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Annual Review of Food Science and Technology

Volume 8, 2017

CRISPR-Cas Technologies and Applications in Food Bacteria

Abstract

Clustered regularly interspaced short palindromic repeats (CRISPRs) and CRISPR-associated (Cas) proteins form adaptive immune systems that occur in many bacteria and most archaea. In addition to protecting bacteria from phages and other invasive mobile genetic elements, CRISPR-Cas molecular machines can be repurposed as tool kits for applications relevant to the food industry. A primary concern of the food industry has long been the proper management of food-related bacteria, with a focus on both enhancing the outcomes of beneficial microorganisms such as starter cultures and probiotics and limiting the presence of detrimental organisms such as pathogens and spoilage microorganisms. This review introduces CRISPR-Cas as a novel set of technologies to manage food bacteria and offers insights into CRISPR-Cas biology. It primarily focuses on the applications of CRISPR-Cas systems and tools in starter cultures and probiotics, encompassing strain-typing, phage resistance, plasmid vaccination, genome editing, and antimicrobial activity.

Keyword(s): antimicrobial, cultures, genome editing, phage resistance, plasmid vaccination, probiotics, strain-typing
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/content/journals/10.1146/annurev-food-072816-024723
2017-02-28
2024-04-26
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Literature Cited

  1. Abudayyeh OO, Gootenberg JS, Konermann S, Joung J, Slaymaker IM. et al. 2016. C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science 353:aaf5573 [Google Scholar]
  2. Andersson AF, Banfield JF. 2008. Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320:58791047–50 [Google Scholar]
  3. 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. Nucleic Acids Res 42:127884–93 [Google Scholar]
  4. Barrangou R. 2014. Cas9 targeting and the CRISPR revolution. Science 344:6185707–8 [Google Scholar]
  5. Barrangou R. 2015a. The roles of CRISPR-Cas systems in adaptive immunity and beyond. Curr. Opin. Immunol. 32:36–41 [Google Scholar]
  6. Barrangou R. 2015b. Diversity of CRISPR-Cas immune systems and molecular machines. Genome Biol 16:247 [Google Scholar]
  7. Barrangou R, Coûté-Monvoisin AC, Stahl B, Chavichvily I, Damange F. et al. 2013. Genomic impact of CRISPR immunization against bacteriophages. Biochem. Soc. Trans. 41:61383–91 [Google Scholar]
  8. Barrangou R, Dudley EG. 2016. CRISPR-based typing and next-generation tracking. Annu. Rev. Food Sci. Technol. 7:395–411 [Google Scholar]
  9. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P. et al. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:58191709–12 [Google Scholar]
  10. Barrangou R, Horvath P. 2012. CRISPR: new horizons in phage resistance and strain identification. Annu. Rev. Food Sci. Technol. 3:143–62 [Google Scholar]
  11. Barrangou R, van Pijkeren JP. 2016. Exploiting CRISPR-Cas immune systems for genome editing in bacteria. Curr. Opin. Biotechnol. 37:61–68 [Google Scholar]
  12. Benda C, Ebert J, Scheltema RA, Schiller HB, Baumgartner M. et al. 2014. Structural model of a CRISPR RNA-silencing complex reveals the RNA-target cleavage activity in Cmr4. Mol. Cell 56:143–54 [Google Scholar]
  13. Beisel CL, Gomaa AA, Barrangou R. 2014. A CRISPR design for next-generation antimicrobials. Genome Biol 15:516 [Google Scholar]
  14. Bikard D, Euler CW, Jiang W, Nussenzweig PM, Goldberg GW. et al. 2014. Exploiting the CRISPR-Cas nucleases to produce sequence-specific antimicrobials. Nat. Biotechnol. 32:111146–50 [Google Scholar]
  15. Bolotin A, Ouinquis B, Sorokin A, Ehrlich SD. 2005. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151:2551–61 [Google Scholar]
