Genome-wide mapping of furfural tolerance genes in Escherichia coli

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Glebes, Tirzah Y ^a   Sandoval, Nicholas R ^a   Reeder, Philippa J ^a   Schilling, Katherine D ^a   Zhang, Min ^b   Gill, Ryan T ^a  

^a UCB 450   (United States)

^b NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FURFURAL; LIGNOCELLULOSE;

ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; CONTROLLED STUDY; ESCHERICHIA COLI; FUEL AND FUEL RELATED PHENOMENA; FUEL PRODUCTION; GENE MAPPING; GENE OVEREXPRESSION; GENETIC ENGINEERING; GENETIC PROCEDURES; GROESL GENE; LPCA GENE; MOLECULAR CLONING; MULTISCALE ANALYSIS OF LIBRARY ENRICHMENT; NONHUMAN; PHYSICAL TOLERANCE; PLASMID; STRAIN IMPROVEMENT; THYA GENE;

CHROMOSOME MAPPING; CLONING, MOLECULAR; DNA MUTATIONAL ANALYSIS; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FURALDEHYDE; GENETIC ASSOCIATION STUDIES; HEAT-SHOCK PROTEINS; MUTAGENS;

EID: 84900329142     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087540     Document Type: Article

References (69)

1. Sandoval NR, Kim JY, Glebes TY, Reeder PJ, Aucoin HR, et al. (2012) Strategy for directing combinatorial genome engineering in Escherichia coli. Proc Natl Acad Sci U S A 109: 10540-10545.
2. Woodruff LB, Gill RT (2011) Engineering genomes in multiplex. Curr Opin Biotechnol 22: 576-583.
3. 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: 612-616. (Pubitemid 41724901)
4. Tyo KE, Ajikumar PK, Stephanopoulos G (2009) Stabilized gene duplication enables long-term selection-free heterologous pathway expression. Nat Biotechnol 27: 760-765.
5. Yim H, Haselbeck R, Niu W, Pujol-Baxley C, Burgard A, et al. (2011) Metabolic engineering of Escherichia coli for direct production of 1,4-butanediol. Nat Chem Biol 7: 445-452.
6. Atsumi S, Wu TY, Machado IM, Huang WC, Chen PY, et al. (2010) Evolution, genomic analysis, and reconstruction of isobutanol tolerance in Escherichia coli. Mol Syst Biol 6: 449.
7. Sandoval NR, Mills TY, Zhang M, Gill RT (2011) Elucidating acetate tolerance in E. coli using a genome-wide approach. Metab Eng 13: 214-224.
8. Woodruff LB, Boyle NR, Gill RT (2013) Engineering improved ethanol production in Escherichia coli with a genome-wide approach. Metab Eng.
9. Woodruff LB, Pandhal J, Ow SY, Karimpour-Fard A, Weiss SJ, et al. (2013) Genome-scale identification and characterization of ethanol tolerance genes in Escherichia coli. Metab Eng 15: 124-133.
10. Yomano LP, York SW, Ingram LO (1998) Isolation and characterization of ethanol-tolerant mutants of Escherichia coli KO11 for fuel ethanol production. J Ind Microbiol Biotechnol 20: 132-138. (Pubitemid 28204301)
11. Cho RJ, Fromont-Racine M, Wodicka L, Feierbach B, Stearns T, et al. (1998) Parallel analysis of genetic selections using whole genome oligonucleotide arrays. Proc Natl Acad Sci U S A 95: 3752-3757. (Pubitemid 28173201)
12. 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: 7033-7038. (Pubitemid 34526252)
13. Lynch MD, Warnecke T, Gill RT (2007) SCALEs: multiscale analysis of library enrichment. Nat Methods 4: 87-93. (Pubitemid 46029481)
14. Nicolaou SA, Gaida SM, Papoutsakis ET (2011) Coexisting/Coexpressing Genomic Libraries (CoGeL) identify interactions among distantly located genetic loci for developing complex microbial phenotypes. Nucleic Acids Res 39: e152.
15. Shoemaker DD, Lashkari DA, Morris D, Mittmann M, Davis RW (1996) Quantitative phenotypic analysis of yeast deletion mutants using a highly parallel molecular bar-coding strategy. Nat Genet 14: 450-456. (Pubitemid 26414589)
16. Warner JR, Reeder PJ, Karimpour-Fard A, Woodruff LB, Gill RT (2010) Rapid profiling of a microbial genome using mixtures of barcoded oligonucleotides. Nat Biotechnol 28: 856-862.
17. Skerker JM, Leon D, Price MN, Mar JS, Tarjan DR, et al. (2013) Dissecting a complex chemical stress: chemogenomic profiling of plant hydrolysates. Mol Syst Biol 9: 674.
18. Boyle NR, Gill RT (2012) Tools for genome-wide strain design and construction. Curr Opin Biotechnol 23: 666-671.
