Improving Escherichia coli fucO for furfural tolerance by saturation mutagenesis of individual amino acid positions

Applied and Environmental Microbiology

Volumn 79, Issue 10, 2013, Pages 3202-3208

  Zheng, Huabao ^a   Wang, Xuan ^a   Yomano, Lorraine P ^a   Geddes, Ryan D ^a   Shanmugam, Keelnatham T ^a   Ingram, Lonnie O ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FREE-ENERGY CALCULATIONS; INCLUSION BODIES; INTERFACIAL REGION; MRNA ABUNDANCES; OXIDOREDUCTASES; SATURATION MUTAGENESIS; SUBSTRATE CONCENTRATIONS; TRANSLATIONAL INITIATION;

ALDEHYDES; AMINO ACIDS; ENZYMES; ESCHERICHIA COLI; GENE ENCODING; GENE EXPRESSION; MUTAGENESIS;

FURFURAL;

ALCOHOL DEHYDROGENASE; BACTERIAL RNA; FURFURAL; LACTALDEHYDE REDUCTASE; LEUCINE; MESSENGER RNA;

AMINO ACID; AROMATIC HYDROCARBON; BACTERIOLOGY; CELLULOSE; CONCENTRATION (COMPOSITION); ENZYME ACTIVITY; FECAL COLIFORM; FERMENTATION; GENE EXPRESSION; GENETIC ENGINEERING; MUTATION; POLLUTION TOLERANCE; SATURATION;

ADAPTATION; ARTICLE; BACTERIAL GENE; DRUG EFFECT; ENZYME ACTIVATION; ENZYMOLOGY; ESCHERICHIA COLI; FERMENTATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MICROBIAL SENSITIVITY TEST; MUTATION; PROTEIN MULTIMERIZATION; RNA FOLDING; SITE DIRECTED MUTAGENESIS;

ADAPTATION, BIOLOGICAL; ALCOHOL OXIDOREDUCTASES; ENZYME ACTIVATION; ESCHERICHIA COLI; FERMENTATION; FURALDEHYDE; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENES, BACTERIAL; LEUCINE; MICROBIAL SENSITIVITY TESTS; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTEIN MULTIMERIZATION; RNA FOLDING; RNA, BACTERIAL; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 84877154575     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00149-13     Document Type: Article

References (41)

