occurred adjacent to the leader while in a third locus single spacers were incorporated throughout the array. Protospacer DNAs were excised from the invading genetic element immediately after CCN motifs, on either strand, with the secondary cut apparently produced by a ruler mechanism. Over a 10‐week period, there was a gradual decrease in the number of wild‐type cells present in the culture but the virus and putative conjugative plasmid were still propagating. The results underline the complex dynamics of CRISPR‐based immune systems within a population infected with genetic elements.

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References 57

1. 1.

   Andersson AF, Banfield JF. Virus population dynamics and acquired virus resistance in natural microbial communities. Science. 2008;320:1047-1050.

   Not in our library10.1126/science.1157358

2. 2.

   Aranaz A, Liébana E, Mateos A, Dominguez L, Vidal D, Domingo M, et al. Spacer oligonucleotide typing of Mycobacterium bovis strains from cattle and other animals: a tool for studying epidemiology of tuberculosis. J Clin Microbiol. 1996;34:2734-2740.

   Not in our library10.1128/jcm.34.11.2734-2740.1996

3. 3.

   Arnold HP, She Q, Phan H, Stedman K, Prangishvili D, Holz I, et al. The genetic element pSSVx of the extremely thermophilkic crenarchaeon Sulfolobus is a hybrid between a plasmid and a virus. Mol Microbiol. 1999;34:217-226.

   Not in our library10.1046/j.1365-2958.1999.01573.x

4. 4.

   Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science. 2007;315:1709-1712.

   Not in our library10.1126/science.1138140

5. 5.

   Basta T, Smyth J, Forterre P, Prangishvili D, Peng X. Novel archaeal plasmid pAH1 and its interactions with the lipothrixvirus AFV1. Mol Microbiol. 2009;71:23-34.

   Not in our library10.1111/j.1365-2958.2008.06488.x

6. 6.

   Bize A, Karlsson EA, Ekefjard K, Quax TE, Pina M, Prevost MC, et al. A unique virus release mechanism in the Archaea. Proc Natl Acad Sci USA. 2009;106:11306-11311.

   Not in our library10.1073/pnas.0901238106

7. 7.

   Bolotin A, Quinquis B, Sorokin A, Ehrlich SD. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology. 2005;151:2551-2561.

   Not in our library10.1099/mic.0.28048-0

8. 8.

   Brouns SJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJ, Snijders AP, et al. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science. 2008;321:960-964.

   Not in our library10.1126/science.1159689

9. 9.

   Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y, Pirzada ZA, et al. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature. 2011;471:602-607.

   Not in our library10.1038/nature09886

10. 10.

    Deng L, Kenchappa CS, Peng X, She Q, Garrett RA. Modulation of CRISPR locus transcription by the repeat-binding protein Cbp1 in Sulfolobus. Nucleic Acids Res. 2012;40:2470-2480.

    Not in our library10.1093/nar/gkr1111

11. 11.

    Deveau H, Barrangou R, Garneau JE, Labonté J, Fremaux C, Boyaval P, et al. Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J Bacteriol. 2008;190:1390-1400.

    Not in our library10.1128/jb.01412-07

12. 12.

    Garrett RA, Bize A, Shah SA, Stetter K, Prangishvili D, Peng X. Metagenomic analyses of novel viruses, plasmids, and their variants, from an environmental sample of hyperthermophilic neutrophiles cultured in a bioreactor. Environ Microbiol. 2010;12:2918-2930.

    Not in our library10.1111/j.1462-2920.2010.02266.x

13. 13.

    Garrett RA, Vestergaard G, Shah SA. Archaeal CRISPR-based immune systems: exchangeable functional modules. Trends Microbiol. 2011a;19:549-556.

    Not in our library10.1016/j.tim.2011.08.002

14. 14.

    Garrett RA, Shah SA, Vestergaard G, Deng L, Gudbergsdottir S, Kenchappa CS, et al. CRISPR-based immune systems of the Sulfolobales – complexity and diversity. Biochem Soc Trans. 2011b;39:51-57.

    Not in our library10.1042/bst0390051

15. 15.

    Greve B, Jensen S, Brügger K, Zillig W, Garrett RA. Genomic comparison of archaeal conjugative plasmids from Sulfolobus. Archaea. 2004;1:231-239.

    Not in our library10.1155/2004/151926

16. 16.

    Groenen PM, Bunschoten AE, van Soolingen D, van Embden JD. Nature of DNA polymorphism in the direct repeat cluster of Mycobacterium tuberculosis; application for strain differentiation by a novel typing method. Mol Microbiol. 1993;10:1057-1065.

    Not in our library10.1111/j.1365-2958.1993.tb00976.x

17. 17.
    Dynamic properties of the Sulfolobus CRISPR/Cas and CRISPR/Cmr systems when challenged with vector‐borne viral and plasmid genes and protospacers · 2010

    No notice
18. 18.

    Hale CR, Zhao P, Olson S, Duff MO, Graveley BR, Wells L, et al. RNA-guided RNA cleavage by a CRISPR RNA–Cas protein complex. Cell. 2009;139:945-956.

    Not in our library10.1016/j.cell.2009.07.040

19. 19.