  16. Bourdichon F, Casaregola S, Farrokh C, Frisvad JC, Gerds ML. et al. 2012. Food fermentations: microorganisms with technological beneficial use. Int. J. Food Microbiol. 154:387–97 [Google Scholar]
  17. Briner AE, Barrangou R. 2014. Lactobacillus buchneri genotyping on the basis of clustered regularly interspaced short palindromic repeat (CRISPR) locus diversity. Appl. Environ. Microbiol. 80:3994–1001 [Google Scholar]
  18. Briner AE, Donohoue PD, Gomaa AA, Selle K, Slorach EM. et al. 2014. Guide RNA functional modules direct Cas9 activity and orthogonality. Mol. Cell 53:333–39 [Google Scholar]
  19. Briner AE, Lugli GA, Milani C, Duranti S, Turroni F. et al. 2015. Occurrence and diversity of CRISPR-Cas systems in the genus Bifidobacterium. PLOS ONE 10:7e0133661 [Google Scholar]
  20. Broadbent JR, Neeno-Eckwall EC, Stahl B, Tandee K, Cai H. et al. 2012. Analysis of the Lactobacillus casei supragenome and its influence in species evolution and lifestyle adaptation. BMC Genom 13:533 [Google Scholar]
  21. Brouns SJJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJH. et al. 2008. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321:5891960–64 [Google Scholar]
  22. Caplice E, Fitzgerald GF. 1999. Food fermentations: role of microorganisms in food production and preservation. Int. J. Food. Microbiol. 50:1–2131–49 [Google Scholar]
  23. Carte J, Christopher RT, Smith JT, Olson S, Barrangou R. et al. 2014. The three major types of CRISPR-Cas systems function independently in CRISPR RNA biogenesis in Streptococcus thermophilus. Mol. Microbiol. 93:198–112 [Google Scholar]
  24. Carte J, Wang R, Li H, Terns RM, Terns MP. 2008. Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes Dev 22:3489–96 [Google Scholar]
  25. Citorik RJ, Mimee M, Lu TK. 2014. Sequence-specific antimicrobials using efficiently delivered RNA-guided nucleases. Nat. Biotechnol. 32:1141–45 [Google Scholar]
  26. Datsenko KA, Pougach A, 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 [Google Scholar]
  27. D'Auria G, Jimenez-Hernandez N, Peris-Bondia F, Moya A, Latorre A. 2010. Legionella pneumophila pangenome reveals strain-specific virulence factors. BMC Genom 11:181 [Google Scholar]
  28. Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao YJ. et al. 2011. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471:7340602–7 [Google Scholar]
  29. Deng L, Garrett RA, Shah SA, Peng X, She Q. 2013. A novel interference mechanism by a type IIIB CRISPR-Cmr module in Sulfolobus. Mol. Microbiol. 87:51088–99 [Google Scholar]
  30. Deveau H, Barrangou R, Garneau JE, J Labonté, Fremaux C. et al. 2008. Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J. Bacteriol. 190:1390–400 [Google Scholar]
  31. DiMarzio M, Shariat N, Kariyawasam S, Barrangou R, Dudley EG. 2013. Antibiotic resistance in Salmonella enterica serovar Typhimurium associates with CRISPR sequence type. Antimicrob. Agents Chemother. 57:94282–89 [Google Scholar]
  32. Djordjevic GM, O'Sullivan DJ, Walker SA, Conkling MA, Klaenhammer TR. 1997. A triggered-suicide system designed as a defense against bacteriophages. J. Bacteriol. 179:216741–48 [Google Scholar]
  33. Doudna JA, Charpentier E. 2014. Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346:62131258096 [Google Scholar]
  34. Douglas GL, Klaenhammer TR. 2010. Genomic evolution of domesticated microorganisms. Annu. Rev. Food Sci. Technol. 1:397–414 [Google Scholar]
  35. Douillard FP, Ribbera A, Kant R, TA Pietilä, Järvinen HM. et al. 2013. Comparative genomic and functional analysis of 100 Lactobacillusrhamnosus strains and their comparison with strain GG. PLOS ONE 9:8e1003683 [Google Scholar]
