Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Global Functional Analysis of Butanol-Sensitive Escherichia coli and Its Evolved Butanol-Tolerant Strain

  • Jeong, Haeyoung (Infectious Disease Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Lee, Seung-Won (SeqGenesis) ;
  • Kim, Sun Hong (Infectious Disease Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Kim, Eun-Youn (School of Basic Sciences, Hanbat National University) ;
  • Kim, Sinyeon (Department of Bioscience and Biotechnology, Konkuk University) ;
  • Yoon, Sung Ho (Department of Bioscience and Biotechnology, Konkuk University)
  • Received : 2017.02.10
  • Accepted : 2017.03.18
  • Published : 2017.06.28
Download PDF
⟨ Previous Next ⟩

Abstract

Butanol is a promising alternative to ethanol and is desirable for use in transportation fuels and additives to gasoline and diesel fuels. Microbial production of butanol is challenging primarily because of its toxicity and low titer of production. Herein, we compared the transcriptome and phenome of wild-type Escherichia coli and its butanol-tolerant evolved strain to understand the global cellular physiology and metabolism responsible for butanol tolerance. When the ancestral butanol-sensitive E. coli was exposed to butanol, gene activities involved in respiratory mechanisms and oxidative stress were highly perturbed. Intriguingly, the evolved butanol-tolerant strain behaved similarly in both the absence and presence of butanol. Among the mutations occurring in the evolved strain, cis-regulatory mutations may be the cause of butanol tolerance. This study provides a foundation for the rational design of the metabolic and regulatory pathways for enhanced biofuel production.