    Hale CR, Majumdar S, Elmore J, Pfister N, Compton M, Olson S, et al. Essential features and rational design of CRISPR RNAs that function with the Cas RAMP module complex to cleave RNAs. Mol Cell. 2012;45:292-302.

    Not in our library10.1016/j.molcel.2011.10.023

20. 20.

    Häring M, Vestergaard G, Rachel R, Chen L, Garrett RA, Prangishvili D. Independent virus development outside a host. Nature. 2005;436:1101-1102.

    Not in our library10.1038/4361101a

21. 21.

    Hatoum-Aslan A, Maniv I, Marraffini LA. Mature clustered, regularly interspaced, short palindromic repeats RNA (crRNA) length is measured by a ruler mechanism anchored at the precursor processing site. Proc Natl Acad Sci USA. 2011;108:21218-21222.

    Not in our library10.1073/pnas.1112832108

22. 22.

    Held NL, Whitaker RJ. Viral biogeography revealed by signatures in Sulfolobus islandicus genomes. Environ Microbiol. 2009;11:457-466.

    Not in our library10.1111/j.1462-2920.2008.01784.x

23. 23.

    Hermans PW, van Soolingen D, Bik EM, de Haas PE, Dale JW, van Embden JD. Insertion element IS987 from Mycobacterium bovis BCG is located in a hot-spot integration region for insertion elements in Mycobacterium tuberculosis complex strains. Infect Immun. 1991;59:2695-2705.

    Not in our library10.1128/iai.59.8.2695-2705.1991

24. 24.

    Horvath P, Romero DA, Coûté-Monvoisin A-C, Richards M, Deveau H, Moineau S, et al. Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J Bacteriol. 2008;190:1401-1412.

    Not in our library10.1128/jb.01415-07

25. 25.

    Jore MM, Lundgren M, Van Duijn E, Bultema JB, Westra ER, Waghmare SP, et al. Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nat Struct Mol Biol. 2011;18:529-536.

    Not in our library10.1038/nsmb.2019

26. 26.

    Kamerbeek J, Schouls L, Kolk A, van Agterfeld M, van Soolingen D, Kuijper S, et al. Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol. 1997;35:907-914.

    Not in our library10.1128/jcm.35.4.907-914.1997

27. 27.

    Lillestøl RK, Redder P, Garrett RA, Brügger K. A putative viral defence mechanism in archaeal cells. Archaea. 2006;2:59-72.

    Not in our library10.1155/2006/542818

28. 28.

    Lillestøl RK, Shah SA, Brügger K, Redder P, Phan H, Christiansen J, Garrett RA. CRISPR families of the crenarchaeal genius Sulfolobus: bidirectional transcription and dynamic properties. Mol Microbiol. 2009;72:259-272.

    Not in our library10.1111/j.1365-2958.2009.06641.x

29. 29.

    Lintner NG, Frankel KA, Tsutakawa SE, Alsbury DL, Copié V, Young MJ, et al. The structure of the CRISPR-associated protein Csa3 provides insight into the regulation of the CRISPR/Cas system. J Mol Biol. 2011;405:939-955.

    Not in our library10.1016/j.jmb.2010.11.019

30. 30.

    Makarova KS, Haft DH, Barrangou R, Brouns SJ, Charpentier E, Horvath P, et al. Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol. 2011;9:467-477.

    Not in our library10.1038/nrmicro2577

31. 31.

    Manica A, Zebec Z, Teichmann D, Schleper C. In vivo activity of CRISPR-mediated virus defence in a hyperthermophilic archaeon. Mol Microbiol. 2011;80:481-491.

    Not in our library10.1111/j.1365-2958.2011.07586.x

32. 32.

    Marraffini LA, Sontheimer EJ. CRISPR interference limits horizontal gene transfer in Staphylococci by targeting DNA. Science. 2008;322:1843-1845.

    Not in our library10.1126/science.1165771

33. 33.

    Mojica FJ, Diez-Villasenor C, Garcia-Martinez J, Soria E. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J Mol Evol. 2005;60:174-182.

    Not in our library10.1007/s00239-004-0046-3

34. 34.

    Mojica FJM, Díez-Villaseñor C, García-Martínez J, Almendros C. Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology. 2009;155:733-740.

    Not in our library10.1099/mic.0.023960-0

35. 35.

    Pina M, Bize A, Forterre P, Prangishvili D. The archaeoviruses. FEMS Microbiol Rev. 2011;35:1035-1054.

    Not in our library10.1111/j.1574-6976.2011.00280.x

36. 36.

    Porter K, Russ BE, Dyall-Smith ML. Virus–host interactions in salt lakes. Curr Opin Microbiol. 2007;10:418-424.

    Not in our library10.1016/j.mib.2007.05.017

37. 37.

    Pourcel C, Salvignol G, Vergnaud G. CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology. 2005;151:653-663.

    Not in our library10.1099/mic.0.27437-0

38. 38.

    Prangishvili D, Albers SV, Holz I, Arnold HP, Stedman K, Klein T, et al. Conjugation in archaea: frequent occurrence of conjugative plasmids in Sulfolobus. Plasmid. 1998;40:190-202.