  36. Durmaz E, Klaenhammer TR. 2007. Abortive phage resistance mechanism AbiZ speeds the lysis clock to cause premature lysis of phage-infected Lactococcus lactis. J. Bacteriol. 189:41417–25 [Google Scholar]
  37. Edgar R, Qimron U. 2010. The Escherichia coli CRISPR system protects from lambda lysogenization, lysogens, and prophage induction. J. Bacteriol. 192:6291–94 [Google Scholar]
  38. Edmond E, Moineau S. 2007. Bacteriophages and food fermentations. Bacteriophage: Genetics and Molecular Biology S McGrath, D van Sinderen 93–124 Poole, UK: Caister Acad. [Google Scholar]
  39. Fabre L, Zhang J, Guigon G, Hello SL, Guibert V. et al. 2012. CRISPR typing and subtyping for improved laboratory surveillance of Salmonella infections. PLOS ONE 7:5e36995 [Google Scholar]
  40. Fagerlund RD, Staals RHJ, Fineran PC. 2015. The Cpf1 CRISPR-Cas protein expands genome-editing tools. Genome Biol 16:251 [Google Scholar]
  41. FAO/WHO. 2002. Guidelines for the Evaluation of Probiotics in Food London, ON: FAO/WHO
  42. Fonfara I, Richter H, Bratovič M, Le Rhun A, Charpentier E. 2016. The CRISPR-associated DNA-cleaving enzyme Cpf1 also processes precursor CRISPR RNA. Nature 532:517–21 [Google Scholar]
  43. Fox PF. 1993. Cheese: an overview. Cheese: Chemistry, Physics and Microbiology PF Fox 1–36 New York: Springer [Google Scholar]
  44. Fricke WF, Mammel MK, McDermott PF, Tartera C, White DG. et al. 2011. Comparative genomics of 28 Salmonellaenterica isolates: Evidence for CRISPR-mediated adaptive sublineage evolution. J. Bacteriol. 193:143556–68 [Google Scholar]
  45. Garneau JE, Dupuis ME, Villion M, Romero DA, Barrangou R. et al. 2010. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468:67–71 [Google Scholar]
  46. Gasiunas G, Barrangou R, Horvath P, Siksnys V. 2012. Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. PNAS 109:39E2579–86 [Google Scholar]
  47. Gomaa AA, Klumpe HE, Luo ML, Selle K, Barrangou R, Beisel CL. 2014. Programmable removal of bacterial strains by use of genome-targeting CRISPR-Cas systems. mBio 5:1e00928–13 [Google Scholar]
  48. Grissa I, Vergnaud G, Pourcel C. 2007. CRISPRFinder: A webtool to identify clustered regularly interspersed short palindromic repeats. Nucleic Acids Res 35:W52–57 [Google Scholar]
  49. Hale C, Kleppe K, Terns RM, Terns MP. 2008. Prokaryotic silencing (psi)RNAs in Pyrococcus furiosus. RNA 14:122572–79 [Google Scholar]
  50. Hale CR, Majumdar S, Elmore J, Plister N, Compton M. et al. 2012. Essential features and rational design of CRISPR RNAs that function with the Cas RAMP module complex to cleave RNAs. Mol. Cell 45:3292–302 [Google Scholar]
  51. Hale CR, Zhao P, Olson S, Duff MO, Gravely BR. et al. 2009. RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 139:5945–56 [Google Scholar]
  52. 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. 288:27888–97 [Google Scholar]
  53. Hargreaves KR, Flores CO, Lawley TD, Clokie MRJ. 2014. Abundant and diverse clustered regularly interspaced short palindromic repeat spacers in Clostridium difficile strains and prophages target multiple phage types within this pathogen. mBio 5:5e01045–13 [Google Scholar]
  54. Hesseltine CS. 1992. Mixed culture fermentations. Applications of Biotechnology to Fermented Foods: Report of an ad hoc Panel of the Board on Science and Technology for International Development Natl. Res. Counc 52–57 Washington, DC: Natl. Acad. Press [Google Scholar]
  55. Higgins DL, Sanozky-Dawes RB, Klaenhammer TR. 1988. Restriction and modification activities from Streptococcus lactis ME are encoded by a self-transmissible plasmid, pTN20, that forms cointegrates during mobilization of lactose-fermenting ability. J. Bacteriol. 170:83435–42 [Google Scholar]
  56. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ. et al. 2014. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics consensus statement on the score and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. 11:506–14 [Google Scholar]
