DOI QR코드

DOI QR Code

irrE, an Exogenous Gene from Deinococcus radiodurans, Improves the Growth of and Ethanol Production by a Zymomonas mobilis Strain Under Ethanol and Acid Stresses

  • Zhang, Ying (Biotechnology Research Institute, Chinese Academy of Agricultural Sciences) ;
  • Ma, Ruiqiang (Biotechnology Research Institute, Chinese Academy of Agricultural Sciences) ;
  • Zhao, Zhonglin (College of Life Sciences, Shenzhen University) ;
  • Zhou, Zhengfu (Biotechnology Research Institute, Chinese Academy of Agricultural Sciences) ;
  • Lu, Wei (Biotechnology Research Institute, Chinese Academy of Agricultural Sciences) ;
  • Zhang, Wei (Biotechnology Research Institute, Chinese Academy of Agricultural Sciences) ;
  • Chen, Ming (Biotechnology Research Institute, Chinese Academy of Agricultural Sciences)
  • 투고 : 2009.12.30
  • 심사 : 2010.04.09
  • 발행 : 2010.07.28

초록

During ethanol fermentation, bacterial strains may encounter various stresses, such as ethanol and acid shock, which adversely affect cell viability and the production of ethanol. Therefore, ethanologenic strains that tolerate abiotic stresses are highly desirable. Bacteria of the genus Deinococcus are extremely resistant to ionizing radiation, ultraviolet light, and desiccation, and therefore constitute an important pool of extreme resistance genes. The irrE gene encodes a general switch responsible for the extreme radioresistance of D. radiodurans. Here, we present evidence that IrrE, acting as a global regulator, confers high stress tolerance to a Zymomonas mobilis strain. Expression of the gene protected Z. mobilis cells against ethanol, acid, osmotic, and thermal shocks. It also markedly improved cell viability, the expression levels and enzyme activities of pyruvate decarboxylase and alcohol dehydrogenase, and the production of ethanol under both ethanol and acid stresses. These data suggest that irrE is a potentially promising gene for improving the abiotic stress tolerance of ethanologenic bacterial strains.

