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Improved traceability of Shiga-toxin-producing Escherichia coli using CRISPRs for detection and typing

  • Environmental issues facing Chemical, Biological, Radiological and Nuclear risks
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Abstract

Among strains of Shiga-toxin-producing Escherichia coli (STEC), seven serogroups (O26, O45, O103, O111, O121, O145, and O157) are frequently associated with severe clinical illness in humans. The development of methods for their reliable detection from complex samples such as food has been challenging thus far, and is currently based on the PCR detection of the major virulence genes stx1, stx2, and eae, and O-serogroup-specific genes. However, this approach lacks resolution. Moreover, new STEC serotypes are continuously emerging worldwide. For example, in May 2011, strains belonging to the hitherto rarely detected STEC serotype O104:H4 were identified as causative agents of one of the world’s largest outbreak of disease with a high incidence of hemorrhagic colitis and hemolytic uremic syndrome in the infected patients. Discriminant typing of pathogens is crucial for epidemiological surveillance and investigations of outbreaks, and especially for tracking and tracing in case of accidental and deliberate contamination of food and water samples. Clustered regularly interspaced short palindromic repeats (CRISPRs) are composed of short, highly conserved DNA repeats separated by unique sequences of similar length. This distinctive sequence signature of CRISPRs can be used for strain typing in several bacterial species including STEC. This review discusses how CRISPRs have recently been used for STEC identification and typing.

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References

  • Auvray F, Dilasser F, Bibbal D, Kérourédan M, Oswald E, Brugère H (2012) French cattle is not a reservoir of the highly virulent enteroaggregative Shiga toxin-producing Escherichia coli of serotype O104:H4. Vet Microbiol 158(3-4):443–445. doi:10.1016/j.vetmic.2012.02.029

    Article  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. doi:10.1111/j.1365-2958.2010.07465.x

    Article  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(5819):1709–1712

    Article  CAS  Google Scholar 

  • Beutin L, Miko A, Krause G, Pries K, Haby S, Steege K, Albrecht N (2007) Identification of human-pathogenic strains of Shiga toxin-producing Escherichia coli from food by a combination of serotyping and molecular typing of Shiga toxin genes. Appl Environ Microbiol 73(15):4769–4775

    Article  CAS  Google Scholar 

  • Bielaszewska M, Mellmann A, Zhang W, Köck R, Fruth A, Bauwens A, Peters G, Karch H (2011) Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany, 2011: a microbiological study. Lancet Infect Dis 11(9):671–676. doi:10.1016/S1473-3099(11)70165-7

    Article  CAS  Google Scholar 

  • Bielaszewska M, Mellmann A, Bletz S, Zhang W, Köck R, Kossow A, Prager R, Fruth A, Orth-Höller D, Marejková M, Morabito S, Caprioli A, Piérard D, Smith G, Jenkins C, Curová K, Karch H (2013) Enterohemorrhagic Escherichia coli O26:H11/H-: a new virulent clone emerges in Europe. Clin Infect Dis 56(10):1373–1381. doi:10.1093/cid/cit055

    Article  CAS  Google Scholar 

  • Bland C, Ramsey TL, Sabree F, Lowe M, Brown K, Kyrpides NC, Hugenholtz P (2007) CRISPR Recognition Tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinforma 8(1):209

    Article  Google Scholar 

  • Bourgogne A, Garsin DA, Qin X, Singh KV, Sillanpaa J, Yerrapragada S, Ding Y, Dugan-Rocha S, Buhay C, Shen H, Chen G, Williams G, Muzny D, Maadani A, Fox KA, Gioia J, Chen L, Shang Y, Arias CA, Nallapareddy SR, Zhao M, Prakash VP, Chowdhury S, Jiang H, Gibbs RA, Murray BE, Highlander SK, Weinstock GM (2008) Large scale variation in Enterococcus faecalis illustrated by the genome analysis of strain OG1RF. Genome Biol 9(7):R110. doi:10.1186/gb-2008-9-7-r110

