Extending CRISPR-Cas9 technology from genome editing to transcriptional engineering in the genus Clostridium

Applied and Environmental Microbiology

Volumn 82, Issue 20, 2016, Pages 6109-6119

  Bruder, Mark R ^a   Pyne, Michael E ^a,d   Moo Young, Murray ^a   Chung, Duane A ^a,b,c   Chou, C Perry ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

^b Algaeneers Inc   (Canada)

^c Neemo Inc   (Canada)

^d Gina Cody School of Engineering and Computer Science   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; CLOSTRIDIUM; GENE ENCODING; GENETIC ENGINEERING; MACHINERY; PRASEODYMIUM COMPOUNDS; PROTEINS;

CARBON CATABOLITE REPRESSION; CLOSTRIDIUM ACETOBUTYLICUM; CLOSTRIDIUM PASTEURIANUM; LIGNOCELLULOSIC FEEDSTOCKS; STREPTOCOCCUS PYOGENES; TRANSCRIPTIONAL ENGINEERINGS; TRANSCRIPTIONAL PROGRAM; TRANSCRIPTIONAL REPRESSION;

POTASSIUM COMPOUNDS;

BACTERIUM; CARBON; CELLULOSE; GENE EXPRESSION; GENETIC ENGINEERING; GENOME; IMMUNITY; PROKARYOTE; PROTEIN;

CLOSTRIDIUM; CLOSTRIDIUM ACETOBUTYLICUM; CLOSTRIDIUM PASTEURIANUM; PROKARYOTA; STREPTOCOCCUS PYOGENES;

BACTERIAL PROTEIN;

BACTERIAL GENOME; CLOSTRIDIUM ACETOBUTYLICUM; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CRISPR CAS SYSTEM; EVALUATION STUDY; GENE EDITING; GENETIC ENGINEERING; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PROCEDURES;

BACTERIAL PROTEINS; CLOSTRIDIUM ACETOBUTYLICUM; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CRISPR-CAS SYSTEMS; GENE EDITING; GENETIC ENGINEERING; GENOME, BACTERIAL; TRANSCRIPTION, GENETIC;

EID: 84991281155     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02128-16     Document Type: Article

References (74)