키워드

참고문헌

  1. Alper, H., Y. S. Jin, J. F. Moxley, and G. Stephanopoulos. 2005. Identifying gene targets for the metabolic engineering of lycopene biosynthesis in Escherichia coli. Metab. Eng. 7: 155-164. https://doi.org/10.1016/j.ymben.2004.12.003
  2. Alper, H., K. Miyaoku, and G. Stephanopoulos. 2005. Construction of lycopene-overproducing E. coli strains by combining systematic and combinatorial gene knockout targets. Nat. Biotechnol. 23: 612-616. https://doi.org/10.1038/nbt1083
  3. Alper, H. and G. Stephanopoulos. 2007. Global transcription machinery engineering: A new approach for improving cellular phenotype. Metab. Eng. 9: 258-267. https://doi.org/10.1016/j.ymben.2006.12.002
  4. Barnell, W. O., K. C. Yi, and T. Conway. 1990. Sequence and genetic organization of a Zymomonas mobilis gene cluster that encodes several enzymes of glucose metabolism. J. Bacteriol. 172: 7227-7240.
  5. Baumler, D. J., K. F. Hung, J. L. Bose, B. M. Vykhodets, C. M. Cheng, K. C. Jeong, and C. W. Kaspar. 2006. Enhancement of acid tolerance in Zymomonas mobilis by a proton-buffering peptide. Appl. Biochem. Biotechnol. 134: 15-26. https://doi.org/10.1385/ABAB:134:1:15
  6. Conway, T., Y. A. Osman, J. I. Konnan, E. M. Hoffmann, and L. O. Ingram. 1987. Promoter and nucleotide sequences of the Zymomonas mobilis pyruvate decarboxylase. J. Bacteriol. 169: 949-954.
  7. Earl, A. M., M. M. Mohundro, I. S. Mian, and J. R. Battista. 2002. The IrrE protein of Deinococcus radiodurans R1 is a novel regulator of recA expression. J. Bacteriol. 123: 6216-6224.
  8. Galani, T. M. A. A. 1992. Chemical and UV mutagenesis in Zymomonas mobilis. Genetica 87: 37-45. https://doi.org/10.1007/BF00128771
  9. Gao, G., B. Tian, L. Liu, D. Sheng, B. Shen, and Y. Hua. 2003. Expression of Deinococcus radiodurans PprI enhances the radioresistance of Escherichia coli. DNA Repair (Amst) 2: 1419-1427. https://doi.org/10.1016/j.dnarep.2003.08.012
  10. Haber, J. E., D. T. Rogers, and J. H. McCusker. 1980. Homothallic conversions of yeast mating-type genes occur by intrachromosomal recombination. Cell 22: 277-289. https://doi.org/10.1016/0092-8674(80)90175-0
  11. Hengge-Aronis, R. 2002. Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase. Microbiol. Mol. Biol. Rev. 66: 373-395, table of contents. https://doi.org/10.1128/MMBR.66.3.373-395.2002
  12. Hirasawa, T., K. Yoshikawa, Y. Nakakura, K. Nagahisa, C. Furusawa, Y. Katakura, H. Shimizu, and S. Shioya. 2007. Identification of target genes conferring ethanol stress tolerance to Saccharomyces cerevisiae based on DNA microarray data analysis. J. Biotechnol. 131: 34-44. https://doi.org/10.1016/j.jbiotec.2007.05.010
  13. Hua, Y., I. Narumi, G. Gao, B. Tian, K. Satoh, S. Kitayama, and B. Shen. 2003. PprI: A general switch responsible for extreme radioresistance of Deinococcus radiodurans. Biochem. Biophys. Res. Communication 306: 354-360. https://doi.org/10.1016/S0006-291X(03)00965-3
  14. Joachimsthal, E. L. and P. L. Rogers. 2000. Characterization of a high-productivity recombinant strain of Zymomonas mobilis for ethanol production from glucose/xylose mixtures. Appl. Biochem. Biotechnol. 84-86: 343-356. https://doi.org/10.1385/ABAB:84-86:1-9:343
  15. Kajiwara, S, K. Suga, H. Sone, and K. Nakamura. 2000. Improved ethanol tolerance of Saccharomyces cerevisiae strains by increases in fatty acid unsaturation via metabolic engineering. Biotechnol. Lett. 22: 1839-1843. https://doi.org/10.1023/A:1005632522620
  16. Kim, I. S., K. D. Barrow, and P. L. Rogers. 2000. Nuclear magnetic resonance studies of acetic acid inhibition of rec Zymomonas mobilis ZM4(pZB5). Appl. Biochem. Biotechnol. 84-86: 357-370. https://doi.org/10.1385/ABAB:84-86:1-9:357
  17. Kobayashi, A., H. Hirakawa, T. Hirata, K. Nishino, and A. Yamaguchi. 2006. Growth phase-dependent expression of drug exporters in Escherichia coli and its contribution to drug tolerance. J. Bacteriol. 188: 5693-5703. https://doi.org/10.1128/JB.00217-06
  18. Lawford, H. G. 1992. The effect of lactic acid on fuel ethanol production by Zymomonas. Appl. Biochem. Biotechnol. 34-35: 205-216. https://doi.org/10.1007/BF02920546