    Article  Google Scholar 

  • Briner AE, Barrangou R (2014) Lactobacillus buchneri genotyping on the basis of clustered regularly interspaced short palindromic repeat (CRISPR) locus diversity. Appl Environ Microbiol 80(3):994–1001. doi:10.1128/AEM.03015-13

    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(5891):960–964. doi:10.1126/science.1159689

    Article  CAS  Google Scholar 

  • Brudey K, Driscoll JR, Rigouts L, Prodinger WM, Gori A, Al-Hajoj SA, Allix C 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  Google Scholar 

  • Buchholz U, Bernard H, Werber D, Böhmer MM, Remschmidt C, Wilking H, Deleré Y, an der Heiden M, Adlhoch C, Dreesman J, Ehlers J, Ethelberg S, Faber M, Frank C, Fricke G, Greiner M, Höhle M, Ivarsson S, Jark U, Kirchner M, Koch J, Krause G, Luber P, Rosner B, Stark K, Kühne M (2011) German outbreak of Escherichia coli O104:H4 associated with sprouts. N Engl J Med 365(19):1763–1770. doi:10.1056/NEJMoa1106482

    Article  CAS  Google Scholar 

  • Bugarel M, Beutin L, Scheutz F, Loukiadis E, Fach P (2011) Identification of genetic markers for differentiation of Shiga toxin-producing, enteropathogenic, and avirulent strains of Escherichia coli O26. Appl Environ Microbiol 77(7):2275–2281. doi:10.1128/AEM.02832-10

    Article  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(Pt 2):430–437. doi:10.1099/mic.0.045732-0

    Article  CAS  Google Scholar 

  • CDC (1997) Outbreaks of Escherichia coli O157:H7 infection associated with eating alfalfa sprouts-Michigan and Virginia, June-July 1997. MMWR Morb Mortal Wkly Rep 46:741–744

    Google Scholar 

  • CDC (2006) Ongoing multistate outbreak of Escherichia coli serotype O157:H7 infections associated with consumption of fresh spinach—United States, September 2006. MMWR Morb Mortal Wkly Rep 55(38):1045–1046

    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(7):e2652. doi:10.1371/journal.pone.0002652

    Article  Google Scholar 

  • Dallman TJ, Byrne L, Launders N, Glen K, Grant KA, Jenkins C (2015) The utility and public health implications of PCR and whole genome sequencing for the detection and investigation of an outbreak of Shiga toxin-producing Escherichia coli serogroup O26:H11. Epidemiol Infect 143(8):1672–1680. doi:10.1017/S0950268814002696

    Article  CAS  Google Scholar 

  • Dang TN, Zhang L, Zöllner S, Srinivasan U, Abbas K, Marrs CF, Foxman B (2013) Uropathogenic Escherichia coli are less likely than paired fecal E. coli to have CRISPR loci. Infect Genet Evol 19:212–218. doi:10.1016/j.meegid.2013.07.017

    Article  CAS  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. doi:10.1038/ncomms1937

    Article  Google Scholar 

  • Delannoy S, Beutin L, Burgos Y, Fach P (2012a) Specific detection of enteroaggregative hemorrhagic Escherichia coli O104:H4 strains by use of the CRISPR locus as a target for a diagnostic real-time PCR. J Clin Microbiol 50:3485–3492. doi:10.1128/JCM.01656-12

    Article  CAS  Google Scholar 

  • Delannoy S, Beutin L, Fach P (2012b) Use of clustered regularly interspaced short palindromic repeat sequence polymorphisms for specific detection of enterohemorrhagic Escherichia coli strains of serotypes O26:H11, O45:H2, O103:H2, O111:H8, O121:H19, O145:H28, and O157:H7 by real-time PCR. J Clin Microbiol 50:4035–4040. doi:10.1128/JCM.02097-12

