Comparison of genome-wide selection strategies to identify furfural tolerance genes in Escherichia coli

Biotechnology and Bioengineering

Volumn 112, Issue 1, 2015, Pages 129-140

  Glebes, Tirzah Y ^a   Sandoval, Nicholas R ^a   Gillis, Jacob H ^a   Gill, Ryan T ^a  

^a University of Colorado at Boulder   (United States)

Author keywords

Biofuels; Directed evolution; Furfural; Metabolic engineering

Indexed keywords

ALDEHYDES; BIOFUELS; DNA; ESCHERICHIA COLI; FURFURAL; GENE EXPRESSION; METABOLIC ENGINEERING;

CHEMICAL INHIBITORS; COMPLEX PHENOTYPE; DIRECTED EVOLUTION; GENETIC CHANGES; GENOMIC LIBRARIES; GROWTH SELECTION; OVER-EXPRESSION; RENEWABLE SOURCES;

GENES;

BACTERIAL DNA; FURFURAL; GENOMIC DNA; OXIDOREDUCTASE; PANCREATIC RIBONUCLEASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; BIOFUEL;

ALLELE; ARTICLE; BACTERIAL GENETICS; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL STRAIN; BIOSYNTHESIS; CELL STRESS; CLONE; CLOSTRIDIUM BEIJERINCKII; COMPARATIVE STUDY; DEGRADATION; ESCHERICHIA COLI; GENE DOSAGE; GENE EXPRESSION; GENE LIBRARY; GENE MUTATION; GENETIC SELECTION; GENETIC VARIABILITY; GLYCOLYSIS; NONHUMAN; OPERON; PENTOSE PHOSPHATE CYCLE; PH; PLASMID; POPULATION DYNAMICS; PROMOTER REGION; PYRIMIDINE SYNTHESIS; STARVATION; TRANSLATION INITIATION; DIRECTED MOLECULAR EVOLUTION; GENETICS; METABOLIC ENGINEERING; METABOLISM; PHYSIOLOGY; PROCEDURES;

ESCHERICHIA COLI;

BIOFUELS; DIRECTED MOLECULAR EVOLUTION; ESCHERICHIA COLI; FURALDEHYDE; GENOME, BACTERIAL; METABOLIC ENGINEERING;

EID: 84911988986     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.25325     Document Type: Article

References (65)