Keywords

References

  1. Fortman JL, Chhabra S, Mukhopadhyay A, Chou H, Lee TS, Steen E, et al. 2008. Biofuel alternatives to ethanol: pumping the microbial well. Trends Biotechnol. 26: 375-381. https://doi.org/10.1016/j.tibtech.2008.03.008
  2. Lutke-Eversloh T, Bahl H. 2011. Metabolic engineering of Clostridium acetobutylicum: recent advances to improve butanol production. Curr. Opin. Biotechnol. 22: 634-647. https://doi.org/10.1016/j.copbio.2011.01.011
  3. Jang YS, Lee JY, Lee J, Park JH, Im JA, Eom MH, et al. 2012. Enhanced butanol production obtained by reinforcing the direct butanol-forming route in Clostridium acetobutylicum. MBio 3: e00314-12.
  4. Knoshaug EP, Zhang M. 2009. Butanol tolerance in a selection of microorganisms. Appl. Biochem. Biotechnol. 153: 13-20. https://doi.org/10.1007/s12010-008-8460-4
  5. Yoon SH, Jeong H, Kwon S-K, Kim JF. 2009. Genomics, biological features, and biotechnological applications of Escherichia coli B: "Is B for better?!", pp. 1-17. In Lee SY (ed.). Systems Biology and Biotechnology of Escherichia coli. Springer, Berlin, Germany.
  6. Atsumi S, Cann AF, Connor MR, Shen CR, Smith KM, Brynildsen MP, et al. 2008. Metabolic engineering of Escherichia coli for 1-butanol production. Metab. Eng. 10: 305-311. https://doi.org/10.1016/j.ymben.2007.08.003
  7. Gulevich AY, Skorokhodova AY, Sukhozhenko AV, Shakulov RS, Debabov VG. 2012. Metabolic engineering of Escherichia coli for 1-butanol biosynthesis through the inverted aerobic fatty acid beta-oxidation pathway. Biotechnol. Lett. 34: 463-469. https://doi.org/10.1007/s10529-011-0797-z
  8. Shen CR, Liao JC. 2008. Metabolic engineering of Escherichia coli for 1-butanol and 1-propanol production via the ketoacid pathways. Metab. Eng. 10: 312-320. https://doi.org/10.1016/j.ymben.2008.08.001
  9. Dong H, Zhao C, Zhang T, Lin Z, Li Y, Zhang Y. 2016. Engineering Escherichia coli cell factories for n-butanol production. Adv. Biochem. Eng. Biotechnol. 155: 141-163.
  10. Zhang H, Chong H, Ching CB, Song H, Jiang R. 2012. Engineering global transcription factor cyclic AMP receptor protein of Escherichia coli for improved 1-butanol tolerance. Appl. Microbiol. Biotechnol. 94: 1107-1117. https://doi.org/10.1007/s00253-012-4012-5
  11. 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. https://doi.org/10.1002/bit.22989
  12. Reyes LH, Almario MP, Kao KC. 2011. Genomic library screens for genes involved in n-butanol tolerance in Escherichia coli. PLoS One 6: e17678. https://doi.org/10.1371/journal.pone.0017678
  13. Tomas CA, Welker NE, Papoutsakis ET. 2003. Overexpression of groESL in Clostridium acetobutylicum results in increased solvent production and tolerance, prolonged metabolism, and changes in the cell's transcriptional program. Appl. Environ. Microbiol. 69: 4951-4965. https://doi.org/10.1128/AEM.69.8.4951-4965.2003
  14. Rutherford BJ, Dahl RH, Price RE, Szmidt HL, Benke PI, Mukhopadhyay A, et al. 2010. Functional genomic study of exogenous n-butanol stress in Escherichia coli. Appl. Environ. Microbiol. 76: 1935-1945. https://doi.org/10.1128/AEM.02323-09
  15. Atsumi S, Wu TY, Machado IM, Huang WC, Chen PY, Pellegrini M, et al. 2010. Evolution, genomic analysis, and reconstruction of isobutanol tolerance in Escherichia coli. Mol. Syst. Biol. 6: 449.
  16. Jeong H, Kim S, Han S, Kim M, Lee K. 2012. Changes in membrane fatty acid composition through proton-induced fabF mutation enhancing 1-butanol tolerance in E. coli. J. Korean Phys. Soc. 61: 227-233. https://doi.org/10.3938/jkps.61.227
  17. Barrick JE, Yu DS, Yoon SH, Jeong H, Oh TK, Schneider D, et al. 2009. Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461: 1243-1247. https://doi.org/10.1038/nature08480
  18. Jeong H, Han J. 2010. Enhancing the 1-butanol tolerance in Escherichia coli through repetitive proton beam irradiation. J. Korean Phys. Soc. 56: 2041-2045. https://doi.org/10.3938/jkps.56.2041
  19. Garwin JL, Klages AL, Cronan JE Jr. 1980. Beta-ketoacyl-acyl carrier protein synthase II of Escherichia coli. Evidence for function in the thermal regulation of fatty acid synthesis. J. Biol. Chem. 255: 3263-3265.
  20. Yoon SH, Han MJ, Jeong H, Lee CH, Xia XX, Lee DH, et al. 2012. Comparative multi-omics systems analysis of Escherichia coli strains B and K-12. Genome Biol. 13: R37. https://doi.org/10.1186/gb-2012-13-5-r37
  21. Richter M, Rossello-Mora R. 2009. Shifting the genomic gold standard for the prokaryotic species definition. Proc. Natl. Acad. Sci. USA 106: 19126-19131. https://doi.org/10.1073/pnas.0906412106
  22. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. 2009. BLAST+: architecture and applications. BMC Bioinformatics 10: 421. https://doi.org/10.1186/1471-2105-10-421
  23. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, et al. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5: R80. https://doi.org/10.1186/gb-2004-5-10-r80