    Article  CAS  Google Scholar 

  • Delannoy S, Mariani-Kurkdjian P, Bonacorsi S, Liguori S, Fach P (2015) Characteristics of emerging human-pathogenic Escherichia coli O26:H11 strains isolated in France between 2010 and 2013 and carrying the stx2d gene only. J Clin Microbiol 53:486–492. doi:10.1128/JCM.02290-14

    Article  CAS  Google Scholar 

  • Demay C, Liens B, Burguière T, Hill V, Couvin D, Millet J, Mokrousov I, Sola C, Zozio T, Rastogi N (2012) SITVITWEB--a publicly available international multimarker database for studying Mycobacterium tuberculosis genetic diversity and molecular epidemiology. Infect Genet Evol 12(4):755–766. doi:10.1016/j.meegid.2012.02.004

    Article  CAS  Google Scholar 

  • Diez-Villasenor C, Almendros C, Garcia-Martinez J, Mojica FJ (2010) Diversity of CRISPR loci in Escherichia coli. Microbiology 156:1351–1361. doi:10.1099/mic.0.036046-0

    Article  CAS  Google Scholar 

  • Edgar RC, Myers EW (2005) PILER: identification and classification of genomic repeats. Bioinformatics 21(Suppl 1):i152–i158

    Article  CAS  Google Scholar 

  • EFSA Panel on Biological Hazards (BIOHAZ) (2013a) Scientific opinion on VTEC—seropathotype and scientific criteria regarding pathogenicity assessment. EFSA J 11(4):3138. doi:10.2903/j.efsa.2013.3138, 106 pp

    Google Scholar 

  • EFSA Panel on Biological Hazards (BIOHAZ) (2013b) Scientific opinion on the evaluation of molecular typing methods for major food-borne microbiological hazards and their use for attribution modelling, outbreak investigation and scanning surveillance: part 1 (evaluation of methods and applications). EFSA J 11(12):3502, 84 pp

    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(5):e36995. doi:10.1371/journal.pone.0036995

    Article  CAS  Google Scholar 

  • Fabre L, Le Hello S, Roux C, Issenhuth-Jeanjean S, Weill FX (2014) CRISPR is an optimal target for the design of specific PCR assays for Salmonella enterica serotypes Typhi and Paratyphi A. PLoS Negl Trop Dis 8(1):e2671. doi:10.1371/journal.pntd.0002671

    Article  Google Scholar 

  • Feng PC, Delannoy S, Lacher DW, Dos Santos LF, Beutin L, Fach P, Rivas M, Hartland EL, Paton AW, Guth BE (2014) Genetic diversity and virulence potential of shiga toxin-producing Escherichia coli O113:H21 strains isolated from clinical, environmental, and food sources. Appl Environ Microbiol 80:4757–4763. doi:10.1128/AEM.01182-14

    Article  Google Scholar 

  • Franz E, Delaquis P, Morabito S, Beutin L, Gobius K, Rasko DA, Bono J, French N, Osek J, Lindstedt BA, Muniesa M, Manning S, LeJeune J, Callaway T, Beatson S, Eppinger M, Dallman T, Forbes KJ, Aarts H, Pearl DL, Gannon VPJ, Laing CR, Strachan NJC (2014) Exploiting the explosion of information associated with whole genome sequencing to tackle Shiga toxin-producing Escherichia coli (STEC) in global food production systems. Int J Food Microbiol 187:57–72. doi:10.1016/j.ijfoodmicro.2014.07.002

    Article  Google Scholar 

  • FSIS (2013) FSIS verification testing for non-O157 Shiga toxin-producing Escherichia coli (non-O157 STEC) under MT60, MT52, and MT53 sampling programs. USDA FSIS, Washington, DC

    Google Scholar 

  • García-Gutiérrez E, Almendros C, Mojica FJM, Guzmán NM, García-Martínez J (2015) CRISPR content correlates with the pathogenic potential of Escherichia coli. PLoS ONE 10(7):e0131935. doi:10.1371/journal.pone.0131935