1. Tracy BP, Jones SW, Fast AG, Indurthi DC, Papoutsakis ET. 2012. Clostridia: the importance of their exceptional substrate and metabolite diversity for biofuel and biorefinery applications. Curr Opin Biotechnol 23:364-381. http://dx.doi.org/10.1016/j.copbio.2011.10.008.
2. Papoutsakis ET. 2008. Engineering solventogenic clostridia. Curr Opin Biotechnol 19:420-429. http://dx.doi.org/10.1016/j.copbio.2008.08.003.
3. Pyne ME, Bruder M, Moo-Young M, Chung DA, Chou CP. 2014. Technical guide for genetic advancement of underdeveloped and intractable Clostridium. Biotechnol Adv 32:623-641. http://dx.doi.org/10.1016/j.biotechadv.2014.04.003.
4. Mermelstein LD, Papoutsakis ET. 1993. In vivo methylation in Escherichia coli by the Bacillus subtilis phage phi 3T I methyltransferase to protect plasmids from restriction upon transformation of Clostridium acetobutylicum ATCC 824. Appl Environ Microbiol 59:1077-1081.
5. Green EM, Boynton ZL, Harris LM, Rudolph FB, Papoutsakis ET, Bennett GN. 1996. Genetic manipulation of acid formation pathways by gene inactivation in Clostridium acetobutylicum ATCC 824. Microbiology 142:2079-2086. http://dx.doi.org/10.1099/13500872-142-8-2079.
6. Harris LM, Welker NE, Papoutsakis ET. 2002. Northern, morphological, and fermentation analysis of spo0A inactivation and overexpression in Clostridium acetobutylicum ATCC 824. J Bacteriol 184:3586-3597. http://dx.doi.org/10.1128/JB.184.13.3586-3597.2002.
7. Heap JT, Pennington OJ, Cartman ST, Carter GP, Minton NP. 2007. The ClosTron: a universal gene knock-out system for the genus Clostridium. J Microbiol Methods 70:452-464. http://dx.doi.org/10.1016/j.mimet.2007.05.021.
8. Shao L, Hu S, Yang Y, Gu Y, Chen J, Yang Y, Jiang W, Yang S. 2007. Targeted gene disruption by use of a group II intron (targetron) vector in Clostridium acetobutylicum. Cell Res 17:963-965. http://dx.doi.org/10.1038/cr.2007.91.
9. Pyne ME, Moo-Young M, Chung DA, Chou CP. 2014. Expansion of the genetic toolkit for metabolic engineering of Clostridium pasteurianum: chromosomal gene disruption of the endogenous CpaAI restriction enzyme. Biotechnol Biofuels 7:163. http://dx.doi.org/10.1186/s13068-014-0163-1.
10. 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.
11. Perutka J, Wang W, Goerlitz D, Lambowitz AM. 2004. Use of computerdesigned group II introns to disrupt Escherichia coli DExH/D-box protein and DNA helicase genes. J Mol Biol 336:421-439. http://dx.doi.org/10.1016/j.jmb.2003.12.009.
12. Heap JT, Kuehne SA, Ehsaan M, Cartman ST, Cooksley CM, Scott JC, Minton NP. 2010. The ClosTron: mutagenesis in Clostridium refined and streamlined. J Microbiol Methods 80:49-55. http://dx.doi.org/10.1016/j.mimet.2009.10.018.
13. Chen Y, Caruso L, McClane B, Fisher D, Gupta P. 2007. Disruption of a toxin gene by introduction of a foreign gene into the chromosome of Clostridium perfringens using targetron-induced mutagenesis. Plasmid 58: 182-189. http://dx.doi.org/10.1016/j.plasmid.2007.04.002.
14. Plante I, Cousineau B. 2006. Restriction for gene insertion within the Lactococcus lactis Ll. LtrB group II intron. RNA 12:1980-1992.
15. Heap JT, Ehsaan M, Cooksley CM, Ng YK, Cartman ST, Winzer K, Minton NP. 2012. Integration of DNA into bacterial chromosomes from plasmids without a counter-selection marker. Nucleic Acids Res 40:e59. http://dx.doi.org/10.1093/nar/gkr1321.
16. Al-Hinai MA, Fast AG, Papoutsakis ET. 2012. Novel system for efficient isolation of Clostridium double-crossover allelic exchange mutants enabling markerless chromosomal gene deletions and DNA integration. Appl Environ Microbiol 78:8112-8121. http://dx.doi.org/10.1128/AEM.02214-12.