  24. Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK. 2015. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43: e47. https://doi.org/10.1093/nar/gkv007
  25. Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, et al. 2015. STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 43: D447-D452. https://doi.org/10.1093/nar/gku1003
  26. Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N, Workman C, et al. 2007. Integration of biological networks and gene expression data using Cytoscape. Nat. Protoc. 2: 2366-2382. https://doi.org/10.1038/nprot.2007.324
  27. Shannon PT, Reiss DJ, Bonneau R, Baliga NS. 2006. The Gaggle: an open-source software system for integrating bioinformatics software and data sources. BMC Bioinformatics 7: 176. https://doi.org/10.1186/1471-2105-7-176
  28. Vaas LA, Sikorski J, Hofner B, Fiebig A, Buddruhs N, Klenk HP, et al. 2013. opm: an R package for analysing OmniLog$^{(R)}$ phenotype microarray data. Bioinformatics 29: 1823-1824. https://doi.org/10.1093/bioinformatics/btt291
  29. Yoon SH, Reiss DJ, Bare JC, Tenenbaum D, Pan M, Slagel J, et al. 2011. Parallel evolution of transcriptome architecture during genome reorganization. Genome Res. 21: 1892-1904. https://doi.org/10.1101/gr.122218.111
  30. Tatusov RL, Galperin MY, Natale DA, Koonin EV. 2000. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 28: 33-36. https://doi.org/10.1093/nar/28.1.33
  31. Hesslinger C, Fairhurst SA, Sawers G. 1998. Novel keto acid formate-lyase and propionate kinase enzymes are components of an anaerobic pathway in Escherichia coli that degrades L-threonine to propionate. Mol. Microbiol. 27: 477-492. https://doi.org/10.1046/j.1365-2958.1998.00696.x
  32. Volkers RJ, Ballerstedt H, Ruijssenaars H, de Bont JA, de Winde JH, Wery J. 2009. TrgI, toluene repressed gene I, a novel gene involved in toluene-tolerance in Pseudomonas putida S12. Extremophiles 13: 283-297. https://doi.org/10.1007/s00792-008-0216-0
  33. Park SJ, Gunsalus RP. 1995. Oxygen, iron, carbon, and superoxide control of the fumarase fumA and fumC genes of Escherichia coli: role of the arcA, fnr, and soxR gene products. J. Bacteriol. 177: 6255-6262. https://doi.org/10.1128/jb.177.21.6255-6262.1995
  34. Dunlop MJ. 2011. Engineering microbes for tolerance to next-generation biofuels. Biotechnol. Biofuels 4: 32. https://doi.org/10.1186/1754-6834-4-32
  35. Rowley G, Spector M, Kormanec J, Roberts M. 2006. Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens. Nat. Rev. Microbiol. 4: 383-394. https://doi.org/10.1038/nrmicro1394
  36. Darwin AJ. 2005. The phage-shock-protein response. Mol. Microbiol. 57: 621-628. https://doi.org/10.1111/j.1365-2958.2005.04694.x
  37. Janausch IG, Zientz E, Tran QH, Kroger A, Unden G. 2002. $C_4$-dicarboxylate carriers and sensors in bacteria. Biochim. Biophys. Acta 1553: 39-56. https://doi.org/10.1016/S0005-2728(01)00233-X
  38. Doerrler WT, Sikdar R, Kumar S, Boughner LA. 2013. New functions for the ancient DedA membrane protein family. J. Bacteriol. 195: 3-11. https://doi.org/10.1128/JB.01006-12
  39. Kumar S, Doerrler WT. 2014. Members of the conserved DedA family are likely membrane transporters and are required for drug resistance in Escherichia coli. Antimicrob. Agents Chemother. 58: 923-930. https://doi.org/10.1128/AAC.02238-13
  40. Sikdar R, Simmons AR, Doerrler WT. 2013. Multiple envelope stress response pathways are activated in an Escherichia coli strain with mutations in two members of the DedA membrane protein family. J. Bacteriol. 195: 12-24. https://doi.org/10.1128/JB.00762-12
  41. Jair KW, Yu X, Skarstad K, Thony B, Fujita N, Ishihama A, Wolf RE Jr. 1996. Transcriptional activation of promoters of the superoxide and multiple antibiotic resistance regulons by Rob, a binding protein of the Escherichia coli origin of chromosomal replication. J. Bacteriol. 178: 2507-2513. https://doi.org/10.1128/jb.178.9.2507-2513.1996
  42. Bennik MH, Pomposiello PJ, Thorne DF, Demple B. 2000. Defining a rob regulon in Escherichia coli by using transposon mutagenesis. J. Bacteriol. 182: 3794-3801. https://doi.org/10.1128/JB.182.13.3794-3801.2000
  43. Wray GA. 2007. The evolutionary significance of cisregulatory mutations. Nat. Rev. Genet. 8: 206-216.
  44. Stern DL, Orgogozo V. 2008. The loci of evolution: how predictable is genetic evolution? Evolution 62: 2155-2177. https://doi.org/10.1111/j.1558-5646.2008.00450.x

Cited by

  1. Escherichia coli as a model organism for systems metabolic engineering vol.6, pp.None, 2017, https://doi.org/10.1016/j.coisb.2017.11.001
  2. Understanding and engineering alcohol-tolerant bacteria using OMICS technology vol.34, pp.11, 2017, https://doi.org/10.1007/s11274-018-2542-4
  3. Synthetic Biology and Metabolic Engineering Employing Escherichia coli for C2–C6 Bioalcohol Production vol.8, pp.None, 2020, https://doi.org/10.3389/fbioe.2020.00710
  4. Metabolic engineering strategies for butanol production in Escherichia coli vol.117, pp.8, 2017, https://doi.org/10.1002/bit.27377