Advertisement

Journal of Molecular Evolution

, Volume 60, Issue 2, pp 174–182 | Cite as

Intervening Sequences of Regularly Spaced Prokaryotic Repeats Derive from Foreign Genetic Elements

  • Francisco J.M. Mojica
  • Chc)sar Díez-Villaseñor
  • Jesús García-Martínez
  • Elena Soria
Article

Abstract

Prokaryotes contain short DNA repeats known as CRISPR, recognizable by the regular spacing existing between the recurring units. They represent the most widely distributed family of repeats among prokaryotic genomes, suggesting a biological function. The origin of the intervening sequences, at present unknown, could provide clues about their biological activities. Here we show that CRISPR spacers derive from preexisting sequences, either chromosomal or within transmissible genetic elements such as bacteriophages and conjugative plasmids. Remarkably, these extrachromosomal elements fail to infect the specific spacer-carrier strain, implying a relationship between CRISPR and immunity against targeted DNA. Bacteriophages and conjugative plasmids are involved in prokaryotic population control, evolution, and pathogenicity. All these biological traits could be influenced by the presence of specific spacers. CRISPR loci can be visualized as mosaics of a repeated unit, separated by sequences at some time present elsewhere in the cell.

Keywords

CRISPR DNA repeats Conjugative plasmids Bacteriophages Lateral gene transfer Prokaryotic evolution Pathogenicity 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

This work was financed by research grants from the Conselleria de Cultura, Educació i Ciència, Generalitat Valenciana (CTIDIB/2002/155 and gv04B-457). C.D. is supported by a graduate fellowship from the Ministerio de Educación, Cultura y Deporte. We are indebted to Kathy Hernández for assistance and to J. Antón for critical reading of the manuscript.

