DOI QR코드

DOI QR Code

Development of Genome Engineering Tools for Metabolic Engineering of Butanol-producing Clostridium Species

Butanol 생합성 Clostridium 속 미생물 대사공학용 게놈 편집 도구 개발

  • Woo, Ji Eun (Institute of Agriculture & Life Science (IALS), Department of Agricultural Chemistry and Food Science Technology, Gyeongsang National University) ;
  • Kim, Minji (Institute of Agriculture & Life Science (IALS), Department of Agricultural Chemistry and Food Science Technology, Gyeongsang National University) ;
  • Lee, Ji Won (Institute of Agriculture & Life Science (IALS), Department of Agricultural Chemistry and Food Science Technology, Gyeongsang National University) ;
  • Seo, Hyo Joo (Institute of Agriculture & Life Science (IALS), Department of Agricultural Chemistry and Food Science Technology, Gyeongsang National University) ;
  • Lee, Sang Yup (Metabolic and Biomolecular Engineering National Research Laboratory, Department of Chemical and Biomolecular Engineering (BK21 plus program), Bioinformatics Research Center, BioProcess Engineering Research Center, Center for Systems and Synthetic Biotechnology, KAIST) ;
  • Jang, Yu-Sin (Institute of Agriculture & Life Science (IALS), Department of Agricultural Chemistry and Food Science Technology, Gyeongsang National University)
  • 우지은 (경상대학교 농업생명과학연구원) ;
  • 김민지 (경상대학교 농업생명과학연구원) ;
  • 이지원 (경상대학교 농업생명과학연구원) ;
  • 서효주 (경상대학교 농업생명과학연구원) ;
  • 이상엽 (한국과학기술원 생명화학공학과) ;
  • 장유신 (경상대학교 농업생명과학연구원)
  • Received : 2016.11.22
  • Accepted : 2016.12.05
  • Published : 2016.12.31

Abstract

Global warming caused from the heavy consumption of fossil fuel is one of the biggest problems to be solved. Biofuel has been gained more attention as an alternative to reduce the consumption of fossil fuel. Recently, butanol produced from the genus Clostridium has been considered as one of the promising alternatives for gasoline, fossil based fuel. Nevertheless, the lack of the genome-engineering tools for the genus Clostridium is the major hurdle for the economic production of butanol. More recently, genome engineering tools have been developed for metabolic engineering of butanol-producing Clostridium species, which includes genome scale network model and genome editing tools on the basis of mobile group II introns and CRISPR/Cas system. In this study, the genome engineering tools for butanol-producing Clostridium species have been reviewed with a brief future perspective.

