Skip to main content
SpringerLink
Log in

Applications of the Versatile CRISPR-Cas Systems

  • Chapter
  • First Online:
CRISPR-Cas Systems

Abstract

CRISPR-Cas systems provide adaptive immunity against viruses and plasmids in bacteria and archaea. Interference is mediated by small non-coding CRISPR RNAs (crRNAs) that guide the Cas machinery towards complementary nucleic acids for sequence-specific cleavage. Several recent studies have shown that CRISPR-encoded immunity can increase the breadth and depth of phage resistance in bacteria, and can provide a barrier to acquisition of undesirable genetic elements, notably plasmid-encoded antibiotic resistance genes. Further, the adaptive and inheritable nature of those idiosyncratic chromosomal loci provide valuable genetic polymorphism which can be leveraged for typing purposes, proprietary strain tagging, ecological surveys, and epidemiological studies. The ability to readily transfer functional CRISPR-Cas systems across even distant bacteria, and re-program their endonuclease activity make them amenable to genetic engineering and useful for genome editing. These features, in combination with recent breakthroughs in unravelling the molecular underpinnings of the CRISPR mechanism of action have paved the way for several applications in a diversity of industrial and biotechnological areas.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Abadia E, Zhang J, dos Vultos T, Ritacco V, Kremer K, Aktas E, Matsumoto T, Refregier G, van Soolingen D, Gicquel B, Sola C (2010) Resolving lineage assignation on Mycobacterium tuberculosis clinical isolates classified by spoligotyping with a new high-throughput 3R SNPs based method. Infect Genet Evol 10:1066–1074

    Article  PubMed  CAS  Google Scholar 

  • Aklujkar M, Lovley DR (2010) Interference with histidyl-tRNA synthetase by a CRISPR spacer sequence as a factor in the evolution of Pelobacter carbinolicus. BMC Evol Biol 10:230

    Article  PubMed  Google Scholar 

  • Andersson AF, Banfield JF (2008) Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320:1047–1050

    Article  PubMed  CAS  Google Scholar 

  • Anderson RE, Brazelton WJ, Baross JA (2011) Using CRISPRs as a metagenomic tool to identify microbial hosts of a diffuse flow hydrothermal vent viral assemblage. FEMS Microbiol Ecol 77:120–133

    Article  PubMed  CAS  Google Scholar 

  • Babu M, Beloglazova N, Flick R, Graham C, Skarina T, Nocek B, Gagarinova A, Pogoutse O, Brown G, Binkowski A, Phanse S, Joachimiak A, Koonin EV, Savchenko A, Emili A, Greenblatt J, Edwards AM, Yakunin AF (2011) A dual function of the CRISPR-Cas system in bacterial antivirus immunity and DNA repair. Mol Microbiol 79:484–502

    Article  PubMed  CAS  Google Scholar 

  • Barrangou R (2012) RNA-mediated programmable DNA cleavage. Nat Biotechnol 30:836–838

    Article  PubMed  CAS  Google Scholar 

  • Barrangou R, Horvath P (2012) CRISPR: new horizons in phage resistance and strain identification. Annu Rev Food Sci Technol 3:143–162

    Article  PubMed  CAS  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 315:1709–1712

    Article  PubMed  CAS  Google Scholar 

  • Berg Miller ME, Yeoman CJ, Chia N, Tringe SG, Angly FE, Edwards RA, Flint HJ, Lamed R, Bayer EA, White BA (2012) Phage-bacteria relationships and CRISPR elements revealed by a metagenomic survey of the rumen microbiome. Environ Microbiol 14:207–227

    Article  PubMed  Google Scholar 

  • Bikard D, Hatoum-Aslan A, Mucida D, Marraffini LA (2012) CRISPR interference can prevent natural transformation and virulence acquisition during in vivo bacterial infection. Cell Host Microbe 12:177–186

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Borile C, Labarre M, Franz S, Sola C, Refrégier G (2011) Using affinity propagation for identifying subspecies among clonal organisms: lessons from M. tuberculosis. BMC Bioinf 12:224