References

  1. Altschul, SF, Madden, TL, Schaffer, AA, Zhang, J, Zhang, Z, Miller, W, Lipman, DJ 1997Gapped BLAST and PSI-BLAST: A new generation of protein database search programsNucleic Acids Res2533893402PubMedGoogle Scholar
  2. Banks, DJ, Beres, SB, Musser, JM 2002The fundamental contribution of phages to GAS evolution, genome diversification and strain emergenceTrends Microbiol10515521Google Scholar
  3. Beres, SB, Sylva, GL, Barbian, KD, Lei, BF, Hoff, JS, Mammarella, ND, Liu, MY, Smoot, JC, Porcella, SF, Parkins, LD, Campbell, DS, Smith, TM, McCormick, JK, Leung, DYM, Schlievert, PM, Musser, JM 2002Genome sequence of a serotype M3 strain of group A Streptococcus: Phage-encoded toxins, the high-virulence phenotype, and clone emergenceProc Natl Acad Sci USA991007810083Google Scholar
  4. Birkenbihl, RP, Neef, K, Prangishvili, D, Kemper, B 2001Holliday junction resolving enzymes of archaeal viruses SIRV1 and SIRV2J Mol Biol30910671076Google Scholar
  5. Boucher, Y, Douady, CJ, Papke, RT, Walsh, DA, Boudreau, ME, Nesbo, CL, Case, RJ, Doolittle, WF 2003Lateral gene transfer and the origins of prokaryotic groupsAnnu Rev Genet37283328Google Scholar
  6. Boyd, EF, Brussow, H 2002Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involvedTrends Microbiol10521529Google Scholar
  7. Cabezón, E, Sastre, JI, la Cruz, F 1997Genetic evidence of a coupling role for the TraG protein family in bacterial conjugationMol Gen Genet254400406Google Scholar
  8. Canchaya, C, Proux, C, Fournous, G, Bruttin, A, Brq/4ssow, H 2003Prophage genomicsMicrobiol Mol Biol Rev6738276Google Scholar
  9. Cunningham, MW 2000Pathogenesis of group A streptococcal infectionsClin Microbiol Rev13470511Google Scholar
  10. Easter, CL, Sobecky, PA, Helinski, DR 1997Contribution of different segments of the par region to stable maintenance of the broad-host-range plasmid RK2J Bacteriol17964726479PubMedGoogle Scholar
  11. Ferretti, JJ, McShan, WM, Ajdic, D,  et al. 2001Complete genome sequence of an M1 strain of Streptococcus pyogenesProc Natl Acad Sci USA9846584663Google Scholar
  12. Firth, N, Skurray, R 1992Characterization of the F plasmid bifunctional conjugation gene traGMol Gen Genet232145153Google Scholar
  13. Glaser, P, Frangeul, L, Buchrieser, C,  et al. 2001Comparative genomics of Listeria speciesScience294849852CrossRefPubMedGoogle Scholar
  14. Iida, S, Streiff, MB, Bickle, TA, Arber, W 1987Two DNA antirestriction systems of bacteriophage P1, darA, and darB: Characterization of darA↓ phagesVirology157156166Google Scholar
  15. Jansen, R, Embden, JD, Gaastra, W, Schouls, LM 2002Identification of genes that are associated with DNA repeats in prokaryotesMol Microbiol4315651575Google Scholar
  16. Kawarabayasi, Y, Hino, Y, Horikawa, H,  et al. 2001Complete genome sequence of an aerobic thermoacidophilic crenarchaeon, Sulfolobus tokodaii strain7DNA Res8123140PubMedGoogle Scholar
  17. Lane, D, Feyter, R, Kennedy, M, Phua, SH, Semon, D 1986D protein of miniF plasmid acts as a repressor of transcription and as a site-specific resolvaseNucleic Acids Res1497139728Google Scholar
  18. Luo, YN, Pfister, P, Leisinger, T, Wasserfallen, A 2001The genome of archaeal prophage Ψ M100 encodes the lytic enzyme responsible for autolysis of Methanothermobacter wolfeiiJ Bacteriol18357885792Google Scholar
  19. Martin, KA, Davis, MA, Austin, S 1991Fine-structure analysis of the P1 plasmid partition siteJ Bacteriol17336303634Google Scholar
  20. Martínez, JL, Baquero, F 2002Interactions among strategies associated with bacterial infection: Pathogenicity, epidemicity, and antibiotic resistanceClin Microbiol Rev15647679Google Scholar
  21. Mojica, FJM, Ferrer, C, Juez, G, Rodríguez-Valera, F 1995Long stretches of short tandem repeats are present in the largest replicons of the Archaea Haloferax mediterranei and Haloferax volcanii and could be involved in replicon partitioningMol Microbiol178593Google Scholar
  22. Mojica, FJM, Díez-Villaseñor, C, Soria, E, Juez, G 2000Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondriaMol Microbiol36244246Google Scholar