    Not in our library10.1006/plas.1998.1363

39. 39.

    Prangishvili D, Forterre P, Garrett RA. Viruses of the Archaea: a unifying view. Nat Rev Microbiol. 2006a;11:837-848.

    Not in our library10.1038/nrmicro1527

40. 40.

    Prangishvili D, Vestergaard G, Häring M, Aramayo R, Basta T, Rachel R, et al. Structural and genomic properties of the hyperthermophilic archaeal virus ATV with an extracellular stage of the reproductive cycle. J Mol Biol. 2006b;359:1203-1216.

    Not in our library10.1016/j.jmb.2006.04.027

41. 41.

    Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, et al. Artemis: sequence visualization and annotation. Bioinformatics. 2000;16:944-945.

    Not in our library10.1093/bioinformatics/16.10.944

42. 42.

    Shah SA, Garrett RA. CRISPR/Cas and Cmr modules, mobility and evolution of adaptive immune systems. Res Microbiol. 2011;162:27-38.

    Not in our library10.1016/j.resmic.2010.09.001

43. 43.

    Shah SA, Hansen NR, Garrett RA. Distributions of CRISPR spacer matches in viruses and plasmids of crenarchaeal acidothermophiles and implications for their inhibitory mechanism. Biochem Soc Trans. 2009;37:23-28.

    Not in our library10.1042/bst0370023

44. 44.

    Shah SA, Vestergaard G, Garrett RA, Marchfelder A, Hess W. CRISPR/Cas and CRISPR/Cmr immune systems of Archaea. Regulatory RNAs in Prokaryotes. 2011;163-181.

    Not in our library

45. 45.

    She Q, Singh RK, Confalonieri F, Zivanovic Y, Allard G, Awayez MJ, et al. The complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc Natl Acad Sci USA. 2001;98:7835-7840.

    Not in our library10.1073/pnas.141222098

46. 46.

    Soler N, Marguet E, Verbavatz JM, Forterre P. Virus-like vesicles and extracellular DNA from hyperthermophilic archaea of the order Thermococcales. Res Microbiol. 2008;159:390-399.

    Not in our library10.1016/j.resmic.2008.04.015

47. 47.
    CRISPR Interference Directs Strand Specific Spacer Acquisition · 2012

    No notice
48. 48.

    Tang T-H, Bachellerie J-P, Rozhdestvensky T, Bortolin M-L, Huber H, Drungowski M, et al. Identification of 86 candidates for small non-messenger RNAs from the archaeon Archaeoglobus fulgidus. Proc Natl Acad Sci USA. 2002;99:7536-7541.

    Not in our library10.1073/pnas.112047299

49. 49.

    Tang T-H, Polacek N, Zywicki M, Huber H, Brügger K, Garrett R, et al. Identification of novel non-coding RNAs as potential antisense regulators in the archaeon Sulfolobus solfataricus. Mol Microbiol. 2005;55:469-481.

    Not in our library10.1111/j.1365-2958.2004.04428.x

50. 50.

    Tyson GW, Banfield JF. Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ Microbiol. 2008;10:200-207.

    Not in our library10.1111/j.1462-2920.2007.01444.x

51. 51.

    Wang Y, Duan Z, Zhu H, Guo X, Wang Z, Zhou J, et al. A novel Sulfolobus non-conjugative extrachromosomal element capable of integration into the host genome and spreading in the presence of a fusellovirus. Virology. 2007;363:124-133.

    Not in our library10.1016/j.virol.2007.01.035

52. 52.

    Wurtzel O, Sapra R, Chen F, Zhu YW, Simmons BA, Sorek R. A single-base resolution map of an archaeal transcriptome. Genome Res. 2010;20:133-141.

    Not in our library10.1101/gr.100396.109

53. 53.

    Xiang X, Chen L, Huang X, Luo Y, She Q, Huang L. Sulfolobus tengchongensis spindle-shaped virus STSV1: virus–host interactions and genomic features. J Virol. 2005;79:8677-8686.

    Not in our library10.1128/jvi.79.14.8677-8686.2005

54. 54.

    Yosef I, Goren MG, Qimron U. Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli. Nucleic Acids Res. 2012;40:5569-5576.

    Not in our library10.1093/nar/gks216

55. 55.

    Zhang J, Rouillon C, Kerou M, Reeks J, Brugger K, Graham S, et al. Structure and mechanism of the Cmr complex of CRISPR-mediated antiviral immunity. Mol Cell. 2012;45:303-313.

    Not in our library10.1016/j.molcel.2011.12.013

56. 56.

    Zillig W, Kletzin A, Schleper C, Holz I, Janekovic D, Hain J, et al. Screening for Sulfolobales, their plasmids and their viruses in Icelandic solfataras. Syst Appl Microbiol. 1994;16:109-128.

    Not in our library

57. 57.

    Zillig W, Arnold HP, Holz I, Prangishvili D, Schweier A, Stedman K, et al. Genetic elements in the extremely thermophilic archaeon Sulfolobus. Extremophiles. 1998;2:131-140.

    Not in our library10.1007/s007920050052

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