  57. Hirano H, Gootenberg JS, Horii T, Abudayyeh OO, Kimura M. et al. 2016. Structure and engineering of Francisella novicida Cas9. Cell 164:5950–61 [Google Scholar]
  58. Hochstrasser ML, Taylor DW, Bhat P, Guegler CK, Sternberg SH. et al. 2014. CasA mediates Cas3-catalyzed target degradation during CRISPR RNA-guided interference. PNAS 111:186618–23 [Google Scholar]
  59. Horvath P, Romero DA, Coûté-Monvoisin AC, Richards M, Deveau H. et al. 2008. Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J. Bacteriol. 190:41401–12 [Google Scholar]
  60. Horvath P, Barrangou R. 2011. Protection against foreign DNA. Bacterial Stress Responses G Storz, R Hengge 333–48 Washington, DC: ASM Press, 2nd. ed. [Google Scholar]
  61. Huis in't Veld JHJ. 1996. Microbial and biochemical spoilage of foods: an overview. Int. J. Food Microbiol. 33:11–18 [Google Scholar]
  62. Hullahalli K, Rodrigues M, Schmidt BD, Li X, Bhardwaj P, Palmer KL. 2015. Comparative analysis of the orphan CRISPR2 locus in 242 Enterococcus faecalis strains. PLOS ONE 10:9e0138890 [Google Scholar]
  63. Huo Y, Nam KH, Ding F, Lee H, Wu L. et al. 2014. Structures of CRISPR Cas3 offer mechanistic insights into Cascade-activated DNA unwinding and degradation. Nat. Struct. Mol. Biol. 21:771–77 [Google Scholar]
  64. 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 169:125429–33 [Google Scholar]
  65. Jansen R, van Embden JDA, Gaastra W, Schouls LM. 2002. Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43:61565–75 [Google Scholar]
  66. Jiang F, Zhou K, Ma L, Gressel S, Doudna JA. 2015a. A Cas9-guide RNA complex preorganized for target DNA recognition. Science 348:62421477–81 [Google Scholar]
  67. Jiang Y, Yin S, Dudley EG, Cutter CN. 2015b. Diversity of CRISPR loci and virulence genes in pathogenic Escherichia coli isolates from various sources. Int.J. Food Microbiol. 204:41–46 [Google Scholar]
  68. 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 337:816–21 [Google Scholar]
  69. Johnson BR, Klaenhammer TR. 2014. Impact of genomics on the field of probiotic research: historical perspectives to modern paradigms. Antonie van Leeuwenhoek 106:1141–56 [Google Scholar]
  70. Jore MM, Lundgren M, van Duijn E, Bultema JB, Westra ER. et al. 2011. Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nat. Struct. Mol. Biol. 18:529–36 [Google Scholar]
  71. Karvelis T, Gasiunas G, Miksys A, Barrangou R, Horvath P, Siksnys V. 2013. crRNA and tracrRNA guide Cas9-mediated DNA interference in Streptococcus thermophilus. RNA Biol. 10:5841–51 [Google Scholar]
  72. Kinnevey PM, Shore AC, Brennan GI, Sullivan DJ, Ehricht R. et al. 2013. Emergence of sequence type 779 methicillin-resistant Staphylococcus aureus harboring a novel pseudo staphylococcal cassette chromosome mec (SCCmec)-SCC-SCCCRISPR composite element in Irish hospitals. Antimicrob. Agents Chemother 57:524–31 [Google Scholar]
  73. Kovanen SM, RI Kivistö, Rossi M, Hänninen ML. 2014. A combination of MLST and CRISPR typing reveals dominant Campylobacter jejuni types in organically farmed laying hens. J. Appl. Microbiol. 117:1249–57 [Google Scholar]
  74. Kunin V, Sorek R, Hugenholtz P. 2007. Evolutionary conservation of sequence and secondary structures in CRISPR repeats. Genome Biol 8:4R61 [Google Scholar]
  75. Kupczok A, Bollback JP. 2013. Probabilistic models for CRISPR spacer content evolution. BMC Evol. Biol. 13:54 [Google Scholar]
  76. Labrie SJ, Samson JE, Moineau S. 2010. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8:317–27 [Google Scholar]
  77. Levin BR. 2010. Nasty viruses, costly plasmids, population dynamics, and the conditions for establishing and maintaining CRISPR-mediated adaptive immunity in bacteria. PLOS Genet 6:e1001171 [Google Scholar]