Keywords

References

  1. Jang, Y. S., J. Y. Lee, J. Lee, J. H. Park, J. A. Im, M. H. Eom, J. Lee, S. H. Lee, H. Song, J. H. Cho, D. Y. Seung, and S. Y. Lee (2012) Enhanced butanol production obtained by reinforcing the direct butanol-forming route in Clostridium acetobutylicum. mBio 3: e00314-12.
  2. Nolling, J., G. Breton, M. V. Omelchenko, K. S. Makarova, Q. Zeng, R. Gibson, H. M. Lee, J. Dubois, D. Qiu, J. Hitti, Y. I. Wolf, R. L. Tatusov, F. Sabathe, L. Doucette-Stamm, P. Soucaille, M. J. Daly, G. N. Bennett, E. V. Koonin, and D. R. Smith (2001) Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum. J. Bacteriol. 183: 4823-4838. https://doi.org/10.1128/JB.183.16.4823-4838.2001
  3. Cho, C., Y.-S. Jang, H. G. Moon, J. Lee, and S. Y. Lee (2015) Metabolic engineering of clostridia for the production of chemicals. Biof. Bioprod. Bioref. 9: 211-225. https://doi.org/10.1002/bbb.1531
  4. Mo, X., J. Pei, Y. Guo, L. Lin, L. Peng, C. Kou, D. Fan, and H. Pang (2015) Genome sequence of Clostridium acetobutylicum GX AS18-1, a novel biobutanol production strain. Genome Announc. 3: e00033-15.
  5. Bao, G., R. Wang, Y. Zhu, H. Dong, S. Mao, Y. Zhang, Z. Chen, Y. Li, and Y. Ma (2011) Complete genome sequence of Clostridium acetobutylicum DSM 1731, a solvent-producing strain with multireplicon genome architecture. J. Bacteriol. 193: 5007-5008. https://doi.org/10.1128/JB.05596-11
  6. Hu, S., H. Zheng, Y. Gu, J. Zhao, W. Zhang, Y. Yang, S. Wang, G. Zhao, S. Yang, and W. Jiang (2011) Comparative genomic and transcriptomic analysis revealed genetic characteristics related to solvent formation and xylose utilization in Clostridium acetobutylicum EA 2018. BMC Genomics 12: 93. https://doi.org/10.1186/1471-2164-12-93
  7. Li, N., J. Yang, C. Chai, S. Yang, W. Jiang, and Y. Gu (2015) Complete genome sequence of Clostridium carboxidivorans P7T, a syngas-fermenting bacterium capable of producing long-chain alcohols. J. Biotechnol. 211: 44-45. https://doi.org/10.1016/j.jbiotec.2015.06.430
  8. Wang, Y., X. Li, Y. Mao, and H. P. Blaschek (2012) Genome-wide dynamic transcriptional profiling in Clostridium beijerinckii NCIMB 8052 using single-nucleotide resolution RNA-Seq. BMC Genomics 13: 102. https://doi.org/10.1186/1471-2164-13-102
  9. Lee, J., Y. S. Jang, M. J. Han, J. Y. Kim, and S. Y. Lee (2016) Deciphering Clostridium tyrobutyricum metabolism based on the wholegenome sequence and proteome analyses. mBio 7: e00743-16.
  10. Kopke, M., C. Held, S. Hujer, H. Liesegang, A. Wiezer, A. Wollherr, A. Ehrenreich, W. Liebl, G. Gottschalk, and P. Durre (2010) Clostridium ljungdahlii represents a microbial production platform based on syngas. Proc. Natl. Acad. Sci. USA 107: 13087-13092. https://doi.org/10.1073/pnas.1004716107
  11. Papoutsakis, E. T. (1984) Equations and calculations for fermentations of butyric acid bacteria. Biotechnol. Bioeng. 26: 174-187. https://doi.org/10.1002/bit.260260210
  12. Papoutsakis, E. T. and C. L. Meyer (1985) Equations and calculations of product yields and preferred pathways for butanediol and mixed-acid fermentations. Biotechnol. Bioeng. 27: 50-66. https://doi.org/10.1002/bit.260270108
  13. Kim, S., Y. S. Jang, S. C. Ha, J. W. Ahn, E. J. Kim, J. H. Lim, C. Cho, Y. S. Ryu, S. K. Lee, S. Y. Lee, and K. J. Kim (2015) Redoxswitch regulatory mechanism of thiolase from Clostridium acetobutylicum. Nat. Commun. 6: 8410. https://doi.org/10.1038/ncomms9410
  14. Desai, R. P., L. M. Harris, N. E. Welker, and E. T. Papoutsakis (1999) Metabolic flux analysis elucidates the importance of the acid-formation pathways in regulating solvent production by Clostridium acetobutylicum. Metab. Eng. 1: 206-213. https://doi.org/10.1006/mben.1999.0118
  15. Sillers, R., M. A. Al-Hinai, and E. T. Papoutsakis (2009) Aldehyde-alcohol dehydrogenase and/or thiolase overexpression coupled with CoA transferase downregulation lead to higher alcohol titers and selectivity in Clostridium acetobutylicum fermentations. Biotechnol. Bioeng. 102: 38-49. https://doi.org/10.1002/bit.22058