  19. Mackenzie, K. F., C. K. Eddy, and L. O. Ingram. 1989. Modulation of alcohol dehydrogenase isoenzyme levels in Zymomonas mobilis by iron and zinc. J. Bacteriol. 171: 1063-1067.
  20. Makarova, K. S., M. V. Omelchenko, E. K. Gaidamakova, V. Y. Matrosova, A. Vasilenko, M. Zhai, et al. 2007. Deinococcus geothermalis: The pool of extreme radiation resistance genes shrinks. PLoS ONE 2: e955. https://doi.org/10.1371/journal.pone.0000955
  21. Michel, G. P. and J. Starka. 1986. Effect of ethanol and heat stresses on the protein pattern of Zymomonas mobilis. J. Bacteriol. 165: 1040-1042.
  22. Miller, E. N. and L. O. Ingram. 2007. Combined effect of betaine and trehalose on osmotic tolerance of Escherichia coli in mineral salts medium. Biotechnol. Lett. 29: 213-217. https://doi.org/10.1007/s10529-006-9226-0
  23. Neale, A. D., R. K. Scopes, J. M. Kelly, and R. E. Wettenhall. 1986. The two alcohol dehydrogenases of Zymomonas mobilis. Purification by differential dye ligand chromatography, molecular characterisation and physiological roles. Eur. J. Biochem. 154: 119-124. https://doi.org/10.1111/j.1432-1033.1986.tb09366.x
  24. Osman, Y. A. and L. O. Ingram. 1985. Mechanism of ethanol inhibition of fermentation in Zymomonas mobilis CP4. J. Bacteriol. 164: 173-180.
  25. Pan, J., J. Z. Wang, Z. Yan, Y. Zhang, W. Lu, W. Ping, et al. 2009. IrrE, a global regulator of extreme radiation resistance in Deinococcus radiodurans, enhances salt tolerance in Escherichia coli and Brassica napus. PLoS ONE 4: e4422. https://doi.org/10.1371/journal.pone.0004422
  26. Park, S. C. and J. Baratti. 1991. Batch fermentation kinetics of sugar beet molasses by Zymomonas mobilis. Biotechnol. Bioeng. 38: 304-313. https://doi.org/10.1002/bit.260380312
  27. Purvis, J. E., L. P. Yomano, and L. O. Ingram. 2005. Enhanced trehalose production improves growth of Escherichia coli under osmotic stress. Appl. Environ. Microbiol. 71: 3761-3769. https://doi.org/10.1128/AEM.71.7.3761-3769.2005
  28. Seo, J. S. C., H. Park, H. S. Yoon, K. O. Jung, C. Kim, J. J. Hong, et al. 2005. The genome sequence of the ethanologenic bacterium Zymomonas mobilis ZM4. Nat. Biotechnol. 23: 63-68. https://doi.org/10.1038/nbt1045
  29. Tao, F., J. Y. Miao, G. Y. Shi, and K. C. Zhang. 2005. Ethanol fermentation by an acid-tolerant Zymomonas mobilis under nonsterilized condition. Process Biochem. 40: 183-187. https://doi.org/10.1016/j.procbio.2003.11.054
  30. Thanonkeo, P., P. Laopaiboon, K. Sootsuwan, and M. Yamada. 2007. Magnesium ions improve growth and ethanol production of Zymomonas mobilis under heat or ethanol stress. Biotechnology 6: 112-119. https://doi.org/10.3923/biotech.2007.112.119
  31. van Voorst, F., J. Houghton-Larsen, L. Jonson, M. C. Kielland- Brandt, and A. Brandt. 2006. Genome-wide identification of genes required for growth of Saccharomyces cerevisiae under ethanol stress. Yeast 23: 351-359. https://doi.org/10.1002/yea.1359
  32. Vijayakumar, S. R., M. G. Kirchhof, C. L. Patten, and H. E. Schellhorn. 2004. RpoS-regulated genes of Escherichia coli identified by random lacZ fusion mutagenesis. J. Bacteriol. 186: 8499-8507. https://doi.org/10.1128/JB.186.24.8499-8507.2004
  33. Vujicic-Zagar, A., R. Dulermo, M. Le Gorrec, F. Vannier, P. Servant, S. Sommer, A. de Groot, and L. Serre. 2009. Crystal structure of the IrrE protein, a central regulator of DNA damage repair in Deinococcaceae. J. Mol. Biol. 386: 704-716. https://doi.org/10.1016/j.jmb.2008.12.062
  34. Weber, A., S. A. Kogl, and K. Jung. 2006. Time-dependent proteome alterations under osmotic stress during aerobic and anaerobic growth in Escherichia coli. J. Bacteriol. 188: 7165-7175. https://doi.org/10.1128/JB.00508-06
  35. Weber, H., T. Polen, J. Heuveling, V. F. Wendisch, and R. Hengge. 2005. Genome-wide analysis of the general stress response network in Escherichia coli: SigmaS-dependent genes, promoters, and sigma factor selectivity. J. Bacteriol. 187: 1591-1603. https://doi.org/10.1128/JB.187.5.1591-1603.2005
  36. Young, J. J., C. J. Svenson, E. L. Joachimsthal, and P. L. Rogers. 2002. Kinetic analysis of ethanol production by an acetate-resistant strain of recombinant Zymomonas mobilis. Biotechnology Letters 24: 819-824. https://doi.org/10.1023/A:1015546521000