17. Cartman ST, Kelly ML, Heeg D, Heap JT, Minton NP. 2012. Precise manipulation of the Clostridium difficile chromosome reveals a lack of association between the tcdC genotype and toxin production. Appl Environ Microbiol 78:4683-4690. http://dx.doi.org/10.1128/AEM.00249-12.
18. Nariya H, Miyata S, Suzuki M, Tamai E, Okabe A. 2011. Development and application of a method for counterselectable in-frame deletion in Clostridium perfringens. Appl Environ Microbiol 77:1375-1382. http://dx.doi.org/10.1128/AEM.01572-10.
19. Dong H, Tao W, Gong F, Li Y, Zhang Y. 2014. A functional recT gene for recombineering of Clostridium. J Biotechnol 173:65-67. http://dx.doi.org/10.1016/j.jbiotec.2013.12.011.
20. Alper H, Miyaoku K, Stephanopoulos G. 2005. Construction of lycopene-overproducing E. coli strains by combining systematic and combi-natorial gene knockout targets. Nat Biotechnol 23:612-616. http://dx.doi.org/10.1038/nbt1083.
21. Rossi A, Kontarakis Z, Gerri C, Nolte H, Hölper S, Krüger M, Stainier DYR. 2015. Genetic compensation induced by deleterious mutations but not gene knockdowns. Nature 524:230-233. http://dx.doi.org/10.1038/nature14580.
22. Lee JY, Yang KS, Jang SA, Sung BH, Kim SC. 2011. Engineering butanol-tolerance in Escherichia coli with artificial transcription factor libraries. Biotechnol Bioeng 108:742-749. http://dx.doi.org/10.1002/bit.22989.
23. Desai RP, Papoutsakis ET. 1999. Antisense RNA strategies for metabolic engineering of Clostridium acetobutylicum. Appl Environ Microbiol 65: 936-945.
24. 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.
25. Park K-S, Lee D, Lee H, Lee Y, Jang Y-S, Kim YH, Yang H-Y, Lee S-I, Seol W, Kim J-S. 2003. Phenotypic alteration of eukaryotic cells using randomized libraries of artificial transcription factors. Nat Biotechnol 21: 1208-1214. http://dx.doi.org/10.1038/nbt868.
26. Bogdanove AJ, Voytas DF. 2011. TAL effectors: customizable proteins for DNAtargeting. Science 333:1843-1846. http://dx.doi.org/10.1126/science.1204094.
27. Copeland MF, Politz MC, Pfleger BF. 2014. Application of TALEs, CRISPR/Cas and sRNAs as trans-acting regulators in prokaryotes. Curr Opin Biotechnol 29:46-54. http://dx.doi.org/10.1016/j.copbio.2014.02.010.
28. Rasmussen LC, Sperling-Petersen HU, Mortensen KK. 2007. Hitting bacteria at the heart of the central dogma: sequence-specific inhibition. Microb Cell Fact 6:24. http://dx.doi.org/10.1186/1475-2859-6-24.
29. Marraffini LA, Sontheimer EJ. 2010. CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat Rev Genet 11:181-190. http://dx.doi.org/10.1038/nrg2749.
30. Grissa I, Vergnaud G, Pourcel C. 2007. The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics 8:172. http://dx.doi.org/10.1186/1471-2105-8-172.
31. 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. http://dx.doi.org/10.1126/science.1138140.
32. van der Oost J, Jore MM, Westra ER, Lundgren M, Brouns SJJ. 2009. CRISPR-based adaptive and heritable immunity in prokaryotes. Trends Biochem Sci 34:401-407. http://dx.doi.org/10.1016/j.tibs.2009.05.002.
33. Makarova KS, Haft DH, Barrangou R, Brouns SJJ, Charpentier E, Horvath P, Moineau S, Mojica FJM, Wolf YI, Yakunin AF, van der Oost J, Koonin EV. 2011. Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 9:467-477. http://dx.doi.org/10.1038/nrmicro2577.
34. Makarova KS, Wolf YI, Alkhnbashi OS, Costa F, Shah SA, Saunders SJ, Barrangou R, Brouns SJJ, Charpentier E, Haft DH, Horvath P, Moineau S, Mojica FJM, Terns RM, Terns MP, White MF, Yakunin AF, Garrett RA, van der Oost J, Backofen R, Koonin EV. 2015. An updated evolutionary classification of CRISPR-Cas systems. Nat Rev Microbiol 13:722-736. http://dx.doi.org/10.1038/nrmicro3569.
35. Jiang WY, 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.