1. Boronat A, Aguilar J. 1979. Rhamnose-induced propanediol oxidoreductase in Escherichia coli: purification, properties, and comparison with the fucose-induced enzyme. J. Bacteriol. 140:320 -326.
2. Chen YM, Lin ECC. 1984. Dual control of a common L-1,2-propanediol oxidoreductase by L-fucose and L-rhamnose in Escherichia coli. J. Bacteriol. 157:828-832.
3. Zhu Y, Lin ECC. 1989. L-1,2-Propanediol exits more rapidly than L-lactaldehyde from Escherichia coli. J. Bacteriol. 171:862- 867.
4. Montella C, Bellsolell L, Perez-Luque R, Badia J, Baldoma L, Coll M, Aguilar J. 2005. Crystal structure of an iron-dependent group III dehydrogenase that interconverts L-lactaldehyde and L-1,2-propanediol in Escherichia coli. J. Bacteriol. 187:4957- 4966.
5. Blikstad C, Widersten M. 2010. Functional characterization of a stereospecific diol dehydrogenase, FucO, from Escherichia coli: substrate specificity, pH dependence, kinetic isotope effects and influence of solvent viscosity. J. Mol. Catal. B Enzym. 66:148 -155.
6. Wang X, Miller EN, Yomano LP, Zhang X, Shanmugam KT, Ingram LO. 2011. Increased furfural tolerance due to overexpression of NADHdependent oxidoreductase FucO in Escherichia coli strains engineered for the production of ethanol and lactate. Appl. Environ. Microbiol. 77:5132- 5140.
7. Mills TY, Sandoval NR, Gill RT. 2009. Cellulosic hydrolysate toxicity and tolerance mechanisms in Escherichia coli. Biotechnol. Biofuels 2:11. doi:10.1186/1754-6834-2-11.
8. Parawira W, Tekere M. 2011. Biotechnological strategies to overcome inhibitors in lignocellulose hydrolysates for ethanol production: review. Crit. Rev. Biotechnol. 31:20 -31.
9. Zheng HB, Wang X, Yomano LP, Shanmugam KT, Ingram LO. 2012. Increase in furfural tolerance in ethanologenic Escherichia coli LY180 by plasmid-based expression of thyA. Appl. Environ. Microbiol. 78:4346- 4352.
10. Geddes CC, Nieves IU, Ingram LO. 2011. Advances in ethanol production. Curr. Opin. Biotechnol. 22:312-319.
11. Martinez A, Rodriguez ME, Wells ML, York SW, Preston JF, Ingram LO. 2001. Detoxification of dilute acid hydrolysates of lignocellulose with lime. Biotechnol. Prog. 17:287-293.
12. 2 treatments ("overliming") on the composition and toxicity of bagasse hemicellulose hydrolysates. Biotechnol. Bioeng. 69: 526-536.
13. Zaldivar J, Martinez A, Ingram LO. 1999. Effect of selected aldehydes on the growth and fermentation of ethanologenic Escherichia coli. Biotechnol. Bioeng. 65:24 -33.
14. Mayer C, Boos W. 29 March 2005, posting date. Chapter 3.4.1, Hexose/ pentose and hexitol/pentitol metabolism. In Böck A (ed), EcoSal---Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, DC. http://www.ecosal.org.
15. Miller EN, Jarboe LR, Yomano LP, York SW, Shanmugam KT, Ingram LO. 2009. Silencing of NADPH-dependent oxidoreductase genes (yqhD and dkgA) in furfural-resistant ethanologenic Escherichia coli. Appl. Environ. Microbiol. 75:4315- 4323.
16. Wang X, Yomano LP, Lee JY, York SW, Zheng HB, Mullinnix MT, Shanmugam KT, Ingram LO. 2013. Engineering furfural tolerance in Escherichia coli improves the fermentation of lignocellulosic sugars into renewable chemicals. Proc. Natl. Acad. Sci. U. S. A. 110:4021- 4026.
17. Martinez A, Grabar TB, Shanmugam KT, Yomano LP, York SW, Ingram LO. 2007. Low salt medium for lactate and ethanol production by recombinant Escherichia coli B. Biotechnol. Lett. 29:397- 404.
18. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
19. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, Olson AJ. 2009. Autodock4 and AutoDockTools4: automated docking with selective receptor flexibility. J. Comput. Chem. 30:2785-2791.
20. Martinez A, Rodriguez ME, York SW, Preston JF, Ingram LO. 2000. Use of UV absorbance to monitor furans in dilute acid hydrolysates of biomass. Biotechnol. Prog. 16:637- 641.