    Article  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(3):696–701. doi:10.1128/JCM.06180-11

    Article  CAS  Google Scholar 

  • González J, Sanso AM, Lucchesi PM, Bustamante AV (2014) Comparison of 2 proposed MLVA protocols for subtyping non-O157:H7 verotoxigenic Escherichia coli. Diagn Microbiol Infect Dis 78(4):328–332. doi:10.1016/j.diagmicrobio.2013.10.017

    Article  Google Scholar 

  • Grissa I, Vergnaud G, Pourcel C (2007a) The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinforma 8:172

    Article  Google Scholar 

  • Grissa I, Vergnaud G, Pourcel C (2007b) CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 35(Web Server issue):W52–W57

    Article  Google Scholar 

  • Haft DH, Selengut J, Mongodin EF, Nelson KE (2005) A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Comput Biol 1(6):e60

    Article  Google Scholar 

  • Han W, Liu B, Cao B, Beutin L, Krüger U, Liu H, Li Y, Liu Y, Feng L, Wang L (2007) DNA microarray-based identification of serogroups and virulence gene patterns of Escherichia coli isolates associated with porcine postweaning diarrhea and edema disease. Appl Environ Microbiol 73(12):4082–4088. doi:10.1128/AEM.01820-06

    Article  CAS  Google Scholar 

  • Holmes A, Perry N, Willshaw G, Hanson M, Allison L (2015) Inter-laboratory comparison of multi-locus variable-number tandem repeat analysis (MLVA) for verocytotoxin-producing Escherichia coli O157 to facilitate data sharing. Epidemiol Infect 143(1):104–107. doi:10.1017/S0950268814000739

    Article  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(4):1401–1412

    Article  CAS  Google Scholar 

  • Hyytia-Trees E, Lafon P, Vauterin P, Ribot EM (2010) Multilaboratory validation study of standardized multiple-locus variable-number tandem repeat analysis protocol for shiga toxin-producing Escherichia coli O157: a novel approach to normalize fragment size data between capillary electrophoresis platforms. Foodborne Pathog Dis 7(2):129–136. doi:10.1089/fpd.2009.0371

    Article  CAS  Google Scholar 

  • International Organization for Standardization (ISO) (2012) ISO/TS 13136:2012 “Microbiology of food and animal feed—real-time polymerase chain reaction (PCR)-based method for the detection of food-borne pathogens–horizontal method for the detection of Shiga toxin-producing Escherichia coli(STEC) and the determination of O157, O111, O26, O103 and O145 serogroups”. In: International Organization for Standardization. ISO Central Secretariat, Geneva, Switzerland

  • Ishino Y, Shinagawa H, Makino K, Amemura M, Nakata A (1987) Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J Bacteriol 169(12):5429–5433

    CAS  Google Scholar 

  • Ison SA, Delannoy S, Bugarel M, Nightingale KK, Webb HE, Renter DG, Nagaraja TG, Loneragan GH, Fach P (2015) Genetic diversity and pathogenic potential of attaching and effacing Escherichia coli O26:H11 strains recovered from bovine feces in the United States. Appl Environ Microbiol 81:3671–3678. doi:10.1128/AEM.00397-15

    Article  CAS  Google Scholar 

  • Jackson RN, Golden SM, van Erp PBG, Carter J, Westra ER, Brouns SJJ, van der Oost J, Terwilliger TC, Read RJ, Wiedenheft B (2014) Crystal structure of the CRISPR RNA-guided surveillance complex from Escherichia coli. Science 345:1473–1479. doi:10.1126/science.1256328

    Article  CAS  Google Scholar 

  • Jenkins C, Dallman TJ, Launders N, Willis C, Byrne L, Jorgensen F, Eppinger M, Adak GK, Aird H, Elviss N, Grant KA, Morgan D, McLauchlin J (2015) Public health investigation of two outbreaks of shiga toxin-producing Escherichia coli O157 associated with consumption of watercress. Appl Environ Microbiol 81(12):3946–3952. doi:10.1128/AEM.04188-14