피인용 문헌

  1. Laboratory-Evolved Mutants of an Exogenous Global Regulator, IrrE from Deinococcus radiodurans , Enhance Stress Tolerances of Escherichia coli vol.6, pp.1, 2011, https://doi.org/10.1371/journal.pone.0016228
  2. Oxidative Stress Resistance inDeinococcus radiodurans vol.75, pp.1, 2010, https://doi.org/10.1128/mmbr.00015-10
  3. Global regulator engineering significantly improved Escherichia coli tolerances toward inhibitors of lignocellulosic hydrolysates vol.109, pp.12, 2010, https://doi.org/10.1002/bit.24574
  4. Sorbitol required for cell growth and ethanol production by Zymomonas mobilis under heat, ethanol, and osmotic stresses vol.6, pp.None, 2010, https://doi.org/10.1186/1754-6834-6-180
  5. Dissecting a complex chemical stress: chemogenomic profiling of plant hydrolysates vol.9, pp.1, 2013, https://doi.org/10.1038/msb.2013.30
  6. Elucidation of Zymomonas mobilis physiology and stress responses by quantitative proteomics and transcriptomics vol.5, pp.None, 2010, https://doi.org/10.3389/fmicb.2014.00246
  7. Improving a recombinant Zymomonas mobilis strain 8b through continuous adaptation on dilute acid pretreated corn stover hydrolysate vol.8, pp.None, 2010, https://doi.org/10.1186/s13068-015-0233-z
  8. Global transcriptional analysis of Escherichia coli expressing IrrE, a regulator from Deinococcus radiodurans, in response to NaCl shock vol.11, pp.4, 2010, https://doi.org/10.1039/c5mb00080g
  9. Improving furfural tolerance of Zymomonas mobilis by rewiring a sigma factor RpoD protein vol.99, pp.12, 2010, https://doi.org/10.1007/s00253-015-6577-2
  10. Adaptive laboratory evolution of ethanologenic Zymomonas mobilis strain tolerant to furfural and acetic acid inhibitors vol.99, pp.13, 2015, https://doi.org/10.1007/s00253-015-6616-z
  11. Ethanol production from Jerusalem artichoke tubers at high temperature by newly isolated thermotolerant inulin-utilizing yeast Kluyveromyces marxianus using consolidated bioprocessing vol.108, pp.1, 2010, https://doi.org/10.1007/s10482-015-0476-5
  12. Expression of PprI from Deinococcus radiodurans Improves Lactic Acid Production and Stress Tolerance in Lactococcus lactis vol.10, pp.11, 2010, https://doi.org/10.1371/journal.pone.0142918
  13. Using global transcription machinery engineering (gTME) to improve ethanol tolerance of Zymomonas mobilis vol.15, pp.None, 2010, https://doi.org/10.1186/s12934-015-0398-y
  14. Microbial processing of fruit and vegetable wastes into potential biocommodities: a review vol.38, pp.1, 2018, https://doi.org/10.1080/07388551.2017.1311295
  15. IrrE Improves Organic Solvent Tolerance and Δ1-Dehydrogenation Productivity of Arthrobacter simplex vol.66, pp.20, 2010, https://doi.org/10.1021/acs.jafc.8b01311
  16. Advances and prospects in metabolic engineering of Zymomonas mobilis vol.50, pp.None, 2018, https://doi.org/10.1016/j.ymben.2018.04.001
  17. Progress and perspective on lignocellulosic hydrolysate inhibitor tolerance improvement in Zymomonas mobilis vol.5, pp.None, 2010, https://doi.org/10.1186/s40643-018-0193-9
  18. New technologies provide more metabolic engineering strategies for bioethanol production in Zymomonas mobilis vol.103, pp.5, 2010, https://doi.org/10.1007/s00253-019-09620-6
  19. Construction of a Robust Sphingomonas sp. Strain for Welan Gum Production via the Expression of Global Transcriptional Regulator IrrE vol.8, pp.None, 2010, https://doi.org/10.3389/fbioe.2020.00674
  20. Impact of hfq and sig E on the tolerance of Zymomonas mobilis ZM4 to furfural and acetic acid stresses vol.15, pp.10, 2020, https://doi.org/10.1371/journal.pone.0240330
  21. Engineering prokaryotic regulator IrrE to enhance stress tolerance in budding yeast vol.13, pp.None, 2010, https://doi.org/10.1186/s13068-020-01833-6
  22. Engineering prokaryotic regulator IrrE to enhance stress tolerance in budding yeast vol.13, pp.None, 2010, https://doi.org/10.1186/s13068-020-01833-6
  23. Improving Biotransformation Efficiency of Arthrobacter simplex by Enhancement of Cell Stress Tolerance and Enzyme Activity vol.69, pp.2, 2010, https://doi.org/10.1021/acs.jafc.0c06592
  24. A cold shock protein promotes high-temperature microbial growth through binding to diverse RNA species vol.7, pp.1, 2021, https://doi.org/10.1038/s41421-021-00246-5