36. Westbrook AW, Moo-Young M, Chou CP. 3 June 2016. Development of a CRISPR-Cas9 toolkit for comprehensive engineering of Bacillus subtilis. Appl Environ Microbiol http://dx.doi.org/10.1128/AEM.01159-16.
37. 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.
38. Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, Jaenisch R. 2013. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153: 910-918. http://dx.doi.org/10.1016/j.cell.2013.04.025.
39. 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.
40. 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.
41. 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. http://dx.doi.org/10.1073/pnas.1208507109.
42. 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.
43. Wang Y, Zhang Z-T, Seo S-O, Choi K, Lu T, Jin Y-S, Blaschek HP. 2015. Markerless chromosomal gene deletion in Clostridium beijerinckii using CRISPR/Cas9 system. J Biotechnol 200:1-5. http://dx.doi.org/10.1016/j.jbiotec.2015.02.005.
44. Xu T, Li Y, Shi Z, Hemme CL, Li Y, Zhu Y, Van Nostrand JD, He Z, Zhou J. 2015. Efficient genome editing in Clostridium cellulolyticum via CRISPR-Cas9 nickase. Appl Environ Microbiol 81:4423-4431. http://dx.doi.org/10.1128/AEM.00873-15.
45. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
46. Pyne ME, Moo-Young M, Chung DA, Chou CP. 2013. Development of an electrotransformation protocol for genetic manipulation of Clostridium pasteurianum. Biotechnol Biofuels 6:50. http://dx.doi.org/10.1186/1754-6834-6-50.
47. Heap JT, Pennington OJ, Cartman ST, Minton NP. 2009. A modular system for Clostridium shuttle plasmids. J Microbiol Methods 78:79-85. http://dx.doi.org/10.1016/j.mimet.2009.05.004.
48. Pyne ME, Bruder MR, Moo-Young M, Chung DA, Chou CP. 2016. Harnessing heterologous and endogenous CRISPR-Cas machineries for efficient markerless genome editing in Clostridium. Sci Rep 6:25666. http://dx.doi.org/10.1038/srep25666.
49. Drepper T, Eggert T, Circolone F, Heck A, Krauß U, Guterl J-K, Wendorff M, Losi A, Gärtner W, Jaeger K-E. 2007. Reporter proteins for in vivo fluorescence without oxygen. Nat Biotechnol 25:443-445. http://dx.doi.org/10.1038/nbt1293.
50. Gibson DG, Young L, Chuang R-Y, Venter JC, Hutchison CA, III, Smith HO. 2009. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6:343-345. http://dx.doi.org/10.1038/nmeth.1318.
51. Dong H, Zhang Y, Dai Z, Li Y. 2010. Engineering Clostridium strain to accept unmethylated DNA. PLoS One 5:e9038. http://dx.doi.org/10.1371/journal.pone.0009038.
52. Sternberg SH, Redding S, Jinek M, Greene EC, Doudna JA. 2014. DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 507:62-67. http://dx.doi.org/10.1038/nature13011.
53. Jiang W, Brueggeman AJ, Horken KM, Plucinak TM, Weeks DP. 2014. Successful transient expression of Cas9 and single guide RNA genes in Chlamydomonas reinhardtii. Eukaryot Cell 13:1465-1469. http://dx.doi.org/10.1128/EC.00213-14.
54. Fujii W, Kawasaki K, Sugiura K, Naito K. 2013. Efficient generation of large-scale genome-modified mice using gRNA and Cas9 endonuclease. Nucleic Acids Res 41:e187. http://dx.doi.org/10.1093/nar/gkt772.
55. Gratz SJ, Ukken FP, Rubinstein CD, Thiede G, Donohue LK, Cummings AM, O'Connor-Giles KM. 2014. Highly specific and efficient CRISPR/Cas9-catalyzed homology-directed repair in Drosophila. Genetics 196:961-971. http://dx.doi.org/10.1534/genetics.113.160713.
56. Bruder M, Moo-Young M, Chung DA, Chou CP. 2015. Elimination of carbon catabolite repression in Clostridium acetobutylicum-ajourney toward simultaneous use of xylose and glucose. Appl Microbiol Biotechnol 99:7579-7588. http://dx.doi.org/10.1007/s00253-015-6611-4.
57. Görke B, Stülke J. 2008. Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 6:613-624. http://dx.doi.org/10.1038/nrmicro1932.
