Abstract
Previous results have demonstrated that the silencing of adjacent genes encoding NADPH-dependent furfural oxidoreductases (yqhD dkgA) is responsible for increased furfural tolerance in an E. coli strain EMFR9 [Miller et al., Appl Environ Microbiol 75:4315–4323, 2009]. This gene silencing is now reported to result from the spontaneous insertion of an IS10 into the coding region of yqhC, an upstream gene. YqhC shares homology with transcriptional regulators belonging to the AraC/XylS family and was shown to act as a positive regulator of the adjacent operon encoding YqhD and DkgA. Regulation was demonstrated by constructing a chromosomal deletion of yqhC, a firefly luciferase reporter plasmid for yqhC, and by a direct comparison of furfural resistance and NADPH-dependent furfural reductase activity. Closely related bacteria contain yqhC, yqhD, and dkgA orthologs in the same arrangement as in E. coli LY180. Orthologs of yqhC are also present in more distantly related Gram-negative bacteria. Disruption of yqhC offers a useful approach to increase furfural tolerance in bacteria.
Similar content being viewed by others
References
Almeida JR, Bertilsson M, Gorwa-Grauslund MF, Gorsich S, Liden G (2009) Metabolic effects of furaldehydes and impacts on biotechnological processes. Appl Microbiol Biotechnol 82:625–638
Boopathy R, Bokang H, Daniels L (1993) Biotransformation of furfural and 5-hydroxymethyl furfural by enteric bacteria. J Ind Microbiol 11:147–150
Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97:6640–6645
Gallegos MT, Schleif R, Bairoch A, Hofmann K, Ramos JL (1997) Arac/XylS family of transcriptional regulators. Microbiol Mol Biol Rev 61:393–410
Gama-Castro S, Jimenez-Jacinto V, Peralta-Gil M, Santos-Zavaleta A, Penaloza-Spinola MI, Contreras-Moreira B, Segura-Salazar J, Muniz-Rascado L, Martinez-Flores I, Salgado H, Bonavides-Martinez C, Abreu-Goodger C, Rodriguez-Penagos C, Miranda-Rios J, Morett E, Merino E, Huerta AM, Trevino-Quintanilla L, Collado-Vides J (2008) RegulonDB (version 6.0): gene regulation model of Escherichia coli K-12 beyond transcription, active (experimental) annotated promoters and Textpresso navigation. Nucleic Acids Res 36:D120–D124
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
Guzman LM, Belin D, Carson MJ, Beckwith J (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177:4121–4130
Hahn-Hagerdal B, Galbe M, Gorwa-Grauslund MF, Liden G, Zacchi G (2006) Bio-ethanol—the fuel of tomorrow from the residues of today. Trends Biotechnol 24:549–556
Heer D, Heine D, Sauer U (2009) Resistance of Saccharomyces cerevisiae to high furfural concentration is based on NADPH-dependent reduction by at least two oxireductases. Appl Environ Microbiol. doi:10.1128/AEM.01649-09
Jarboe LR, Grabar TB, Yomano LP, Shanmugan KT, Ingram LO (2007) Development of ethanologenic bacteria. Adv Biochem Eng Biotechnol 108:237–261
Katahira S, Mizuike A, Fukuda H, Kondo A (2006) Ethanol fermentation from lignocellulosic hydrolysate by a recombinant xylose- and cellooligosaccharide-assimilating yeast strain. Appl Microbiol Biotechnol 72:1136–1143
Keseler IM, Bonavides-Martinez C, Collado-Vides J, Gama-Castro S, Gunsalus RP, Johnson DA, Krummenacker M, Nolan LM, Paley S, Paulsen IT, Peralta-Gil M, Santos-Zavaleta A, Shearer AG, Karp PD (2009) EcoCyc: a comprehensive view of Escherichia coli biology. Nucleic Acids Res 37:D464–D470
Ko J, Kim I, Yoo S, Min B, Kim K, Park C (2005) Conversion of methylglyoxal to acetol by Escherichia coli aldo-keto reductases. J Bacteriol 187:5782–5789
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
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
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
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
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
Mosier N, Wyman C, Dale B, Elander R, Lee YY, Holtzapple M, Ladisch M (2005) Features of promising technologies for pretreatment of lignocellulosic biomass. Bioresour Technol 96:673–686
Ohta K, Beall DS, Mejia JP, Shanmugam KT, Ingram LO (1991) Genetic improvement of Escherichia coli for ethanol production: chromosomal integration of Zymomonas mobilis genes encoding pyruvate decarboxylase and alcohol dehydrogenase II. Appl Environ Microbiol 57:893–900
Palmqvist E, Hahn-Hagerdal B (2000) Fermentation of lignocellulosic hydrolysates. II: inhibitors and mechanisms of inhibition. Bioresour Technol 74:25–33
Perez JM, Arenas FA, Pradenas GA, Sandoval JM, Vasquez CC (2008) Escherichia coli YqhD exhibits aldehyde reductase activity and protects from the harmful effect of lipid peroxidation-derived aldehydes. J Biol Chem 283:7346–7353
Um BH, Karim M, Henk L (2003) Effect of sulfuric and phosphoric acid pretreatments on enzymatic hydrolysis of corn stover. Appl Biochem Biotechnol 105–108:115–125
Villegas MEDD, 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
Yum DY, Lee BY, Pan JG (1999) Identification of the yqhE and yafB genes encoding two 2,5-diketo-d-gluconate reductases in Escherichia coli. Appl Environ Microbiol 65:3341–3346
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
Acknowledgments
The authors gratefully acknowledge research support by grants from the US Department of Energy (DE-FG36-08GO88142, DE-FC36-GO17058) and by the Verenium Corporation. This work was facilitated by the EcoCyc database [12].
Author information
Authors and Affiliations
Corresponding author
Additional information
This article is based on a presentation at the 32nd Symposium on Biotechnology for Fuels and Chemicals.
Rights and permissions
About this article
Cite this article
Turner, P.C., Miller, E.N., Jarboe, L.R. et al. 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 (2011). https://doi.org/10.1007/s10295-010-0787-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10295-010-0787-5