Multigene editing in the Escherichia coli genome via the CRISPR-Cas9 system

Applied and Environmental Microbiology

Volumn 81, Issue 7, 2015, Pages 2506-2514

  Jiang, Yu ^a,b   Chen, Biao ^a,b   Duan, Chunlan ^a   Sun, Bingbing ^a,b   Yang, Junjie ^a,b   Yang, Sheng ^a,b,c  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^b Academic Sinica   (China)

^c SHANGHAI COLLABORATIVE INNOVATION CENTER FOR BIOMANUFACTURING TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI;

CHROMOSOMAL DELETIONS; EDITING TOOLS; ENTEROBACTERIACEAE; GENE DELETION; GENOME MODIFICATION; STREPTOCOCCUS PYOGENES; TYPE II;

GENES;

CHROMOSOME; GENE EXPRESSION; GENOME; INDUSTRIAL PRODUCTION; MICROBIAL COMMUNITY; PHYLOGENETICS; PROKARYOTE;

ENTEROBACTERIACEAE; ESCHERICHIA COLI; STREPTOCOCCUS PYOGENES; TATUMELLA;

BACTERIAL GENE; BACTERIAL GENOME; CRISPR CAS SYSTEM; ENTEROBACTERIACEAE; ENZYMOLOGY; GENETIC RECOMBINATION; GENETICS; MICROBIAL GENETICS; MOLECULAR BIOLOGY; PROCEDURES; STREPTOCOCCUS PYOGENES;

CRISPR-CAS SYSTEMS; ENTEROBACTERIACEAE; GENES, BACTERIAL; GENETICS, MICROBIAL; GENOME, BACTERIAL; MOLECULAR BIOLOGY; RECOMBINATION, GENETIC; STREPTOCOCCUS PYOGENES;

EID: 84925355124     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.04023-14     Document Type: Article

References (54)