1. Allen SA, Clark W, McCaffery JM, Cai Z, Lanctot A, Slininger PJ, Liu ZL, Gorsich SW. 2010. Furfural induces reactive oxygen species accumulation and cellular damage in Saccharomyces cerevisiae. Biotechnol Biofuels 3:2.
2. Alper H, Miyaoku K, Stephanopoulos G. 2005. Construction of lycopene-overproducing E. coli strains by combining systematic and combinatorial gene knockout targets. Nat biotechnol 23(5):612-616.
3. Alper H, Stephanopoulos G. 2007. Global transcription machinery engineering: A new approach for improving cellular phenotype. Metab Eng 9(3):258-267.
4. Ask M, Mapelli V, Hock H, Olsson L, Bettiga M. 2013. Engineering glutathione biosynthesis of Saccharomyces cerevisiae increases robustness to inhibitors in pretreated lignocellulosic materials. Microbial cell factories 12:87.
5. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: The Keio collection. Mol Syst Biol 2:20060008.
6. Barrick JE, Lenski RE. 2013. Genome dynamics during experimental evolution. Nat Rev Genet 14(12):827-839.
7. Bartlett DH, Frantz BB, Matsumura P. 1988. Flagellar transcriptional activators FlbB and FlaI: Gene sequences and 5' consensus sequences of operons under FlbB and FlaI control. J Bacteriol 170(4):1575-1581.
8. Bejar S, Bouche JP. 1985. A new dispensable genetic locus of the terminus region involved in control of cell division in Escherichia coli. Mol Gen Genet: MGG 201(2):146-150.
9. Bonomo J, Lynch MD, Warnecke T, Price JV, Gill RT. 2008. Genome-scale analysis of anti-metabolite directed strain engineering. Metabol Eng 10(2):109-120.
10. Burnell JN. 2010. Cloning and characterization of Escherichia coli DUF299: A bifunctional ADP-dependent kinase-Pi-dependent pyrophosphorylase from bacteria. BMC Biochem 11:1.
11. Cho RJ, Fromont-Racine M, Wodicka L, Feierbach B, Stearns T, Legrain P, Lockhart DJ, Davis RW. 1998. Parallel analysis of genetic selections using whole genome oligonucleotide arrays. Proc Natl Acad Sci U S A 95(7):3752-3757.
12. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97(12):6640-6645.
13. Delgenes JH, Moletta R, JM N. 1996. Effects of lignocellulose degradation products on ethanol fermentations of glucose and xylose by Saccharomyces cerevisiae, Zymomonas mobilis, Pichia stipitis, and Candida shehatae. Enzyme Microbial Tech 19(3):220-225.
14. Diaz D, Villa P, Guerra M, Rodriguez E, Redondo D, Martinez A. 1992. Conversion of furfural into furfuryl alcohol by Saccharomyces cerevisiae 354. Acta Biotechnol 12:351-354.
15. Dunlop MJ, Dossani ZY, Szmidt HL, Chu HC, Lee TS, Keasling JD, Hadi MZ, Mukhopadhyay A. 2011. Engineering microbial biofuel tolerance and export using efflux pumps. Mol Syst Biol 7:487.
16. Franden MA, Pilath HM, Mohagheghi A, Pienkos PT, Zhang M. 2013. Inhibition of growth of Zymomonas mobilis by model compounds found in lignocellulosic hydrolysates. Biotech Biofuels 6(1):99.
17. Gall S, Lynch MD, Sandoval NR, Gill RT. 2008. Parallel mapping of genotypes to phenotypes contributing to overall biological fitness. Metabol Eng 10(6):382-393.
18. Gill RT, Wildt S, Yang YT, Ziesman S, Stephanopoulos G. 2002. Genome-wide screening for trait conferring genes using DNA microarrays. Proc Natl Acad Sci U S A 99(10):7033-7038.
19. Glebes TY, Sandoval NR, Reeder PJ, Schilling KD, Zhang M, Gill RT. 2014. Genome-wide mapping of furfural tolerance genes in Escherichia coli. PLoS One 9(1):e87540.
20. Goodarzi H, Bennett BD, Amini S, Reaves ML, Hottes AK, Rabinowitz JD, Tavazoie S. 2010. Regulatory and metabolic rewiring during laboratory evolution of ethanol tolerance in E. coli. Mol Syst Biol 6:378.
21. Gutierrez T, Buszko ML, Ingram LO, Preston JF. 2002. Reduction of furfural to furfuryl alcohol by ethanologenic strains of bacteria and its effect on ethanol production from xylose. Appl Biochem Biotech 98-100:327-340.