    Article  CAS  Google Scholar 

  • Jiang Y, Yin S, Dudley EG, Cutter CN (2015) Diversity of CRISPR loci and virulence genes in pathogenic Escherichia coli isolates from various sources. Int J Food Microbiol 204:41–46. doi:10.1016/j.ijfoodmicro.2015.03.025

    Article  CAS  Google Scholar 

  • Joensen KG, Scheutz F, Lund O, Hasman H, Kaas RS, Nielsen EM, Aarestrup FM (2014) Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J Clin Microbiol 52(5):1501–1510. doi:10.1128/JCM.03617-13

    Article  Google Scholar 

  • Kamerbeek J, Schouls L, Kolk A, van Agterveld M, van Soolingen D, Kuijper S, Bunschoten A, Molhuizen H, Shaw R, Goyal M, van Embden J (1997) Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol 35(4):907–914

    CAS  Google Scholar 

  • Karama M, Gyles CL (2010) Methods for genotyping verotoxin-producing Escherichia coli. Zoonoses Public Health 57(7-8):447–462. doi:10.1111/j.1863-2378.2009.01259.x

    Article  CAS  Google Scholar 

  • King LA, Nogareda F, Weill FX, Mariani-Kurkdjian P, Loukiadis E, Gault G, Jourdan-DaSilva N, Bingen E, Macé M, Thevenot D, Ong N, Castor C, Noël H, Van Cauteren D, Charron M, Vaillant V, Aldabe B, Goulet V, Delmas G, Couturier E, Le Strat Y, Combe C, Delmas Y, Terrier F, Vendrely B, Rolland P, de Valk H (2012) Outbreak of Shiga toxin-producing Escherichia coli O104:H4 associated with organic fenugreek sprouts, France, June 2011. Clin Infect Dis 54(11):1588–1594. doi:10.1093/cid/cis255

    Article  CAS  Google Scholar 

  • Kupczok A, Bollback JP (2013) Probabilistic models for CRISPR spacer content evolution. BMC Evol Biol 13:54. doi:10.1186/1471-2148-13-54

    Article  Google Scholar 

  • Kupczok A, Landan G, Dagan T (2015) The contribution of genetic recombination to CRISPR array evolution. Genome Biol Evol

  • Larsson JT, Torpdahl M, MLVA Working Group, Møller Nielsen E (2013) Proof-of-concept study for successful inter-laboratory comparison of MLVA results. Euro Surveill 18(35):20566

    Article  CAS  Google Scholar 

  • Lazzarini LC, Rosenfeld J, Huard RC, Hill V, Lapa e Silva JR, DeSalle R, Rastogi N, Ho JL (2012) Mycobacterium tuberculosis spoligotypes that may derive from mixed strain infections are revealed by a novel computational approach. Infect Genet Evol 12:798–806. doi:10.1016/j.meegid.2011.08.028

    Article  Google Scholar 

  • Liu F, Barrangou R, Gerner-Smidt P, Ribot EM, Knabel SJ, Dudley EG (2011) 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(6):1946–1956. doi:10.1128/AEM.02625-10

    Article  CAS  Google Scholar 

  • Magnus T, Rother J, Simova O, Meier-Cillien M, Repenthin J, Moller F, Gbadamosi J, Panzer U, Wengenroth M, Hagel C, Kluge S, Stahl RK, Wegscheider K, Urban P, Eckert B, Glatzel M, Fiehler J, Gerloff C (2012) The neurological syndrome in adults during the 2011 northern German E. coli serotype O104:H4 outbreak. Brain 135:1850–1859. doi:10.1093/brain/aws090

    Article  Google Scholar 

  • Makarova KS, Grishin NV, Shabalina SA, Wolf YI, Koonin EV (2006) A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol Direct 1:7