58. Nessler S, Fieulaine S, Poncet S, Galinier A, Deutscher J, Janin J. 2003. HPr kinase/phosphorylase, the sensor enzyme of catabolite repression in Gram-positive bacteria: structural aspects of the enzyme and the complex with its protein substrate. J Bacteriol 185:4003-4010. http://dx.doi.org/10.1128/JB.185.14.4003-4010.2003.
59. Paredes CJ, Rigoutsos I, Papoutsakis ET. 2004. Transcriptional organization of the Clostridium acetobutylicum genome. Nucleic Acids Res 32: 1973-1981. http://dx.doi.org/10.1093/nar/gkh509.
60. Brown SD, Nagaraju S, Utturkar S, De Tissera S, Segovia S, Mitchell W, Land ML, Dassanayake A, Köpke M. 2014. Comparison of singlemolecule sequencing and hybrid approaches for finishing the genome of Clostridium autoethanogenum and analysis of CRISPR systems in industrial relevant clostridia. Biotechnol Biofuels 7:40. http://dx.doi.org/10.1186/1754-6834-7-40.
61. Peng L, Pei J, Pang H, Guo Y, Lin L, Huang R. 2014. Whole-genome sequencing reveals a novel CRISPR system in industrial Clostridium acetobutylicum. J Ind Microbiol Biotechnol 41:1677-1685. http://dx.doi.org/10.1007/s10295-014-1507-3.
62. Bermejo LL, Welker NE, Papoutsakis ET. 1998. Expression of Clostridium acetobutylicum ATCC 824 genes in Escherichia coli for acetone production and acetate detoxification. Appl Environ Microbiol 64:1079-1085.
63. Graves MC, Rabinowitz JC. 1986. In vivo and in vitro transcription of the Clostridium pasteurianum ferredoxin gene. Evidence for "extended" promoter elements in Gram-positive organisms. J Biol Chem 261:11409-11415.
64. Santos CNS, Stephanopoulos G. 2008. Combinatorial engineering of microbes for optimizing cellular phenotype. Curr Opin Chem Biol 12: 168-176. http://dx.doi.org/10.1016/j.cbpa.2008.01.017.
65. Doudna JA, Charpentier E. 2014. Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346:1258096.
66. Alper H, Stephanopoulos G. 2007. Global transcription machinery engineering: a new approach for improving cellular phenotype. Metab Eng 9:258-267. http://dx.doi.org/10.1016/j.ymben.2006.12.002.
67. Tummala SB, Welker NE, Papoutsakis ET. 2003. Design of antisense RNA constructs for downregulation of the acetone formation pathway of Clostridium acetobutylicum. J Bacteriol 185:1923-1934. http://dx.doi.org/10.1128/JB.185.6.1923-1934.2003.
68. Choudhary E, Thakur P, Pareek M, Agarwal N. 2015. Gene silencing by CRISPR interference in mycobacteria. Nat Commun 6:6267.
69. Raser JM, O'Shea EK. 2004. Control of stochasticity in eukaryotic gene expression. Science 304:1811-1814. http://dx.doi.org/10.1126/science.1098641.
70. Elowitz MB, Levine AJ, Siggia ED, Swain PS. 2002. Stochastic gene expression in a single cell. Science 297:1183-1186. http://dx.doi.org/10.1126/science.1070919.
71. Newman JRS, Ghaemmaghami S, Ihmels J, Breslow DK, Noble M, DeRisi JL, Weissman JS. 2006. Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441:840-846. http://dx.doi.org/10.1038/nature04785.
72. Galinier A, Kravanja M, Engelmann R, Hengstenberg W, Kilhoffer M-C, Deutscher J, Haiech J. 1998. New protein kinase and protein phosphatase families mediate signal transduction in bacterial catabolite repression. Proc Natl Acad Sci U S A 95:1823-1828. http://dx.doi.org/10.1073/pnas.95.4.1823.
73. Donahue JL, Bownas JL, Niehaus WG, Larson TJ. 2000. Purification and characterization of glpX-encoded fructose 1, 6-bisphosphatase, a new enzyme of the glycerol 3-phosphate regulon of Escherichia coli. J Bacteriol 182:5624-5627. http://dx.doi.org/10.1128/JB.182.19.5624-5627.2000.
74. Tangney M, Galinier A, Deutscher J, Mitchell WJ. 2003. Analysis of the elements of catabolite repression in Clostridium acetobutylicum ATCC 824. J Mol Microbiol Biotechnol 6:6-11. http://dx.doi.org/10.1159/000073403.