19. Alper H, Stephanopoulos G (2007) Global transcription machinery engineering: A new approach for improving cellular phenotype. Metabolic Engineering 9: 258-267. (Pubitemid 46809525)
20. Isaacs FJ, Carr PA, Wang HH, Lajoie MJ, Sterling B, et al. (2011) Precise manipulation of chromosomes in vivo enables genome-wide codon replacement. Science 333: 348-353.
21. Wang HH, Isaacs FJ, Carr PA, Sun ZZ, Xu G, et al. (2009) Programming cells by multiplex genome engineering and accelerated evolution. Nature 460: 894-898.
22. Sandoval NR, Kim JY, Glebes TY, Reeder PJ, Aucoin HR, et al. (2012) Strategy for directing combinatorial genome engineering in Escherichia coli. Proc Natl Acad Sci U S A.
23. Rubin EM (2008) Genomics of cellulosic biofuels. Nature 454: 841-845.
24. 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. (Pubitemid 29406768)
25. Mills TY, Sandoval NR, Gill RT (2009) Cellulosic hydrolysate toxicity and tolerance mechanisms in Escherichia coli. Biotechnol Biofuels 2: 26.
26. Khan QA, Hadi SM (1993) Effect of furfural on plasmid DNA. Biochem Mol Biol Int 29: 1153-1160. (Pubitemid 23174951)
27. Shahabuddin, Rahman A, Hadi SM (1991) Reaction of furfural and methylfurfural with DNA: use of single-strand-specific nucleases. Food Chem Toxicol 29: 719-721.
28. Hadi SM, Shahabuddin, Rehman A (1989) Specificity of the interaction of furfural with DNA. Mutat Res 225: 101-106.
29. 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: 154-164. (Pubitemid 43040038)
30. Miller EN, Jarboe LR, Turner PC, Pharkya P, Yomano LP, et al. (2009) Furfural inhibits growth by limiting sulfur assimilation in ethanologenic Escherichia coli strain LY180. Appl Environ Microbiol 75: 6132-6141.
31. 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: 4346-4352.
32. Miller EN, Jarboe LR, Yomano LP, York SW, Shanmugam KT, et al. (2009) Silencing of NADPH-dependent oxidoreductase genes (yqhD and dkgA) in furfural-resistant ethanologenic Escherichia coli. Appl Environ Microbiol 75: 4315-4323.
33. Wang X, Miller EN, Yomano LP, Zhang X, Shanmugam KT, et al. (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: 5132-5140.
34. Zheng H, Wang X, Yomano LP, Geddes RD, Shanmugam KT, et al. (2013) Improving Escherichia coli FucO for Furfural Tolerance by Saturation Mutagenesis of Individual Amino Acid Positions. Appl Environ Microbiol 79: 3202-3208.
35. Wang X, Miller EN, Yomano LP, Shanmugam KT, Ingram LO (2012) Increased furan tolerance in Escherichia coli due to a cryptic ucpA gene. Appl Environ Microbiol 78: 2452-2455.
36. Wang X, Yomano LP, Lee JY, York SW, Zheng H, et al. (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.
37. Miller EN, Turner PC, Jarboe LR, Ingram LO (2010) Genetic changes that increase 5-hydroxymethyl furfural resistance in ethanol-producing Escherichia coli LY180. Biotechnol Lett 32: 661-667.
38. Allen SA, Clark W, McCaffery JM, Cai Z, Lanctot A, et al. (2010) Furfural induces reactive oxygen species accumulation and cellular damage in Saccharomyces cerevisiae. Biotechnol Biofuels 3: 2.
39. Wang J, Zhang Y, Chen Y, Lin M, Lin Z (2012) Global regulator engineering significantly improved Escherichia coli tolerances toward inhibitors of lignocellulosic hydrolysates. Biotechnol Bioeng 109: 3133-3142.
40. Cooke MS, Evans MD, Dizdaroglu M, Lunec J (2003) Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J 17: 1195-1214. (Pubitemid 36775767)
41. Brynildsen MP, Winkler JA, Spina CS, MacDonald IC, Collins JJ (2013) Potentiating antibacterial activity by predictably enhancing endogenous microbial ROS production. Nat Biotechnol 31: 160-165.
42. Bonomo J, Lynch MD, Warnecke T, Price JV, Gill RT (2008) Genome-scale analysis of anti-metabolite directed strain engineering. Metab Eng 10: 109-120.
43. Gall S, Lynch MD, Sandoval NR, Gill RT (2008) Parallel mapping of genotypes to phenotypes contributing to overall biological fitness. Metab Eng 10: 382-393.
44. Warnecke TE, Lynch MD, Karimpour-Fard A, Lipscomb ML, Handke P, et al. (2010) Rapid dissection of a complex phenotype through genomic-scale mapping of fitness altering genes. Metab Eng 12: 241-250.