  78. Levin BR, Moineau S, Bushman M, Barrangou R. 2013. The population and evolutionary dynamics of phage and bacteria with CRISPR-mediated immunity. PLOS Genet 9:3e1003312 [Google Scholar]
  79. 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. 77:61946–56 [Google Scholar]
  80. Liu F, Kariyawasam S, Jayarao B, Barrangou R, Gerner-Smidt P. et al. 2011b. Subtyping of 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. 77:134520–26 [Google Scholar]
  81. 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 [Google Scholar]
  82. Makarova KS, Haft DH, Barrangou R, Brouns SJ, Charpentier E. et al. 2011. Evolution and classification of the CRISPR-Cas systems. Nat. Rev. Microbiol. 9:6467–77 [Google Scholar]
  83. Makarova KS, Wolf YI, Alkhnbashi OS, Costa F, Shah SA. et al. 2015. An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol. 13:722–36 [Google Scholar]
  84. Marcó MB, Moineau S, Quiberoni A. 2012. Bacteriophages and dairy fermentations. Bacteriophage 2:31–10 [Google Scholar]
  85. Marraffini LA, Sontheimer EJ. 2008. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322:59091843–45 [Google Scholar]
  86. Marraffini LA, Sontheimer EJ. 2010. Self versus non-self discrimination during CRISPR RNA-directed immunity. Nature 463:568–71 [Google Scholar]
  87. Metchnikoff E. 1907. The Prolongation of Life: Optimistic Studies London: William Heinemann
  88. Mojica FJM, Díez-Villaseñor C, García-Martínez J, Soria E. 2005. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J. Mol. Evol. 60:2174–82 [Google Scholar]
  89. Mojica FJ, Díez-Villaseñor C, García-Martínez J, Almendros C. 2009. Short motif sequences determine the targets of the prokaryotic CRISPR defence system. Microbiology 155:733–40 [Google Scholar]
  90. Mokrousov I, Vyazovaya A, Kolodkina V, Limeschenko E, Titov L, Narvaskaya O. 2009. Novel macroarray-based method of Corynebacterium diphtheriae genotyping: evaluation in a field study in Belarus. Eur. J. Clin. Microbiol. 28:701–3 [Google Scholar]
  91. Mulepati S, Orr A, Bailey S. 2012. Crystal structure of the largest subunit of a bacterial RNA-guided immune complex and its role in DNA target binding. J. Biol. Chem. 287:22445–49 [Google Scholar]
  92. Nam KH, Haitjema C, Liu X, Ding F, Wang H. et al. 2012. Cas5d protein processes pre-crRNA and assembles into a Cascade-like interference complex in Subtype I-C/Dvulg CRISPR-Cas system. Structure 20:91450–52 [Google Scholar]
  93. Niewoehner O, Jinek M, Doudna JA. 2014. Evolution of CRISPR RNA recognition and processing by Cas6 endonucleases. Nucleic Acids Res 42:1341–53 [Google Scholar]
  94. Nishimasu H, Cong L, Yan WX, Ran FA, Zetsche B. et al. 2015. Crystal structure of Staphylococcus aureus Cas9. Cell 162:51113–26 [Google Scholar]
  95. Nishimasu H, Ran FA, Hsu PD, Konermann S, Shehata SI. et al. 2014. Crystal structure of Cas9 in complex with guide RNA and target DNA. Cell 156:5935–49 [Google Scholar]
  96. Nozawa T, Furukawa N, Aikawa C, Watanabe T, Haobam B. et al. 2011. CRISPR inhibition of prophage acquisition in Streptococcus pyogenes. PLOS ONE 6:51–9 [Google Scholar]
  97. Nuñez JK, Lee ASY, Engleman A, Doudna JD. 2015. Integrase-mediated spacer acquisition during CRISPR-Cas adaptive immunity. Nature 519:193–98 [Google Scholar]
  98. Oh JH, van Pijkeren JP. 2014. CRISPR-Cas9-assisted recombineering in Lactobacillus reuteri. Nucleic Acids Res 42:17e131 [Google Scholar]
  99. Palmer KL, Gilmore MS. 2010. Multidrug-resistant enterococci lack CRISPR-cas. mBio 1:e00227–10 [Google Scholar]
  100. Papadimitriou K, Pot B, Tsakalidou E. 2015. How microbes adapt to a diversity of food niches. Curr. Opin. Food Sci. 2:29–35 [Google Scholar]