22. Gutierrez T, Ingram LO, Preston JF. 2006. Purification and characterization of a furfural reductase (FFR) from Escherichia coli strain LYO1-an enzyme important in the detoxification of furfural during ethanol production. J Biotechnol 121(2):154-164.
23. Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA. 2013. RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotech 31(3):233-239.
24. Johnson JE, Lackner LL, de Boer PA. 2002. Targeting of (D)MinC/MinD and (D)MinC/DicB complexes to septal rings in Escherichia coli suggests a multistep mechanism for MinC-mediated destruction of nascent FtsZ rings. J Bacteriol 184(11):2951-2962.
25. Kaplan R, Apirion D. 1975. The fate of ribosomes in Escherichia coli cells starved for a carbon source. J Biol Chem 250(5):1854-1863.
26. Khan QA, Shamsi FA, Hadi SM. 1995. Mutagenicity of furfural in plasmid DNA. Cancer letters 89(1):95-99.
27. Kim D, Hahn JS. 2013. Roles of the Yap1 transcription factor and antioxidants in Saccharomyces cerevisiae's tolerance to furfural and 5-hydroxymethylfurfural, which function as thiol-reactive electrophiles generating oxidative stress. Appl Environ Microbiol 79(16):5069-5077.
28. Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, Toyonaga H, Mori H. 2005. Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): Unique resources for biological research. DNA Res 12(5):291-299.
29. Liu R, Ochman H. 2007. Origins of flagellar gene operons and secondary flagellar systems. J Bacteriol 189(19):7098-7104.
30. Lutz R, Bujard H. 1997. Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Res 25(6):1203-1210.
31. Lynch MD, Warnecke T, Gill RT. 2007. SCALEs: Multiscale analysis of library enrichment. Nat Methods 4(1):87-93.
32. Marisch K, Bayer K, Scharl T, Mairhofer J, Krempl PM, Hummel K, Razzazi-Fazeli E, Striedner G. 2013. A comparative analysis of industrial Escherichia coli K-12 and B strains in high-glucose batch cultivations on process-, transcriptome- and proteome level. PLoS One 8(8):e70516.
33. Marschall C, Labrousse V, Kreimer M, Weichart D, Kolb A, Hengge-Aronis R. 1998. Molecular analysis of the regulation of csiD, a carbon starvation-inducible gene in Escherichia coli that is exclusively dependent on sigma s and requires activation by cAMP-CRP. J Mol Biol 276(2):339-353.
34. Miller EN, Jarboe LR, Turner PC, Pharkya P, Yomano LP, York SW, Nunn D, Shanmugam KT, Ingram LO. 2009a. Furfural inhibits growth by limiting sulfur assimilation in ethanologenic Escherichia coli strain LY180. Appl Environ Microbiol 75(19):6132-6141.
35. Miller EN, Jarboe LR, Yomano LP, York SW, Shanmugam KT, Ingram LO. 2009b. Silencing of NADPH-dependent oxidoreductase genes (yqhD and dkgA) in furfural-resistant ethanologenic Escherichia coli. Appl Environ Microbiol 75(13):4315-4323.
36. Mills TY, Sandoval NR, Gill RT. 2009. Cellulosic hydrolysate toxicity and tolerance mechanisms in Escherichia coli. Biotech biofuels 2:26.
37. Neidhardt FC, Bloch PL, Smith DF. 1974. Culture medium for enterobacteria. J Bacteriol 119(3):736-747.
38. Pesavento C, Becker G, Sommerfeldt N, Possling A, Tschowri N, Mehlis A, Hengge R. 2008. Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli. Genes Dev 22(17):2434-2446.
39. Salis HM. 2011. The ribosome binding site calculator. Methods Enzymol 498:19-42.
40. Salis HM, Mirsky EA, Voigt CA. 2009. Automated design of synthetic ribosome binding sites to control protein expression. Nat Biotech 27(10):946-950.
41. Sandoval NR, Kim JY, Glebes TY, Reeder PJ, Aucoin HR, Warner JR, Gill RT. 2012. Strategy for directing combinatorial genome engineering in Escherichia coli. Proc Natl Acad Sci U S A 109(26):10540-10545.
42. Sandoval NR, Mills TY, Zhang M, Gill RT. 2011. Elucidating acetate tolerance in E. coli using a genome-wide approach. Metabol Eng 13(2):214-224.
43. Seaver LC, Imlay JA. 2001. Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol 183(24):7173-7181.