    Article  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 321:960–964

    Article  PubMed  CAS  Google Scholar 

  • Brudey K, Driscoll JR, Rigouts L et al (2006) Mycobacterium tuberculosis complex genetic diversity: mining the fourth international spoligotyping database (SpolDB4) for classification, population genetics and epidemiology. BMC Microbiol 6:23

    Article  PubMed  Google Scholar 

  • Brüggemann H, Lomholt HB, Tettelin H, Kilian M (2012) CRISPR/cas loci of type II Propionibacterium acnes confer immunity against acquisition of mobile elements present in type I P. acnes. PLoS ONE 7:e34171

    Article  PubMed  Google Scholar 

  • Cady KC, O’Toole GA (2011) Non-identity-mediated CRISPR-bacteriophage interaction mediated via the Csy and Cas3 proteins. J Bacteriol 193:3433–3445

    Article  PubMed  CAS  Google Scholar 

  • Cady KC, White AS, Hammond JH, Abendroth MD, Karthikeyan RS, Lalitha P, Zegans ME, O’Toole GA (2011) Prevalence, conservation and functional analysis of Yersinia and Escherichia CRISPR regions in clinical Pseudomonas aeruginosa isolates. Microbiology 157:430–437

    Article  PubMed  CAS  Google Scholar 

  • Cady KC, Bondy-Denomy J, Heussler GE, Davidson AR, O’Toole GA (2012) The CRISPR/Cas adaptive immune system of Pseudomonas aeruginosa mediates resistance to naturally occurring and engineered phages. J Bacteriol 194:5728–5738

    Article  PubMed  CAS  Google Scholar 

  • Cui Y, Li Y, Gorgé O, Platonov ME, Yan Y, Guo Z, Pourcel C, Dentovskaya SV, Balakhonov SV, Wang X, Song Y, Anisimov AP, Vergnaud G, Yang R (2008) Insight into microevolution of Yersinia pestis by clustered regularly interspaced short palindromic repeats. PLoS ONE 3:e2652

    Article  PubMed  Google Scholar 

  • Datsenko KA, Pougach K, Tikhonov A, Wanner BL, Severinov K, Semenova E (2012) Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system. Nat Commun 3:945

    Article  PubMed  Google Scholar 

  • D’Auria G, Jiménez-Hernández N, Peris-Bondia F, Moya A, Latorre A (2010) Legionella pneumophila pangenome reveals strain-specific virulence factors. BMC Genomics 11:181

    Article  PubMed  Google Scholar 

  • Delaney NF, Balenger S, Bonneaud C, Marx CJ, Hill GE, Ferguson-Noel N, Tsai P, Rodrigo A, Edwards SV (2012) Ultrafast evolution and loss of CRISPRs following a host shift in a novel wildlife pathogen, Mycoplasma gallisepticum. PLoS Genet 8:e1002511

    Article  PubMed  CAS  Google Scholar 

  • Delannoy S, Beutin L, Burgos Y, Fach P (2012) Specific detection of enteroaggregative hemorrhagic Escherichia coli O104:H4 strains using the CRISPR locus as target for a diagnostic real-time PCR. J Clin Microbiol 50:3485−3492

    Article  PubMed  CAS  Google Scholar 

  • Deveau H, Barrangou R, Garneau JE, Labonté J, Fremaux C, Boyaval P, Romero DA, Horvath P, Moineau S (2008) Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J Bacteriol 190:1390–1400

    Article  PubMed  CAS  Google Scholar 

  • Díez-Villaseñor C, Almendros C, García-Martínez J, Mojica FJ (2010) Diversity of CRISPR loci in Escherichia coli. Microbiology 156:1351–1361

    Article  PubMed  Google Scholar 

  • Djordjevic M, Djordjevic M, Severinov K (2012) CRISPR transcript processing: a mechanism for generating a large number of small interfering RNAs. Biol Direct 7:24

    Article  PubMed  Google Scholar 

  • Erdmann S, Garrett RA (2012) Selective and hyperactive uptake of foreign DNA by adaptive immune systems of an archaeon via two distinct mechanisms. Mol Microbiol 85:1044−1056