  101. Peng W, Feng M, Feng X, Liang YX, She Q. 2015. An archaeal CRISPR type III-B system exhibiting distinctive RNA targeting features and mediating dual RNA and DNA interference. Nucleic Acids Res 43:1406–17 [Google Scholar]
  102. Pennisi E. 2013. The CRISPR craze. Science 341:6148833–36 [Google Scholar]
  103. Pettengill JB, Timme RE, Barrangou R, Toro M, Allard MW. et al. 2014. The evolutionary history and diagnostic utility of the CRISPR-Cas system within Salmonella enterica ssp. enterica. Peer J. 2:e340 [Google Scholar]
  104. Plagens A, Tjaden B, Hagemann A, Randau L, Hensel R. 2012. Characterization of the CRISPR/Cas subtype I-A system of the hyperthermophilic crenarchaeon Thermoproteus tenax. J. Bacteriol. 194:102491–500 [Google Scholar]
  105. 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 151:653–63 [Google Scholar]
  106. Ramia NF, Spilman M, Tang L, Shao Y, Elmore J. et al. 2014. Essential structural and functional roles of the Cmr4 subunit in RNA cleavage by the Cmr CRISPR-Cas complex. Cell Rep 9:51610–17 [Google Scholar]
  107. Reeks J, Naismith JH, White MF. 2013. CRISPR interference: a structural perspective. Biochem. J. 453:155–66 [Google Scholar]
  108. Richter C, Dy RL, McKenzie RE, Watson BNJ, Taylor C. et al. 2014. Priming in the Type I-F CRISPR-Cas system triggers strand-independent spacer acquisition, bi-directionally from the primed protospacer. Nucleic Acids Res 42:8516–26 [Google Scholar]
  109. Rutkauskas M, Sinkunas T, Songailiene I, Tikhomirova MS, Siksnys V, Seidel R. 2015. Directional R-loop formation by the CRISPR-Cas surveillance complex provides efficient off-target site rejection. Cell Rep 10:91534–43 [Google Scholar]
  110. 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 161:51164–74 [Google Scholar]
  111. Samson JE, Moineau S. 2013. Bacteriophages in food fermentations: new frontiers in a continuous arms race. Annu. Rev. Food Sci. Technol. 4:347–68 [Google Scholar]
  112. Sander JD, Joung JK. 2014. CRISPR-Cas systems for editing, regulating, and targeting genomes. Nat. Biotechnol. 32:347–55 [Google Scholar]
  113. Sanders ME, Klaenhammer TR. 1981. Evidence for plasmid linkage of restriction and modification in Streptococcus cremoris KH. Appl. Environ. Microbiol. 42:6944–50 [Google Scholar]
  114. Sanders ME, Klaenhammer TR. 1983. Characterization of phage-sensitive mutants from a phage-insensitive strain of Streptococcus lactis: evidence for a plasmid determinant that prevents phage adsorption. Appl. Environ. Microbiol. 46:51125–33 [Google Scholar]
  115. Sanozky-Dawes R, Selle K, O'Flaherty S, Klaenhammer T, Barrangou R. 2015. Occurrence and activity of a type II CRISPR-Cas system in Lactobacillus gasseri. Microbiology 161:1752–61 [Google Scholar]
  116. Sapranauskas R, Gasiunas G, Fremaux C, Barrangou R, Horvath P, Siksnys V. 2011. The Streptococcusthermophilus CRISPR/Cas systems provides immunity in Escherichia coli. Nucleic Acids Res. 39:219275–82 [Google Scholar]
  117. Sashital DG, Jinek M, Doudna JA. 2011. An RNA-induced conformational change required for CRISPR RNA cleavage by the endoribonuclease Cse3. Nat. Struct. Mol. Biol. 18:680–87 [Google Scholar]
  118. Sashital DG, Wiedenheft B, Doudna JA. 2012. Mechanism of foreign DNA selection in a bacterial adaptive immune system. Mol. Cell 46:606–15 [Google Scholar]
  119. Scallen E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA. et al. 2011. Foodborne illness acquired in the United States: major pathogens. Emerg. Infect. Dis. 17:11–15 [Google Scholar]
  120. Scharff RL. 2012. Economic burden from health losses due to foodborne illness in the United States. J. Food Protect. 75:123–31 [Google Scholar]
  121. Schunder E, Rydzewski K, Grunow R, Heuner K. 2013. First indication for a functional CRISPR/Cas system in Francisella tularensis. Int. J. Med. Microbiol 303251–60 [Google Scholar]