    Article  Google Scholar 

  • Makarova KS, Haft DH, Barrangou R, Brouns SJ, Charpentier E, Horvath P, Moineau S, Mojica FJ, Wolf YI, Yakunin AF, van der Oost J, Koonin EV (2011) Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 9(6):467–477. doi:10.1038/nrmicro2577

    Article  CAS  Google Scholar 

  • Martikainen O, Kagambèga A, Bonkoungou IJ, Barro N, Siitonen A, Haukka K (2012) Characterization of Shigatoxigenic Escherichia coli strains from Burkina Faso. Foodborne Pathog Dis 9(11):1015–1021. doi:10.1089/fpd.2012.1228

    Article  CAS  Google Scholar 

  • Michino H, Araki K, Minami S, Takaya S, Sakai N, Miyazaki M, Ono A, Yanagawa H (1999) Massive outbreak of Escherichia coli O157:H7 infection in schoolchildren in Sakai City, Japan, associated with consumption of white radish sprouts. Am J Epidemiol 150(8):787–796

    Article  CAS  Google Scholar 

  • Miko A, Lindstedt BA, Brandal LT, Løbersli I, Beutin L (2010) Evaluation of multiple-locus variable number of tandem-repeats analysis (MLVA) as a method for identification of clonal groups among enteropathogenic, enterohaemorrhagic and avirulent Escherichia coli O26 strains. FEMS Microbiol Lett 303(2):137–146. doi:10.1111/j.1574-6968.2009.01874.x

    Article  CAS  Google Scholar 

  • Mojica FJ, Díez-Villaseñor C, Soria E, Juez G (2000) Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondria. Mol Microbiol 36(1):244–246

    Article  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(2):174–182

    Article  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(Pt 3):733–740. doi:10.1099/mic.0.023960-0

    Article  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(7):901–906

    Article  CAS  Google Scholar 

  • Nataro JP, Kaper JB (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11(1):142–201

    CAS  Google Scholar 

  • Paddock ZD, Bai J, Shi X, Renter DG, Nagaraja TG (2013) Detection of Escherichia coli O104 in the feces of feedlot cattle by a multiplex PCR assay designed to target major genetic traits of the virulent hybrid strain responsible for the 2011 German outbreak. Appl Environ Microbiol 79(11):3522–3525. doi:10.1128/AEM.00246-13

    Article  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(6):1367–1379. doi:10.1111/j.1365-2958.2010.07265.x

    Article  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(Pt 3):653–663

    Article  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(10):3431–3436

    Article  CAS  Google Scholar 

  • Pul U, Wurm R, Arslan Z, Geissen R, Hofmann N, Wagner R (2010) Identification and characterization of E. coli CRISPR-cas promoters and their silencing by H-NS. Mol Microbiol 75(6):1495–1512. doi:10.1111/j.1365-2958.2010.07073.x

    Article  CAS  Google Scholar 

  • Ratner HK, Sampson TR, Weiss DS (2015) 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 28(3):267–274. doi:10.1097/QCO.0000000000000154

    Article  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(11):3819–3829. doi:10.1128/AEM.00177-11

    Article  CAS  Google Scholar 

  • Rohde H, Qin J, Cui Y, Li D, Loman NJ, Hentschke M, Chen W, Pu F, Peng Y, Li J, Xi F, Li S, Li Y, Zhang Z, Yang X, Zhao M, Wang P, Guan Y, Cen Z, Zhao X, Christner M, Kobbe R, Loos S, Oh J, Yang L, Danchin A, Gao GF, Song Y, Li Y, Yang H, Wang J, Xu J, Pallen MJ, Wang J, Aepfelbacher M, Yang R, E. coli O104:H4 Genome Analysis Crowd-Sourcing Consortium (2011) Open-source genomic analysis of Shiga-toxin-producing E. coli O104:H4. N Engl J Med 365(8):718–724. doi:10.1056/NEJMoa1107643