    Article  PubMed  CAS  Google Scholar 

  • Fabre L, Zhang J, Guigon G, Le Hello S, Guibert V, Accou-Demartin M, de Romans S, Lim C, Roux C, Passet V, Diancourt L, Guibourdenche M, Issenhuth-Jeanjean S, Achtman M, Brisse S, Sola C, Weill FX (2012) CRISPR typing and subtyping for improved laboratory surveillance of Salmonella infections. PLoS ONE 7:e36995

    Article  PubMed  CAS  Google Scholar 

  • Fricke WF, Mammel MK, McDermott PF, Tartera C, White DG, Leclerc JE, Ravel J, Cebula TA (2011) Comparative genomics of 28 Salmonella enterica isolates: evidence for CRISPR-mediated adaptive sublineage evolution. J Bacteriol 193:3556–3568

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Heredia I, Martin-Cuadrado AB, Mojica FJ, Santos F, Mira A, Antón J, Rodriguez-Valera F (2012) Reconstructing viral genomes from the environment using fosmid clones: the case of haloviruses. PLoS ONE 7:e33802

    Article  PubMed  CAS  Google Scholar 

  • Garneau JE, Dupuis MÈ, Villion M, Romero DA, Barrangou R, Boyaval P, Fremaux C, Horvath P, Magadán AH, Moineau S (2010) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468:67–71

    Article  PubMed  CAS  Google Scholar 

  • Garrett RA, Shah SA, Vestergaard G, Deng L, Gudbergsdottir S, Kenchappa CS, Erdmann S, She Q (2011) CRISPR-based immune systems of the Sulfolobales: complexity and diversity. Biochem Soc Trans 39:51–57

    Article  PubMed  CAS  Google Scholar 

  • Gasiunas G, Barrangou R, Horvath P, Siksnys V (2012) Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci U S A 109:E2579−E2586

    Article  PubMed  CAS  Google Scholar 

  • Ginevra C, Jacotin N, Diancourt L, Guigon G, Arquilliere R, Meugnier H, Descours G, Vandenesch F, Etienne J, Lina G, Caro V, Jarraud S (2012) Legionella pneumophila sequence type 1/Paris pulsotype subtyping by spoligotyping. J Clin Microbiol 50:696–701

    Article  PubMed  CAS  Google Scholar 

  • Godde JS, Bickerton A (2006) The repetitive DNA elements called CRISPRs and their associated genes: evidence of horizontal transfer among prokaryotes. J Mol Evol 62:718–729

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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 139:945–956

    Article  PubMed  CAS  Google Scholar 

  • Hale CR, Majumdar S, Elmore J, Pfister N, Compton M, Olson S, Resch AM, Glover CV 3rd, Graveley BR, Terns RM, Terns MP (2012) Essential features and rational design of CRISPR RNAs that function with the Cas RAMP module complex to cleave RNAs. Mol Cell 45:292–302

    Article  PubMed  CAS  Google Scholar 

  • Heidelberg JF, Nelson WC, Schoenfeld T, Bhaya D (2009) Germ warfare in a microbial mat community: CRISPRs provide insights into the co-evolution of host and viral genomes. PLoS ONE 4:e4169

    Article  PubMed  Google Scholar 

  • Held NL, Whitaker RJ (2009) Viral biogeography revealed by signatures in Sulfolobus islandicus genomes. Environ Microbiol 11:457–466

    Article  PubMed  CAS  Google Scholar 

  • Hoe N, Nakashima K, Grigsby D, Pan X, Dou SJ, Naidich S, Garcia M, Kahn E, Bergmire-Sweat D, Musser JM (1999) Rapid molecular genetic subtyping of serotype M1 group A Streptococcus strains. Emerg Infect Dis 5:254–263

    Article  PubMed  CAS  Google Scholar 

  • Horvath P, Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327:167–170

    Article  PubMed  CAS  Google Scholar 

  • Horvath P, Romero DA, Coûté-Monvoisin AC, Richards M, Deveau H, Moineau S, Boyaval P, Fremaux C, Barrangou R (2008) Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J Bacteriol 190:1401–1412

    Article  PubMed  CAS  Google Scholar 

  • Horvath P, Coûté-Monvoisin AC, Romero DA, Boyaval P, Fremaux C, Barrangou R (2009) Comparative analysis of CRISPR loci in lactic acid bacteria genomes. Int J Food Microbiol 131:62–70