  16. Lee, J., H. Yun, A. M. Feist, B. O. Palsson, and S. Y. Lee (2008) Genome-scale reconstruction and in silico analysis of the Clostridium acetobutylicum ATCC 824 metabolic network. Appl. Microbiol. Biotechnol. 80: 849-862. https://doi.org/10.1007/s00253-008-1654-4
  17. Senger, R. S. and E. T. Papoutsakis (2008) Genome-scale model for Clostridium acetobutylicum: Part I. Metabolic network resolution and analysis. Biotechnol. Bioeng. 101: 1036-1052. https://doi.org/10.1002/bit.22010
  18. Senger, R. S. and E. T. Papoutsakis (2008) Genome-scale model for Clostridium acetobutylicum: Part II. Development of specific proton flux states and numerically determined sub-systems. Biotechnol. Bioeng. 101: 1053-1071. https://doi.org/10.1002/bit.22009
  19. Gallardo, R., A. Acevedo, J. Quintero, I. Paredes, R. Conejeros, and G. Aroca (2016) In silico analysis of Clostridium acetobutylicum ATCC 824 metabolic response to an external electron supply. Bioprocess Biosyst. Eng. 39: 295-305. https://doi.org/10.1007/s00449-015-1513-5
  20. Milne, C. B., J. A. Eddy, R. Raju, S. Ardekani, P. J. Kim, R. S. Senger, Y. S. Jin, H. P. Blaschek, and N. D. Price (2011) Metabolic network reconstruction and genome-scale model of butanolproducing strain Clostridium beijerinckii NCIMB 8052. BMC Syst. Biol. 5: 130. https://doi.org/10.1186/1752-0509-5-130
  21. Shinto, H., Y. Tashiro, G. Kobayashi, T. Sekiguchi, T. Hanai, Y. Kuriya, M. Okamoto, and K. Sonomoto (2008) Kinetic study of substrate dependency for higher butanol production in acetonebutanol- ethanol fermentation. Process Biochem. 43: 1452-1461. https://doi.org/10.1016/j.procbio.2008.06.003
  22. Li, R.-D., Y.-Y. Li, L.-Y. Lu, C. Ren, Y.-X. Li, and L. Liu (2011) An improved kinetic model for the acetone-butanol-ethanol pathway of Clostridium acetobutylicum and model-based perturbation analysis. BMC Syst. Biol. 5: S12.
  23. Haus, S., S. Jabbari, T. Millat, H. Janssen, R.-J. Fischer, H. Bahl, J. R. King, and O. Wolkenhauer (2011) A systems biology approach to investigate the effect of pH-induced gene regulation on solvent production by Clostridium acetobutylicum in continuous culture. BMC Syst. Biol. 5: 10. https://doi.org/10.1186/1752-0509-5-10
  24. Thorn, G. J., J. R. King, and S. Jabbari (2013) pH-induced gene regulation of solvent production by Clostridium acetobutylicum in continuous culture: parameter estimation and sporulation modelling. Math. Biosci. 241: 149-166. https://doi.org/10.1016/j.mbs.2012.11.004
  25. Millat, T., H. Janssen, H. Bahl, R.-J. Fischer, and O. Wolkenhauer (2013) Integrative modelling of pH-dependent enzyme activity and transcriptomic regulation of the acetone-butanol-ethanol fermentation of Clostridium acetobutylicum in continuous culture. Microb. Biotechnol. 6: 526-539. https://doi.org/10.1111/1751-7915.12033
  26. Millat, T., H. Janssen, G. J. Thorn, J. R. King, H. Bahl, R.-J. Fischer, and O. Wolkenhauer (2013) A shift in the dominant phenotype governs the pH-induced metabolic switch of Clostridium acetobutylicumin phosphate-limited continuous cultures. Appl. Microbiol. Biotechnol. 97: 6451-6466. https://doi.org/10.1007/s00253-013-4860-7
  27. Liao, C., S.-O. Seo, and T. Lu (2016) System-level modeling of acetone-butanol-ethanol fermentation. FEMS Microbiol. Lett. 363: fnw074. https://doi.org/10.1093/femsle/fnw074
  28. Liao, C., S.-O. Seo, V. Celik, H. Liu, W. Kong, Y. Wang, H. Blaschek, Y.-S. Jin, and T. Lu (2015) Integrated, systems metabolic picture of acetone-butanol-ethanol fermentation by Clostridium acetobutylicum. Proc. Natl. Acad. Sci. USA 112: 8505-8510. https://doi.org/10.1073/pnas.1423143112
  29. Swinfield, T. J., J. D. Oultram, D. E. Thompson, J. K. Brehm, and N. P. Minton (1990) Physical characterisation of the replication region of the Streptococcus faecalis plasmid pAM beta 1. Gene 87: 79-90.
  30. Lee, S. Y., L. D. Mermelstein, G. N. Bennett, and E. T. Papoutsakis (1992) Vector construction, transformation, and gene amplification in Clostridium acetobutylicum ATCC 824. Ann. N.Y. Acad. Sci. 665: 39-51. https://doi.org/10.1111/j.1749-6632.1992.tb42572.x