    Article  CAS  Google Scholar 

  • Rousseau C, Gonnet M, Le Romancer M, Nicolas J (2009) CRISPI: a CRISPR interactive database. Bioinformatics 25(24):3317–3318. doi:10.1093/bioinformatics/btp586

    Article  CAS  Google Scholar 

  • Sampson TR, Saroj SD, Llewellyn AC, Tzeng YL, Weiss DS (2013) A CRISPR/Cas system mediates bacterial innate immune evasion and virulence. Nature 497:254–257. doi:10.1038/nature12048

    Article  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(1):15–26

    Article  CAS  Google Scholar 

  • Serbanescu MA, Cordova M, Krastel K, Flick R, Beloglazova N, Latos A, Yakunin AF, Senadheera DB, Cvitkovitch DG (2015) Role of the Streptococcus mutans CRISPR-Cas systems in immunity and cell physiology. J Bacteriol 197(4):749–761. doi:10.1128/JB.02333-14

    Article  CAS  Google Scholar 

  • Shariat N, Dudley EG (2014) CRISPRs: molecular signatures used for pathogen subtyping. Appl Environ Microbiol 80:430–439. doi:10.1128/AEM.02790-13

    Article  CAS  Google Scholar 

  • Sola C (2015) Clustured regularly interspersed short palindromic repeats (CRISPR) genetic diversity studies as a mean to reconstruct the evolution of the Mycobacterium tuberculosis complex. Tuberculosis (Edinb) 95(Suppl 1):S159–S166. doi:10.1016/j.tube.2015.02.029

    Article  CAS  Google Scholar 

  • Sorek R, Kunin V, Hugenholtz P (2008) CRISPR—a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat Rev Microbiol 6(3):181–186

    Article  CAS  Google Scholar 

  • Swaminathan B, Barrett TJ, Hunter SB, Tauxe RV, PulseNet Task Force CDC (2001) PulseNet: the molecular subtyping network for foodborne bacterial disease surveillance, United States. Emerg Infect Dis 7(3):382–389

    Article  CAS  Google Scholar 

  • Swaminathan B, Gerner-Smidt P, Ng LK, Lukinmaa S, Kam KM, Rolando S, Gutiérrez EP, Binsztein N (2006) Building PulseNet International: an interconnected system of laboratory networks to facilitate timely public health recognition and response to foodborne disease outbreaks and emerging foodborne diseases. Foodborne Pathog Dis 3(1):36–50

    Article  Google Scholar 

  • Swarts DC, Mosterd C, van Passel MW, Brouns SJ (2012) CRISPR interference directs strand specific spacer acquisition. PLoS One 7(4):e35888. doi:10.1371/journal.pone.0035888

    Article  CAS  Google Scholar 

  • The European Commission (EC) (2013) Commission regulation (EU) No 209/2013 of 11 March 2013 amending regulation (EC) No 2073/2005 as regards microbiological criteria for sprouts and the sampling rules for poultry carcasses and fresh poultry meat. Off J Eur Union L68:19–23

    Google Scholar 

  • Toro M, Cao G, Ju W, Allard M, Barrangou R, Zhao S, Brown E, Meng J (2014) Association of clustered regularly interspaced short palindromic repeat (CRISPR) elements with specific serotypes and virulence potential of Shiga toxin-producing Escherichia coli. Appl Environ Microbiol 80:1411–1420. doi:10.1128/AEM.03018-13

    Article  Google Scholar 

  • Touchon M, Rocha EP (2010) The small, slow and specialized CRISPR and anti-CRISPR of Escherichia and Salmonella. PLoS One 5:e11126. doi:10.1371/journal.pone.0011126

    Article  Google Scholar 

  • Touchon M, Charpentier S, Clermont O, Rocha EP, Denamur E, Branger C (2011) CRISPR distribution within the Escherichia coli species is not suggestive of immunity-associated diversifying selection. J Bacteriol 193(10):2460–2467. doi:10.1128/JB.01307-10