    Article  PubMed  CAS  Google Scholar 

  • Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816−821

    Article  PubMed  CAS  Google Scholar 

  • Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8:317–327

    Article  PubMed  CAS  Google Scholar 

  • Liu F, Barrangou R, Gerner-Smidt P, Ribot EM, Knabel SJ, Dudley EG (2011a) Novel virulence gene and clustered regularly interspaced short palindromic repeat (CRISPR) multilocus sequence typing scheme for subtyping of the major serovars of Salmonella enterica subsp. enterica. Appl Environ Microbiol 77:1946–1956

    Article  PubMed  CAS  Google Scholar 

  • Liu F, Kariyawasam S, Jayarao BM, Barrangou R, Gerner-Smidt P, Ribot EM, Knabel SJ, Dudley EG (2011b) Subtyping Salmonella enterica serovar enteritidis isolates from different sources by using sequence typing based on virulence genes and clustered regularly interspaced short palindromic repeats (CRISPRs). Appl Environ Microbiol 77:4520–4526

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Sanchez MJ, Sauvage E, Da Cunha V, Clermont D, Ratsima Hariniaina E, Gonzalez-Zorn B, Poyart C, Rosinski-Chupin I, Glaser P (2012) The highly dynamic CRISPR1 system of Streptococcus agalactiae controls the diversity of its mobilome. Mol Microbiol 85:1057–1071

    Article  PubMed  CAS  Google Scholar 

  • Louwen R, Horst-Kreft D, de Boer AG, van der Graaf L, de Knegt G, Hamersma M, Heikema AP, Timms AR, Jacobs BC, Wagenaar JA, Endtz HP, van der Oost J, Wells JM, Nieuwenhuis EE, van Vliet AH, Willemsen PT, van Baarlen P, van Belkum A (2012) A novel link between Campylobacter jejuni bacteriophage defence, virulence and Guillain-Barré syndrome. Eur J Clin Microbiol Infect Dis. doi:10.1007/s10096-012-1733-4

    PubMed  Google Scholar 

  • Magadán AH, Dupuis MÈ, Villion M, Moineau S (2012) Cleavage of Phage DNA by the Streptococcus thermophilus CRISPR3-Cas System. PLoS ONE 7:e40913

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • McGhee GC, Sundin GW (2012) Erwinia amylovora CRISPR elements provide new tools for evaluating strain diversity and for microbial source tracking. PLoS ONE 7:e41706

    Article  PubMed  CAS  Google Scholar 

  • McShan WM, Ferretti JJ, Karasawa T, Suvorov AN, Lin S, Qin B, Jia H, Kenton S, Najar F, Wu H, Scott J, Roe BA, Savic DJ (2008) Genome sequence of a nephritogenic and highly transformable M49 strain of Streptococcus pyogenes. J Bacteriol 190:7773–7785

    Article  PubMed  CAS  Google Scholar 

  • Mills S, Griffin C, Coffey A, Meijer WC, Hafkamp B, Ross RP (2010) CRISPR analysis of bacteriophage-insensitive mutants (BIMs) of industrial Streptococcus thermophilus—implications for starter design. J Appl Microbiol 108:945–955

    Article  PubMed  CAS  Google Scholar 

  • Mojica FJ, Díez-Villaseñor C, García-Martínez J, Soria E (2005) Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J Mol Evol 60:174–182

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Mokrousov I, Limeschenko E, Vyazovaya A, Narvskaya O (2007) Corynebacterium diphtheriae spoligotyping based on combined use of two CRISPR loci. Biotechnol J 2:901–906

    Article  PubMed  CAS  Google Scholar 

  • Mokrousov I, Vyazovaya A, Kolodkina V, Limeschenko E, Titov L, Narvskaya O (2009) Novel macroarray-based method of Corynebacterium diphtheriae genotyping: evaluation in a field study in Belarus. Eur J Clin Microbiol Infect Dis 28:701–703