1. Ingram LO, Gomez PF, Lai X, Moniruzzaman M, Wood BE, Yomano LP, York SW. 1998. Metabolic engineering of bacteria for ethanol production. Biotechnol Bioeng 58:204-214. http://dx.doi.org/10.1002 /(SICI)1097-0290(19980420)58:2/3204::AID-BIT133.0.CO;2-C.
2. Atsumi S, Hanai T, Liao JC. 2008. Non-fermentative pathways for synthesis of branched-chain higher alcohols as biofuels. Nature 451:86-89. http://dx.doi.org/10.1038/nature06450.
3. Steen EJ, Kang Y, Bokinsky G, Hu Z, Schirmer A, McClure A, Del Cardayre SB, Keasling JD. 2010. Microbial production of fatty-acidderived fuels and chemicals from plant biomass. Nature 463:559-562. http://dx.doi.org/10.1038/nature08721.
4. Leuchtenberger W, Huthmacher K, Drauz K. 2005. Biotechnological production of amino acids and derivatives: current status and prospects. Appl Microbiol Biotechnol 69:1-8. http://dx.doi.org/10.1007/s00253-005-0155-y.
5. Bongaerts J, Kramer M, Muller U, Raeven L, Wubbolts M. 2001. Metabolic engineering for microbial production of aromatic amino acids and derived compounds. Metab Eng 3:289-300. http://dx.doi.org/10.1006/mben.2001.0196.
6. Martin VJ, Pitera DJ, Withers ST, Newman JD, Keasling JD. 2003. Engineering a mevalonate pathway in Escherichia coli for production of terpenoids. Nat Biotechnol 21:796-802. http://dx.doi.org/10.1038/nbt833.
7. McDaniel R, Thamchaipenet A, Gustafsson C, Fu H, Betlach M, Ashley G. 1999. Multiple genetic modifications of the erythromycin polyketide synthase to produce a library of novel "unnatural" natural products. Proc Natl Acad Sci U S A 96:1846-1851. http://dx.doi.org/10.1073/pnas.96.5.1846.
8. Yim H, Haselbeck R, Niu W, Pujol-Baxley C, Burgard A, Boldt J, Khandurina J, Trawick JD, Osterhout RE, Stephen R, Estadilla J, Teisan S, Schreyer HB, Andrae S, Yang TH, Lee SY, Burk MJ, Van Dien S. 2011. Metabolic engineering of Escherichia coli for direct production of 1,4-butanediol. Nat Chem Biol 7:445-452. http://dx.doi.org/10.1038/nchembio.580.
9. Nakamura CE, Whited GM. 2003. Metabolic engineering for the microbial production of 1,3-propanediol. Curr Opin Biotechnol 14:454-459. http://dx.doi.org/10.1016/j.copbio.2003.08.005.
10. Esvelt KM, Wang HH. 2013. Genome-scale engineering for systems and synthetic biology. Mol Syst Biol 9:641. http://dx.doi.org/10.1038/msb.2012.66.
11. Enyeart PJ, Chirieleison SM, Dao MN, Perutka J, Quandt EM, Yao J, Whitt JT, Keatinge-Clay AT, Lambowitz AM, Ellington AD. 2013. Generalized bacterial genome editing using mobile group II introns and Cre-lox. Mol Syst Biol 9:685. http://dx.doi.org/10.1038/msb.2013.41.
12. Yu BJ, Kang KH, Lee JH, Sung BH, Kim MS, Kim SC. 2008. Rapid and efficient construction of markerless deletions in the Escherichia coli genome. Nucleic Acids Res 36:e84. http://dx.doi.org/10.1093/nar/gkn359.
13. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640-6645. http://dx.doi.org/10.1073/pnas.120163297.
14. Yu D, Ellis HM, Lee EC, Jenkins NA, Copeland NG, Court DL. 2000. An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci U S A 97:5978-5983. http://dx.doi.org/10.1073/pnas.100127597.
15. Zhang Y, Buchholz F, Muyrers JP, Stewart AF. 1998. A new logic for DNA engineering using recombination in Escherichia coli. Nat Genet 20: 123-128. http://dx.doi.org/10.1038/2417.
16. Sharan SK, Thomason LC, Kuznetsov SG, Court DL. 2009. Recombineering: a homologous recombination-based method of genetic engineering. Nat Protoc 4:206-223. http://dx.doi.org/10.1038/nprot.2008.227.
17. Warner JR, Reeder PJ, Karimpour-Fard A, Woodruff LB, Gill RT. 2010. Rapid profiling of a microbial genome using mixtures of barcoded oligonucleotides. Nat Biotechnol 28:856-862. http://dx.doi.org/10.1038/nbt.1653.
18. Costantino N, Court DL. 2003. Enhanced levels of lambda Red-mediated recombinants in mismatch repair mutants. Proc Natl Acad Sci U S A 100:15748-15753. http://dx.doi.org/10.1073/pnas.2434959100.
19. Posfai G, Kolisnychenko V, Bereczki Z, Blattner FR. 1999. Markerless gene replacement in Escherichia coli stimulated by a double-strand break in the chromosome. Nucleic Acids Res 27:4409-4415. http://dx.doi.org /10.1093/nar/27.22.4409.
20. Yang J, Sun B, Huang H, Jiang Y, Diao L, Chen B, Xu C, Wang X, Liu J, Jiang W, Yang S. 2014. High-efficiency scarless genetic modification in Escherichia coli using lambda-red recombination and I-SceI cleavage. Appl Environ Microbiol 80:3826-3834. http://dx.doi.org/10.1128/AEM.00313-14.
21. Karberg M, Guo H, Zhong J, Coon R, Perutka J, Lambowitz AM. 2001. Group II introns as controllable gene targeting vectors for genetic manipulation of bacteria. Nat Biotechnol 19:1162-1167. http://dx.doi.org/10.1038/nbt1201-1162.
22. Wang HH, Church GM. 2011. Multiplexed genome engineering and genotyping methods applications for synthetic biology and metabolic engineering. Methods Enzymol 498:409-426. http://dx.doi.org/10.1016/B978-0-12-385120-8.00018-8.
23. Wang HH, Isaacs FJ, Carr PA, Sun ZZ, Xu G, Forest CR, Church GM. 2009. Programming cells by multiplex genome engineering and accelerated evolution. Nature 460:894-898. http://dx.doi.org/10.1038/nature08187.
24. Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA. 2013. RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31:233-239. http://dx.doi.org/10.1038/nbt.2508.
25. DiCarlo JE, Norville JE, Mali P, Rios X, Aach J, Church GM. 2013. Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res 41:4336-4343. http://dx.doi.org/10.1093/nar /gkt135.