  23. Nakagawa, I, Kurokawa, K, Yamashita, A, Nakata, M, Tomiyasu, Y, Okahashi, N, Kawabata, S, Yamazaki, K, Shiba, T, Yasunaga, T, Hayashi, H, Hattori, M, Hamada, S 2003Genome sequence of an M3 strain of Streptococcus pyogenes reveals a large-scale genomic rearrangement in invasive strains and new insights into phage evolutionGenome Res1310421055Google Scholar
  24. Ochman, H, Selander, RK 1984Standard reference strains of Escherichia coli from natural populationsJ Bacteriol157690693Google Scholar
  25. Pfister, P, Wesserfallen, A, Stettler, R, Leisinger, T 1998Molecular analysis of Methanobacterium phage ΨM2Mol Microbiol30233244Google Scholar
  26. Prangishvili, D, Arnold, HP, Gotz, D, Ziese, U, Holz, I, Kristjansson, JK, Zillig, W 1999A novel virus family, the Rudiviridae: Structure, virus-host interactions and genome variability of the Sulfolobus viruses SIRV1 and SIRV2Genetics1521387 1396Google Scholar
  27. Profit, T, Sriskandan, S, Yang, L, Fraser, JD 2003Superantigens and streptococcal toxic shock syndromeEmerg Infect Dis912111218Google Scholar
  28. Schleper, C, Holz, I, Janekovic, D, Murphy, J, Zillig, W 1995A multicopy plasmid of the extremely thermophilic archaeon Sulfolobus effects its transfer to recipients by matingJ Bacteriol17744174426Google Scholar
  29. She, Q, Phan, H, Garrett, RA, Albers, SV, Stedman, KM, Zillig, W 1998Genetic profile of pNOB8 from Sulfolobus: The first conjugative plasmid from an archaeonExtremophiles2417425Google Scholar
  30. She, Q, Singh, RK, Confalonieri, F,  et al. 2001The complete genome of the crenarchaeon Sulfolobus solfataricus P2Proc Natl Acad Sci USA9878357840CrossRefPubMedGoogle Scholar
  31. She, Q, Brugger, K, Chen, L 2002Archaeal integrative genetic elements and their impact on genome evolutionRes Microbiol153325332Google Scholar
  32. Smith, DR, DoucetteStamm, LA, Deloughery, C,  et al. 1997Complete genome sequence of Methanobacterium thermoautotrophicum H: Functional analysis and comparative genomicsJ Bacteriol17971357155PubMedGoogle Scholar
  33. Smoot, JC, Barbian, KD, Compel, JJ,,  et al. 2002Genome sequence and comparative microarray analysis of serotype M18 group A Streptococcus strains associated with acute rheumatic fever outbreaksProc Natl Acad Sci USA9946684673Google Scholar
  34. Smoot, LM, McCormick, JK, Smoot, JC, Hoe, NP, Strickland, I, Cole, RL, Barbian, KD, Earhart, CA, Ohlendorf, DH, Veasy, LG, Hill, HR, Leung, DYM, Schlievert, PM, Musser, JM 2002Characterization of two novel pyrogenic toxin superantigens made by an acute rheumatic fever clone of Streptococcus pyogenes associated with multiple disease outbreaksInfect Immun7070957104Google Scholar
  35. Stedman, KM, She, Q, Phan, H, Holz, I, Singh, H, Prangishvili, D, Garrett, R, Zillig, W 2000pING family of conjugative plasmids from the extremely thermophilic archaeon Sulfolobus islandicus: Insights into recombination and conjugation in CrenarchaeotaJ Bacteriol18270147020Google Scholar
  36. Stedman, KM, She, Q, Phan, H, Arnold, HP, Holz, I, Garrett, RA, Zillig, W 2003Relationships between fuselloviruses infecting the extremely thermophilic archaeon Sulfolobus: SSV1 and SSV2Res Microbiol154295302CrossRefPubMedGoogle Scholar
  37. Tang, TH, Bachellerie, JP, Rozhdestvensky, T, Bortolin, ML, Huber, H, Drungowski, M, Elge, T, Brosius, J, Huttenhofer, A 2002Identification of 86 candidates for small non-messenger RNAs from the archaeon Archaeoglobus fulgidusProc Natl Acad Sci USA9975367541Google Scholar
  38. Traxler, BA, Minkley, EG,Jr 1988Evidence that DNA helicase I and oriT site-specific nicking are both functions of the F Tral proteinJ Mol Biol5205209Google Scholar
  39. Young, R 1992Bacteriophage lysis: Mechanism and regulationMicrobiol Rev56430481Google Scholar
  40. Zillig, W, Arnold, HP, Holz, I, Prangishvili, D, Schweier, A, Stedman, K, She, Q, Phan, H, Garrett, R, Kristjansson, JK 1998Genetic elements in the extremely thermophilic archaeon SulfolobusExtremophiles2131140Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • Francisco J.M. Mojica
    • 1
  • Chc)sar Díez-Villaseñor
    • 1
  • Jesús García-Martínez
    • 1
  • Elena Soria
    • 1
  1. 1.División de Microbiología, Departamento de Fisiología, Genhc)tica y MicrobiologíaUniversidad de AlicanteSpain

Personalised recommendations

Cite article

Buy options