  122. Selle K, Klaenhammer TR, Barrangou R. 2015. CRISPR-based screening of genomic island excision events in bacteria. PNAS 112:268076–81 [Google Scholar]
  123. Selle K, Barrangou R. 2015a. CRISPR-based technologies and the future of food science. J. Food Sci. 80:11R2367–72 [Google Scholar]
  124. Selle K, Barrangou R. 2015b. Harnessing CRISPR-Cas systems for bacterial genome editing. Trends Microbiol 23:4225–32 [Google Scholar]
  125. Semenova E, Jore MM, Datsenko KA, Semenova A, Westra ER. et al. 2011. Interference by clustered regularly interspaced short palindromic repeat (CRISPR) RNA is guided by a seed sequence. PNAS 108:2510098–103 [Google Scholar]
  126. Shariat N, DiMarzio MJ, Shuang Y, Dettinger L, Sandt CH. et al. 2013a. The combination of CRISPR-MVLST and PFGE provides increased discriminatory power for differentiating human clinical isolates of Salmonella enterica subsp. enterica serovar Enteritidis. Food Microbiol 34:1164–73 [Google Scholar]
  127. Shariat N, Kirchner MK, Sandt CH, Trees E, Barrangou R, Dudley EG. 2013b. Subtyping of Salmonella enterica serovar Newport outbreak isolates by CRISPR-MVLST and determination of the relationship between CRISPR-MVLST and PFGE results. J. Clin. Microbiol. 51:72328–36 [Google Scholar]
  128. Shariat N, Sandt CH, DiMarzio MJ, Barrangou R, Dudley EG. 2013c. CRISPR-MVLST subtyping of Salmonella enterica subsp. enterica serovars Typhimurium and Heidelberg and application in identifying outbreak isolates. BMC Microbiol 13:254 [Google Scholar]
  129. Shariat N, Timme RE, Pettengill JB, Barrangou R, Dudley EG. 2014. Characterization and evolution of Salmonella CRISPR-Cas systems. Microbiology 161:374–86 [Google Scholar]
  130. Shimomura Y, Okumura K, Yamagata MS, Yagi J, Ubukata K. et al. 2011. Complete genome sequencing and analysis of a Lancefield group G Streptoccus dysgalactiae subsp. equisimilis strain causing streptoccal toxic shock syndrome (STSS). BMC Genom 12:17 [Google Scholar]
  131. Shmakov S, Abudayyeh OO, Makarova KS, Wolf YI, Gootenberg JS. et al. 2015. Discovery and functional characterization of diverse class 2 CRISPR-Cas systems. Mol. Cell 60:3385–97 [Google Scholar]
  132. Sieuwerts S, de Bok FAM, Hugenholtz J, van Hylckama Vlieg JET. 2008. Unraveling microbial interactions in food fermentations: from classical to genomics approaches. Appl. Environ. Microbiol. 74:164997–5007 [Google Scholar]
  133. Smokvina T, Wels M, Polka J, Chervaux C, Brisse S. et al. 2013. Lactobacillus paracasei comparative genomics: towards species pan-genome definition and exploitation of diversity. PLOS ONE 8:7e68731 [Google Scholar]
  134. Sontheimer E, Barrangou R. 2015. The bacterial origins of the CRISPR genome-editing revolution. Hum. Gene Ther. 26:7413–24 [Google Scholar]
  135. Staals RH, Agari Y, Maki-Yonekura S, Zhu Y, Taylor DW, van Duijn E. et al. 2013. Structure and activity of the RNA-targeting type III-B CRISPR-Cas complex of Thermus thermophilus. Mol. Cell 52:1135–45 [Google Scholar]
  136. Staals RHJ, Zhu Y, Taylor DW, Kornfield JE, Sharma K. et al. 2014. RNA targeting by the type III-A CRISPR-Cas Csm complex of Thermus thermophilus. Mol. Cell 56:4518–30 [Google Scholar]
  137. Sternberg SH, Redding S, Jinek M, Greene EC, Doudna JA. 2014. DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 507:749062–67 [Google Scholar]
  138. Sternberg SH, Richter H, Charpentier E, Qimron U. 2016. Adaptation in CRISPR-Cas systems. Mol. Cell 61:6797–808 [Google Scholar]
  139. Sun Z, Harris HMB, McCann A, Guo C, Argimón S. et al. 2015a. Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera. Nat. Commun. 6:8322 [Google Scholar]
  140. Sun H, Li Y, Shi X, Lin Y, Qiu Y. et al. 2015b. Association of CRISPR/Cas evolution with Vibrio parahaemolyticus virulence factors and genotypes. Foodborne Pathog. Dis. 12:68–73 [Google Scholar]