21. Cabiscol E, Hidalgo E, Badia J, Baldoma L, Ros JQ, Aguilar J. 1990. Oxygen regulation of L-1,2-propanediol oxidoreductase activity in Escherichia coli. J. Bacteriol. 172:5514 -5515.
22. Su Y, Rhee MS, Ingram LO, Shanmugam KT. 2011. Physiological and fermentation properties of Bacillus coagulans and a mutant lacking fermentative lactate dehydrogenase activity. J. Ind. Microbiol. Biotechnol. 38:441- 450.
23. Wang QZ, Ingram LO, Shanmugam KT. 2011. Evolution of D-lactate dehydrogenase activity from glycerol dehydrogenase and its utility for D-lactate production from lignocellulose. Proc. Natl. Acad. Sci. U. S. A. 108:18920 -18925.
24. Kudla G, Murray AW, Tollervey D, Plotkin JB. 2009. Coding-sequence determinants of gene expression in Escherichia coli. Science 324:255-258.
25. Miller EN, Jarboe LR, Turner PC, Pharkya P, Yomano LP, York SW, Nunn D, Shanmugam KT, Ingram LO. 2009. Furfural inhibits growth by limiting sulfur assimilation in ethanologenic Escherichia coli strain LY180. Appl. Environ. Microbiol. 75:6132- 6141.
26. Jia M, Li Y. 2005. The Relationship among gene expression, folding free energy and codon usage bias in Escherichia coli. FEBS Lett. 579:5333-5337.
27. Tsao D, Shabalina SA, Gauthier J, Dokholyan NV, Diatchenko L. 2011. DisruptivemRNAfolding increases translational efficiency of catechol-Omethyltransferase variant. Nucleic Acids Res. 39:6201- 6212.
28. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31:3406 -3415.
29. Labrou NE. 2010. Random mutagenesis methods for in vitro directed enzyme evolution. Curr. Protein Pept. Sci. 11:91-100.
30. Jarboe LR. 2011. YqhD: a broad-substrate range aldehyde reductase with various applications in production of biorenewable fuels and chemicals. Appl. Microbiol. Biotechnol. 89:249 -257.
31. Sulzenbacher G, Alvarez K, van den Heuvel RHH, Versluis C, Spinelli M, Campanacci V, Valencia C, Cambillau C, Eklund H, Tegoni M. 2004. Crystal structure of E. coli alcohol dehydrogenase YqhD: evidence of a covalently modified NADP coenzyme. J. Mol. Biol. 342:489 -502.
32. Conway T, Ingram LO. 1989. Similarity of Escherichia coli propanediol oxidoreductase (fucO product) and an unusual alcohol dehydrogenase from Zymomonas mobilis and Saccharomyces cerevisiae. J. Bacteriol. 171:3754-3759.
33. Turner PC, Miller EN, Jarboe LR, Baggett CL, Shanmugam KT, Ingram LO. 2011. YqhC regulates transcription of the adjacent Escherichia coli genes yqhD and dkgA that are involved in furfural tolerance. J. Ind. Microbiol. Biotechnol. 38:431- 439.
34. Kim Y, Ingram LO, Shanmugam KT. 2008. Dihydrolipoamide dehydrogenase mutation alters the NADH sensitivity of pyruvate dehydrogenase complex of Escherichia coli K-12. J. Bacteriol. 190:3851-3858.
35. Reetz MT. 2011. Laboratory evolution of stereoselective enzymes: a prolific source of catalysts for asymmetric reactions. Angew. Chem. Int. Ed. Engl. 50:138 -174.
36. Wang M, Si T, Zhao HM. 2012. Biocatalyst development by directed evolution. Bioresour. Technol. 115:117-125.
37. Chen SH, Hwang DR, Chen GH, Hsu NS, Wu YT, Li TL, Wong CH. 2012. Engineering transaldolase in Pichia stipitis to improve bioethanol production. ACS Chem. Biol. 7:481- 486.
38. Lee S-M, Jellison T, Alper HS. 2012. Directed evolution of xylose isomerase for improved xylose catabolism and fermentation in the yeast Saccharomyces cerevisiae. Appl. Environ. Microbiol. 78:5708 -5716.
39. Chundawat SPS, Vismeh R, Sharma LN, Humpula JF, Sousa LD, Chambliss CK, Jones AD, Balan V, Dale BE. 2010. Multifaceted characterization of cell wall decomposition products formed during ammonia fiber expansion (AFEX) and dilute acid based pretreatments. Bioresour. Technol. 101:8429-8438.
40. Reid MF, Fewson CA. 1994. Molecular characterization of microbial alcohol dehydrogenases. Crit. Rev. Microbiol. 20:13-56.
41. Roodveldt C, Aharoni A, Tawfik DS. 2005. Directed evolution of proteins for heterologous expression and stability. Curr. Opin. Struct. Biol. 15:50 -56.