    Article  PubMed  CAS  Google Scholar 

  • Nozawa T, Furukawa N, Aikawa C, Watanabe T, Haobam B, Kurokawa K, Mauyama F, Nakagawa I (2011) CRISPR inhibition of prophage acquisition in Streptococcus pyogenes. PLoS ONE 6:e19543

    Article  PubMed  CAS  Google Scholar 

  • Palmer KL, Gilmore MS (2010) Multidrug-resistant enterococci lack CRISPR-cas. MBio 1:e00227–e00310

    Article  PubMed  Google Scholar 

  • Palmer KL, Whiteley M (2011) DMS3-42: the secret to CRISPR-dependent biofilm inhibition in Pseudomonas aeruginosa. J Bacteriol 193:3431–3432

    Article  PubMed  CAS  Google Scholar 

  • Pougach K, Semenova E, Bogdanova E, Datsenko KA, Djordjevic M, Wanner BL, Severinov K (2010) Transcription, processing and function of CRISPR cassettes in Escherichia coli. Mol Microbiol 77:1367–1379

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Price EP, Smith H, Huygens F, Giffard PM (2007) High-resolution DNA melt curve analysis of the clustered, regularly interspaced short-palindromic-repeat locus of Campylobacter jejuni. Appl Environ Microbiol 73:3431–3436

    Article  PubMed  CAS  Google Scholar 

  • Pride DT, Sun CL, Salzman J, Rao N, Loomer P, Armitage GC, Banfield JF, Relman DA (2011) Analysis of streptococcal CRISPRs from human saliva reveals substantial sequence diversity within and between subjects over time. Genome Res 21:126–136

    Article  PubMed  CAS  Google Scholar 

  • Pride DT, Salzman J, Relman DA (2012) Comparisons of clustered regularly interspaced short palindromic repeats and viromes in human saliva reveal bacterial adaptations to salivary viruses. Environ Microbiol 14:2564−2576

    Article  PubMed  CAS  Google Scholar 

  • Rezzonico F, Smits TH, Duffy B (2011) Diversity, evolution, and functionality of clustered regularly interspaced short palindromic repeat (CRISPR) regions in the fire blight pathogen Erwinia amylovora. Appl Environ Microbiol 77:3819–3829

    Article  PubMed  CAS  Google Scholar 

  • Rho M, Wu YW, Tang H, Doak TG, Ye Y (2012) Diverse CRISPRs evolving in human microbiomes. PLoS Genet 8:e1002441

    Article  PubMed  CAS  Google Scholar 

  • Riehm JM, Vergnaud G, Kiefer D, Damdindorj T, Dashdavaa O, Khurelsukh T, Zöller L, Wölfel R, Le Flèche P, Scholz HC (2012) Yersinia pestis lineages in Mongolia. PLoS ONE 7:e30624

    Article  PubMed  CAS  Google Scholar 

  • Sapranauskas R, Gasiunas G, Fremaux C, Barrangou R, Horvath P, Siksnys V (2011) The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Res 39:9275–9282

    Article  PubMed  CAS  Google Scholar 

  • Schouls LM, Reulen S, Duim B, Wagenaar JA, Willems RJ, Dingle KE, Colles FM, Van Embden JD (2003) Comparative genotyping of Campylobacter jejuni by amplified fragment length polymorphism, multilocus sequence typing, and short repeat sequencing: strain diversity, host range, and recombination. J Clin Microbiol 41:15–26

    Article  PubMed  CAS  Google Scholar 

  • Snyder JC, Bateson MM, Lavin M, Young MJ (2010) Use of cellular CRISPR (clusters of regularly interspaced short palindromic repeats) spacer-based microarrays for detection of viruses in environmental samples. Appl Environ Microbiol 76:7251–7258

    Article  PubMed  CAS  Google Scholar 

  • Stern A, Keren L, Wurtzel O, Amitai G, Sorek R (2010) Self-targeting by CRISPR: gene regulation or autoimmunity? Trends Genet 26:335–340

    Article  PubMed  CAS  Google Scholar 

  • Stern A, Mick E, Tirosh I, Sagy O, Sorek R (2012) CRISPR targeting reveals a reservoir of common phages associated with the human gut microbiome. Genome Res 22:1985–1994