44. Singh A, Lynch MD, Gill RT. 2009. Genes restoring redox balance in fermentation-deficient E. coli NZN111. Metabol Eng 11(6):347-354.
45. Skerker JM, Leon D, Price MN, Mar JS, Tarjan DR, Wetmore KM, Deutschbauer AM, Baumohl JK, Bauer S, Ibanez AB, et al. 2013. Dissecting a complex chemical stress: Chemogenomic profiling of plant hydrolysates. Mol Syst Biol 9:674.
46. Spindler EC, Boyle NR, Hancock RE, Gill RT. 2013. Genome-wide identification of genes conferring energy related resistance to a synthetic antimicrobial Peptide (bac8c). PLoS One 8(1):e55052.
47. 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 Biotech 38(3):431-439.
48. 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(7257):894-898.
49. Wang HH, Kim H, Cong L, Jeong J, Bang D, Church GM. 2012a. Genome-scale promoter engineering by coselection MAGE. Nat Methods 9(6):591-593.
50. Wang J, Zhang Y, Chen Y, Lin M, Lin Z. 2012b. Global regulator engineering significantly improved Escherichia coli tolerances toward inhibitors of lignocellulosic hydrolysates. Biotech Bioeng 109(12):3133-3142.
51. Wang X, Miller EN, Yomano LP, Shanmugam KT, Ingram LO. 2012c. Increased furan tolerance in Escherichia coli due to a cryptic ucpA gene. Appl Environ Microbiol 78(7):2452-2455.
52. Wang X, Miller EN, Yomano LP, Zhang X, Shanmugam KT, Ingram LO. 2011. Increased furfural tolerance due to overexpression of NADH-dependent oxidoreductase FucO in Escherichia coli strains engineered for the production of ethanol and lactate. Appl Environ Microbiol 77(15):5132-5140.
53. Wang X, Yomano LP, Lee JY, York SW, Zheng H, 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(10):4021-4026.
54. Warnecke TE, Lynch MD, Karimpour-Fard A, Lipscomb ML, Handke P, Mills T, Ramey CJ, Hoang T, Gill RT. 2010. Rapid dissection of a complex phenotype through genomic-scale mapping of fitness altering genes. Metabol Eng 12(3):241-250.
55. Warnecke TE, Lynch MD, Karimpour-Fard A, Sandoval N, Gill RT. 2008. A genomics approach to improve the analysis and design of strain selections. Metabol Eng 10(3-4):154-165.
56. Warner JR, Reeder PJ, Karimpour-Fard A, Woodruff LB, Gill RT. 2010. Rapid profiling of a microbial genome using mixtures of barcoded oligonucleotides. Nat Biotech 28(8):856-862.
57. White RJ, Pasternak CA. 1967. The purification and properties of N-acetylglucosamine 6-phosphate deacetylase from Escherichia coli. Biochem J 105(1):121-125.
58. Woodruff LB, Boyle NR, Gill RT. 2013a. Engineering improved ethanol production in Escherichia coli with a genome-wide approach. Metabol Eng
59. Woodruff LB, Pandhal J, Ow SY, Karimpour-Fard A, Weiss SJ, Wright PC, Gill RT. 2013b. Genome-scale identification and characterization of ethanol tolerance genes in Escherichia coli. Metabol Eng 15:124-133.
60. Zaldivar J, Martinez A, Ingram LO. 1999. Effect of selected aldehydes on the growth and fermentation of ethanologenic Escherichia coli. Biotech Bioeng 65(1):24-33.
61. Zhang Y, Ezeji TC. 2013. Transcriptional analysis of Clostridium beijerinckii NCIMB 8052 to elucidate role of furfural stress during acetone butanol ethanol fermentation. Biotechn Biofuels 6(1):66.
62. Zheng H, Wang X, Yomano LP, Geddes RD, Shanmugam KT, Ingram LO. 2013. Improving Escherichia coli fuco for furfural tolerance by saturation mutagenesis of individual amino acid positions. Appl Environ Microbiol 79(10):3202-3208.
63. Zheng H, 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(12):4346-4352.
64. Zheng Q, Wang XJ. 2008. GOEAST: A web-based software toolkit for Gene Ontology enrichment analysis. Nucleic Acids Res 36: (Web Server issue): W358-363.
65. Zhou K, Zhou L, Lim Q, Zou R, Stephanopoulos G, Too HP. 2011. Novel reference genes for quantifying transcriptional responses of Escherichia coli to protein overexpression by quantitative PCR. BMC Mol Biol 12:18.