  141. Swarts DC, Mosterd C, van Passel MW, Brouns SJ. 2012. CRISPR interference directs strand specific spacer acquisition. PLOS ONE 7:4e35888 [Google Scholar]
  142. Szczelkun MD, Tikhomirova MS, Sinkunas T, Gasiunas G, Karvelis T. et al. 2014. Direct observation of R-loop formation by single RNA-guided Cas9 and Cascade effector complexes. PNAS 111:279798–803 [Google Scholar]
  143. Tamulaitis G, Kazlauskienne M, Manakova E, Venclovas C, Nwokeoji AO. 2014. Programmable RNA shredding by the Type III-A CRISPR-Cas system of Streptoccocus thermophilus. Mol. Cell 56:4506–17 [Google Scholar]
  144. Timme RE, Pettengill JB, Allard MW, Strain E, Barrangou R. et al. 2013. Phylogenetic diversity of the enteric pathogen Salmonella enterica subsp. enterica inferred from the genome-wide reference-free SNP characters. Genome Biol. Evol 5:112109–23 [Google Scholar]
  145. Tyson GW, Banfield JW. 2008. Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ. Microbiol. 10:1200–7 [Google Scholar]
  146. van der Oost J, Westra ER, Jackson RN, Wiedenheft B. 2014. Unravelling the structural and mechanistic basis of CRISPR-Cas systems. Nat. Rev. Microbiol. 12:7479–92 [Google Scholar]
  147. Vercoe RB, Chang JT, Dy RL, Taylor C, Gristwood T. et al. 2013. Cytotoxic chromosomal targeting by CRISPR/Cas systems can reshape bacterial genomes and expel or remodel pathogenicity islands. PLOS Genet 9:4e1003454 [Google Scholar]
  148. Wehnes CA, Rehberger TG, Barrangou R, Smith AH. 2014. Determination of Salmonella clustered regularly interspaced short palindromic repeats (CRISPR) diversity on dairy farms in Wisconsin and Minnesota. J. Dairy Sci. 97:106370–77 [Google Scholar]
  149. Weinberger AD, Sun CL, Pluciński MM, Denef VJ, Thomas BC. et al. 2012. Persisting viral sequences shape microbial CRISPR-based immunity. PLOS Comput. Biol. 8:4e1002475 [Google Scholar]
  150. Westra ER, Van Erp PB, Kunne T, Wong SP, Staals RH. et al. 2012. CRISPR immunity relies on the consecutive binding and degradation of negatively supercoiled invader DNA by Cascade and Cas3. Mol. Cell 46:5595–605 [Google Scholar]
  151. Wiedenheft B, van Duijn E, Bultema JB, Waghmare SP, Zhou K. et al. 2011. RNA-guided complex from a bacterial immune system enhances target recognition through seed sequence interactions. PNAS 108:2510092–97 [Google Scholar]
  152. Yamano T, Nishimasu H, Zetsche B, Hirano H, Slaymaker IM. et al. 2016. Crystal structure of Cpf1 in complex with guide RNA and target DNA. Cell 165:4949–62 [Google Scholar]
  153. 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. 79:5710–20 [Google Scholar]
  154. Zebec Z, Manica A, Zhang J, White MF, Schleper C. 2014. CRISPR-mediated targeted mRNA degradation in the archaeon Sulfolobus solfataricus. Nucleic Acids Res. 42:85280–88 [Google Scholar]
  155. Zetsche B, Gootenberg JS, Abudayyeh OO, Slaymaker IM, Makarova KS. et al. 2015. Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163:3759–71 [Google Scholar]
  156. Zhao H, Sheng G, Wang J, Wang M, Bunkoczi G. et al. 2014. Crystal structure of the RNA-guided immune surveillance Cascade complex in Escherichia coli. Nature 515:7525147–50 [Google Scholar]
  157. Zoephel J, Randau L. 2013. RNA-Seq analyses reveal CRISPR RNA processing and regulation patterns. Biochem. Soc. Trans. 41:1459–63 [Google Scholar]
/content/journals/10.1146/annurev-food-072816-024723
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CRISPR-Cas Technologies and Applications in Food Bacteria
Annual Review of Food Science and Technology 8, 413 (2017); https://doi.org/10.1146/annurev-food-072816-024723
/content/journals/10.1146/annurev-food-072816-024723
/content/journals/10.1146/annurev-food-072816-024723
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