    Article  CAS  Google Scholar 

  • Ullrich S, Bremer P, Neumann-Grutzeck C, Otto H, Rüther C, von Seydewitz CU, Meyer GP, Ahmadi-Simab K, Röther J, Hogan B, Schwenk W, Fischbach R, Caselitz J, Puttfarcken J, Huggett S, Tiedeken P, Pober J, Kirkiles-Smith NC, Hagenmüller F (2013) Symptoms and clinical course of EHEC O104 infection in hospitalized patients: a prospective single center study. PLoS One 8(2):e55278. doi:10.1371/journal.pone.0055278

    Article  CAS  Google Scholar 

  • USDA/FSIS (2011) MLG5B.01 FSIS laboratory methods: non O157 STEC in meat products. In: US Department of Agriculture (Ed.), US Department of Agriculture

  • Vale PF, Little TJ (2010) CRISPR-mediated phage resistance and the ghost of coevolution past. Proc Biol Sci 277(1691):2097–2103. doi:10.1098/rspb.2010.0055

    Article  CAS  Google Scholar 

  • Watanabe Y, Ozasa K, Mermin JH, Griffin PM, Masuda K, Imashuku S, Sawada T (1999) Factory outbreak of Escherichia coli O157:H7 infection in Japan. Emerg Infect Dis 5(3):424–428

    Article  CAS  Google Scholar 

  • Wieczorek K, Beutin L, Osek J (2011) Rare VTEC serotypes of potential zoonotic risk isolated from bovine hides and carcasses. Vet Rec 168(3):80. doi:10.1136/vr.c5263

    Article  CAS  Google Scholar 

  • Wieler LH, Semmler T, Eichhorn I, Antao EM, Kinnemann B, Geue L, Karch H, Guenther S, Bethe A (2011) No evidence of the Shiga toxin-producing E. coli O104:H4 outbreak strain or enteroaggregative E. coli (EAEC) found in cattle faeces in northern Germany, the hotspot of the 2011 HUS outbreak area. Gut Pathog 3(1):17. doi:10.1186/1757-4749-3-17

    Article  CAS  Google Scholar 

  • Yin S, Jensen MA, Bai J, Debroy C, Barrangou R, Dudley EG (2013) The evolutionary divergence of Shiga toxin-producing Escherichia coli is reflected in clustered regularly interspaced short palindromic repeat (CRISPR) spacer composition. Appl Environ Microbiol 79(18):5710–5720. doi:10.1128/AEM.00950-13

    Article  CAS  Google Scholar 

  • Yosef I, Shitrit D, Goren MG, Burstein D, Pupko T, Qimron U (2013) DNA motifs determining the efficiency of adaptation into the Escherichia coli CRISPR array. Proc Natl Acad Sci U S A 110(35):14396–14401. doi:10.1073/pnas.1300108110

    Article  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(1):210–219. doi:10.1128/JB.00797-08

    Article  CAS  Google Scholar 

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Acknowledgments

This project was partly funded by the French joint ministerial program of R&D against CBRNE risks (Grant No. C17609-2).

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Authors and Affiliations

  1. ANSES, Food Safety Laboratory, Platform IdentyPath, Université Paris-Est, Maisons-Alfort, France

    Sabine Delannoy & Patrick Fach

  2. Federal Institute for Risk Assessment (BfR), Berlin, Germany

    Lothar Beutin

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  1. Sabine Delannoy
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  2. Lothar Beutin
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  3. Patrick Fach
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Correspondence to Sabine Delannoy.

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Delannoy, S., Beutin, L. & Fach, P. Improved traceability of Shiga-toxin-producing Escherichia coli using CRISPRs for detection and typing. Environ Sci Pollut Res 23, 8163–8174 (2016). https://doi.org/10.1007/s11356-015-5446-y

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