  31. Fox, M. E., M. J. Lemmon, M. L. Mauchline, T. O. Davis, A. J. Giaccia, N. P. Minton, and J. M. Brown (1996) Anaerobic bacteria as a delivery system for cancer gene therapy: in vitro activation of 5-fluorocytosine by genetically engineered clostridia. Gene Ther. 3: 173-178.
  32. Mermelstein, L. D., N. E. Welker, G. N. Bennett, and E. T. Papoutsakis (1992) Expression of cloned homologous fermentative genes in Clostridium acetobutylicum ATCC 824. Biotechnology 10: 190-195.
  33. Green, E. M., Z. L. Boynton, L. M. Harris, F. B. Rudolph, E. T. Papoutsakis, and G. N. Bennett (1996) Genetic manipulation of acid formation pathways by gene inactivation in Clostridium acetobutylicum ATCC 824. Microbiology 142: 2079-2086. https://doi.org/10.1099/13500872-142-8-2079
  34. Shao, L., S. Hu, Y. Yang, Y. Gu, J. Chen, Y. Yang, W. Jiang, and S. Yang (2007) Targeted gene disruption by use of a group II intron (targetron) vector in Clostridium acetobutylicum. Cell Res. 17: 963-965. https://doi.org/10.1038/cr.2007.91
  35. Heap, J. T., O. J. Pennington, S. T. Cartman, G. P. Carter, and N. P. Minton (2007) The ClosTron: A universal gene knock-out system for the genus Clostridium. J. Microbiol. Methods 70: 452-464. https://doi.org/10.1016/j.mimet.2007.05.021
  36. Lambowitz, A. M. and S. Zimmerly (2004) Mobile Group II Introns. Annu. Rev. Genet. 38: 1-35. https://doi.org/10.1146/annurev.genet.38.072902.091600
  37. Martinez-Abarca, F. and N. Toro (2000) Group II introns in the bacterial world. Mol. Microbiol. 38: 917-926.
  38. Mohr, G., W. Hong, J. Zhang, G. Z. Cui, Y. Yang, Q. Cui, Y. J. Liu, and A. M. Lambowitz (2013) A targetron system for gene targeting in thermophiles and its application in Clostridium thermocellum. PLoS One 8: e69032. https://doi.org/10.1371/journal.pone.0069032
  39. Heap, J. T., S. A. Kuehne, M. Ehsaan, S. T. Cartman, C. M. Cooksley, J. C. Scott, and N. P. Minton (2010) The ClosTron: mutagenesis in Clostridium refined and streamlined. J. Microbiol. Methods 80: 49-55. https://doi.org/10.1016/j.mimet.2009.10.018
  40. Jang, Y.-S., J. A. Im, S. Y. Choi, J. I. Lee, and S. Y. Lee (2014) Metabolic engineering of Clostridium acetobutylicum for butyric acid production with high butyric acid selectivity. Metabol. Eng. 23: 165-174. https://doi.org/10.1016/j.ymben.2014.03.004
  41. Haurwitz, R. E., M. Jinek, B. Wiedenheft, K. Zhou, and J. A. Doudna (2010) Sequence- and structure-specific RNA processing by a CRISPR endonuclease. Science 329: 1355-1358. https://doi.org/10.1126/science.1192272
  42. Jinek, M., K. Chylinski, I. Fonfara, M. Hauer, J. A. Doudna, and E. Charpentier (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337: 816-821. https://doi.org/10.1126/science.1225829
  43. Huang, H., C. Chai, N. Li, P. Rowe, N. P. Minton, S. Yang, W. Jiang, and Y. Gu (2016) CRISPR/Cas9-based efficient genome editing in Clostridium ljungdahlii, an autotrophic gas-fermenting bacterium. ACS Synth. Biol. (doi: 10.1021/acssynbio.6b00044) in press.
  44. Wang, Y., Z.-T. Zhang, S.-O. Seo, K. Choi, T. Lu, Y.-S. Jin, and H. P. Blaschek (2015) Markerless chromosomal gene deletion in Clostridium beijerinckii using CRISPR/Cas9 system. J. Biotechnol. 200: 1-5. https://doi.org/10.1016/j.jbiotec.2015.02.005
  45. Bruder, M. R., M. E. Pyne, M. Moo-Young, D. A. Chung, and C. P. Chou (2016) Extending CRISPR-Cas9 technology from genome editing to transcriptional engineering in Clostridium. Appl. Environ. Microbiol. (doi: 10.1128/aem.02128-16) in press.
  46. Pyne, M. E., M. R. Bruder, M. Moo-Young, D. A. Chung, and C. P. Chou (2016) Harnessing heterologous and endogenous CRISPRCas machineries for efficient markerless genome editing in Clostridium. Sci. Rep. 6: 25666. https://doi.org/10.1038/srep25666

Cited by

  1. Metabolic Engineering Strategies of Clostridia for Butyric Acid Production vol.32, pp.3, 2017, https://doi.org/10.7841/ksbbj.2017.32.3.169