45. Warnecke TE, Lynch MD, Karimpour-Fard A, Sandoval N, Gill RT (2008) A genomics approach to improve the analysis and design of strain selections. Metab Eng 10: 154-165.
46. Struble JM, Gill RT (2009) Genome-scale identification method applied to find cryptic aminoglycoside resistance genes in Pseudomonas aeruginosa. PLoS One 4: e6576.
47. 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: e55052.
48. Singh A, Lynch MD, Gill RT (2009) Genes restoring redox balance in fermentation-deficient E. coli NZN111. Metab Eng 11: 347-354.
49. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, et al. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006 0008.
50. 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: 6640-6645. (Pubitemid 30412767)
51. Neidhardt FC, Bloch PL, Smith DF (1974) Culture medium for enterobacteria. J Bacteriol 119: 736-747.
52. Zheng Q, Wang XJ (2008) GOEAST: a web-based software toolkit for Gene Ontology enrichment analysis. Nucleic Acids Res 36: W358-363.
53. 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. (Pubitemid 30647772)
54. Garibyan L, Huang T, Kim M, Wolff E, Nguyen A, et al. (2003) Use of the rpoB gene to determine the specificity of base substitution mutations on the Escherichia coli chromosome. DNA Repair (Amst) 2: 593-608. (Pubitemid 36507127)
55. Singh A, Karimpour-Fard A, Gill RT (2010) Increased mutation frequency in redox-impaired Escherichia coli due to RelA- and RpoS-mediated repression of DNA repair. Appl Environ Microbiol 76: 5463-5470.
56. Zhou K, Zhou L, Lim Q, Zou R, Stephanopoulos G, et al. (2011) Novel reference genes for quantifying transcriptional responses of Escherichia coli to protein overexpression by quantitative PCR. BMC Mol Biol 12: 18.
57. Schnaitman CA, Klena JD (1993) Genetics of lipopolysaccharide biosynthesis in enteric bacteria. Microbiol Rev 57: 655-682. (Pubitemid 23262513)
58. Fralick JA, Burns-Keliher LL (1994) Additive effect of tolC and rfa mutations on the hydrophobic barrier of the outer membrane of Escherichia coli K-12. J Bacteriol 176: 6404-6406. (Pubitemid 24313823)
59. Nikaido H (1976) Outer membrane of Salmonella typhimurium. Transmembrane diffusion of some hydrophobic substances. Biochim Biophys Acta 433: 118-132.
60. Fayet O, Ziegelhoffer T, Georgopoulos C (1989) The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures. J Bacteriol 171: 1379-1385. (Pubitemid 19080775)
61. Kerner MJ, Naylor DJ, Ishihama Y, Maier T, Chang HC, et al. (2005) Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122: 209-220. (Pubitemid 41032985)
62. Gill RT, Cha HJ, Jain A, Rao G, Bentley WE (1998) Generating controlled reducing environments in aerobic recombinant Escherichia coli fermentations: effects on cell growth, oxygen uptake, heat shock protein expression, and in vivo CAT activity. Biotechnol Bioeng 59: 248-259. (Pubitemid 28277751)
63. Yamamori T, Yura T (1980) Temperature-induced synthesis of specific proteins in Escherichia coli: evidence for transcriptional control. J Bacteriol 142: 843-851. (Pubitemid 11230334)
64. Zingaro KA, Terry Papoutsakis E (2013) GroESL overexpression imparts Escherichia coli tolerance to i-, n-, and 2-butanol, 1,2,4-butanetriol and ethanol with complex and unpredictable patterns. Metab Eng 15: 196-205.
65. Zingaro KA, Papoutsakis ET (2012) Toward a semisynthetic stress response system to engineer microbial solvent tolerance. MBio 3.
66. 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 Biotechnol 98-100: 327-340. (Pubitemid 34457432)
67. Tokuriki N, Tawfik DS (2009) Chaperonin overexpression promotes genetic variation and enzyme evolution. Nature 459: 668-673.
68. Khan QA, Shamsi FA, Hadi SM (1995) Mutagenicity of furfural in plasmid DNA. Cancer Lett 89: 95-99.
69. Taylor PL, Blakely KM, de Leon GP, Walker JR, McArthur F, et al. (2008) Structure and function of sedoheptulose-7-phosphate isomerase, a critical enzyme for lipopolysaccharide biosynthesis and a target for antibiotic adjuvants. J Biol Chem 283: 2835-2845.