26. Cobb RE, Wang Y, Zhao H. 8 December 2014. High-efficiency multiplex genome editing of Streptomyces species using an engineered CRISPR/Cas system. ACS Synth Biol. http://dx.doi.org/10.1021/sb500351f.
27. Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, Zhang K, Liu J, Xi JJ, Qiu JL, Gao C. 2013. Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31:686-688. http://dx.doi.org/10.1038/nbt.2650.
28. Wang Y, Li Z, Xu J, Zeng B, Ling L, You L, Chen Y, Huang Y, Tan A. 2013. The CRISPR/Cas System mediates efficient genome engineering in Bombyx mori. Cell Res 23:1414-1416. http://dx.doi.org/10.1038/cr.2013.146.
29. Yu Z, Ren M, Wang Z, Zhang B, Rong YS, Jiao R, Gao G. 2013. Highly efficient genome modifications mediated by CRISPR/Cas9 in Drosophila. Genetics 195:289-291. http://dx.doi.org/10.1534/genetics.113.153825.
30. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339:819-823. http://dx.doi.org/10.1126/science.1231143.
31. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM. 2013. RNA-guided human genome engineering via Cas9. Science 339:823-826. http://dx.doi.org/10.1126/science.1232033.
32. Zhang Q, Rho M, Tang H, Doak TG, Ye Y. 2013. CRISPR-Cas systems target a diverse collection of invasive mobile genetic elements in human microbiomes. Genome Biol 14:R40. http://dx.doi.org/10.1186/gb-2013-14-4-r40.
33. Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y, Pirzada ZA, Eckert MR, Vogel J, Charpentier E. 2011. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471:602-607. http://dx.doi.org/10.1038/nature09886.
34. 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. http://dx.doi.org /10.1126/science.1225829.
35. Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS, Arkin AP, Lim WA. 2013. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152:1173-1183. http: //dx.doi.org/10.1016/j.cell.2013.02.022.
36. Pujol CJ, Kado CI. 2000. Genetic and biochemical characterization of the pathway in Pantoea citrea leading to pink disease of pineapple. J Bacteriol 182:2230-2237. http://dx.doi.org/10.1128/JB.182.8.2230-2237.2000.
37. Cha JS, Pujol C, Kado CI. 1997. Identification and characterization of a Pantoea citrea gene encoding glucose dehydrogenase that is essential for causing pink disease of pineapple. Appl Environ Microbiol 63:71-76.
38. Ochman H, Gerber AS, Hartl DL. 1988. Genetic applications of an inverse polymerase chain reaction. Genetics 120:621-623.
39. Shetty RP, Endy D, Knight TF, Jr. 2008. Engineering BioBrick vectors from BioBrick parts. J Biol Eng 2:5. http://dx.doi.org/10.1186/1754-1611-2-5.
40. Guzman LM, Belin D, Carson MJ, Beckwith J. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177:4121-4130.
41. Chayot R, Montagne B, Mazel D, Ricchetti M. 2010. An end-joining repair mechanism in Escherichia coli. Proc Natl Acad Sci U S A 107:2141-2146. http://dx.doi.org/10.1073/pnas.0906355107.
42. Koboldt DC, Steinberg KM, Larson DE, Wilson RK, Mardis ER. 2013. The next-generation sequencing revolution and its impact on genomics. Cell 155:27-38. http://dx.doi.org/10.1016/j.cell.2013.09.006.
43. Dodge TC, Valle F, Rashid MH. February 2005. Metabolically engineered bacterial strains having enhanced 2-keto-D-gluconate accumulation. US patent WO2005012486-A2.
44. Banta S, Boston M, Jarnagin A, Anderson S. 2002. Mathematical modeling of in vitro enzymatic production of 2-keto-L-gulonic acid using NAD(H) or NADP(H) as cofactors. Metab Eng 4:273-284. http://dx.doi.org/10.1006/mben.2002.0231.
45. Wilson TE, Topper LM, Palmbos PL. 2003. Non-homologous endjoining: bacteria join the chromosome breakdance. Trends Biochem Sci 28:62-66. http://dx.doi.org/10.1016/S0968-0004(03)00005-7.
46. Malyarchuk S, Wright D, Castore R, Klepper E, Weiss B, Doherty AJ, Harrison L. 2007. Expression of Mycobacterium tuberculosis Ku and ligase D in Escherichia coli results in RecA and RecB-independent DNA end-joining at regions of microhomology. DNA Repair (Amst) 6:1413-1424. http://dx.doi.org/10.1016/j.dnarep.2007.04.004.
47. Siegele DA, Hu JC. 1997. Gene expression from plasmids containing the araBAD promoter at subsaturating inducer concentrations represents mixed populations. Proc Natl Acad SciUS A 94:8168-8172. http://dx.doi.org/10.1073/pnas.94.15.8168.
48. Cradick TJ, Fine EJ, Antico CJ, Bao G. 2013. CRISPR/Cas9 systems targeting beta-globin and CCR5 genes have substantial off-target activity. Nucleic Acids Res 41:9584-9592. http://dx.doi.org/10.1093/nar/gkt714.
49. Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK, Sander JD. 2013. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol 31:822-826. http://dx.doi.org/10.1038/nbt.2623.
50. Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, Scott DA, Inoue A, Matoba S, Zhang Y, Zhang F. 2013. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154:1380-1389. http://dx.doi.org/10.1016/j.cell.2013.08.021.
51. Anders C, Niewoehner O, Duerst A, Jinek M. 2014. Structural basis of PAM-dependent target DNA recognition by the Cas9 endonuclease. Nature 513:569-573. http://dx.doi.org/10.1038/nature13579.
52. Martinez E, Bartolome B, de la Cruz F. 1988. pACYC184-derived cloning vectors containing the multiple cloning site and lacZ alpha reporter gene of pUC8/9 and pUC18/19 plasmids. Gene 68:159-162. http: //dx.doi.org/10.1016/0378-1119(88)90608-7.
53. Amann E, Ochs B, Abel KJ. 1988. Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli. Gene 69:301-315. http://dx.doi.org/10.1016/0378-1119(88)90440-4.
54. Gust B, Challis GL, Fowler K, Kieser T, Chater KF. 2003. PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc Natl Acad Sci U S A 100:1541-1546. http://dx.doi.org/10.1073/pnas.0337542100.