    Article  PubMed  CAS  Google Scholar 

  • Sturino JM, Klaenhammer TR (2006) Engineered bacteriophage-defence systems in bioprocessing. Nat Rev Microbiol 4:395–404

    Article  PubMed  CAS  Google Scholar 

  • Swarts DC, Mosterd C, van Passel MW, Brouns SJ (2012) CRISPR interference directs strand specific spacer acquisition. PLoS ONE 7:e35888

    Article  PubMed  CAS  Google Scholar 

  • Tasaki E, Hirayama J, Tazumi A, Hayashi K, Hara Y, Ueno H, Moore JE, Millar BC, Matsuda M (2012) Molecular identification and characterization of clustered regularly interspaced short palindromic repeats (CRISPRs) in a urease-positive thermophilic Campylobacter sp. (UPTC). World J Microbiol Biotechnol 28:713–720

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • van der Ploeg JR (2009) Analysis of CRISPR in Streptococcus mutans suggests frequent occurrence of acquired immunity against infection by M102-like bacteriophages. Microbiology 155:1966–1976

    Article  PubMed  Google Scholar 

  • Vergnaud G, Li Y, Gorgé O, Cui Y, Song Y, Zhou D, Grissa I, Dentovskaya SV, Platonov ME, Rakin A, Balakhonov SV, Neubauer H, Pourcel C, Anisimov AP, Yang R (2007) Analysis of the three Yersinia pestis CRISPR loci provides new tools for phylogenetic studies and possibly for the investigation of ancient DNA. Adv Exp Med Biol 603:327–338

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Zegans ME, Wagner JC, Cady KC, Murphy DM, Hammond JH, O’Toole GA (2009) Interaction between bacteriophage DMS3 and host CRISPR region inhibits group behaviors of Pseudomonas aeruginosa. J Bacteriol 191:210–219

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Abadia E, Refregier G, Tafaj S, Boschiroli ML, Guillard B, Andremont A, Ruimy R, Sola C (2010) Mycobacterium tuberculosis complex CRISPR genotyping: improving efficiency, throughput and discriminative power of ‘spoligotyping’ with new spacers and a microbead-based hybridization assay. J Med Microbiol 59:285–294

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We are indebted to our DuPont colleagues, notably Patrick Boyaval, Christophe Fremaux, and Dennis Romero, and our many academic collaborators with whom we have had the privilege to share exciting times exploring CRISPR-cas systems, notably the Moineau laboratory at Laval, the Banfield laboratory at the University of California Berkeley, the Roberts laboratory at the Pennsylvania State University, the Dudley laboratory at the Pennsylvania State University, the Terns laboratory at the University of Georgia, the Levin laboratory at Emory, the Bhaya laboratory at Stanford University, the VerBerkmoes laboratory at ORNL, Eugene Koonin and Kira Makarova at NCBI, Eric Brown and Marc Allard at FDA, and our dedicated and talented teams. Work in Vilnius was funded by the European Social Fund under Global Grant measure Project R100.

Author information

Authors and Affiliations

  1. DuPont Nutrition and Health, Dangé-Saint-Romain, 86220, France

    Philippe Horvath

  2. Institute of Biotechnology, Vilnius University, LT–02241, Vilnius, Lithuania

    Giedrius Gasiunas & Virginijus Siksnys

  3. DuPont Nutrition and Health, Madison, WI, 53716, USA

    Rodolphe Barrangou

Authors
  1. Philippe Horvath
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Giedrius Gasiunas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Virginijus Siksnys
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rodolphe Barrangou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Philippe Horvath .

Editor information

Editors and Affiliations

  1. DuPont Nutrition and Health, Agriculture Drive 3329, Madison, 53716, Wisconsin, USA

    Rodolphe Barrangou

  2. , Laboratory of Microbiology, University of Wageningen, Dreijenplein 10, Wageningen, 6703 HB, Netherlands

    John van der Oost

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Horvath, P., Gasiunas, G., Siksnys, V., Barrangou, R. (2013). Applications of the Versatile CRISPR-Cas Systems. In: Barrangou, R., van der Oost, J. (eds) CRISPR-Cas Systems. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-34657-6_11

Download citation

Publish with us

Policies and ethics

Search

Navigation