Abstract
Renewable lignocellulosic materials are attractive low-cost feedstocks for bioethanol production. Furfural and 5-hydroxymethylfurfural (HMF) are among the most potent inhibitory compounds generated from acid hydrolysis of lignocelluloses to simple sugars for fermentation. In Saccharomyces cerevisiae ATCC 211239 and NRRL Y-12632 and Pichia stipitis NRRL Y-7124, furfural and HMF inhibition were determined to be dose-dependent at concentrations from 10 to 120 mM. The yeast strains were more sensitive to inhibition by furfural than HMF at the same concentration, while combined treatment of furfural and HMF synergistically suppressed cell growth. A metabolite transformed from HMF by strain NRRL Y-12632 was isolated from the culture supernatant, and conclusively identified as 2,5-bis-hydroxymethylfuran, a previously postulated HMF alcohol, with a composition of C6H8O3 and a molecular weight of 128. It is proposed that, in the presence of HMF, the yeast reduces the aldehyde group on the furan ring of HMF into an alcohol, in a similar manner as for furfural. The accumulation of this biotransformed metabolite may be less toxic to yeast cultures than HMF, as evidenced by the rapid yeast fermentation and growth rates associated with HMF conversion. The ability of yeasts to adapt to and transform furfural and HMF offers the potential for in situ detoxification of these inhibitors and suggests a genetic basis for further development of highly tolerant strains for biofuel production.
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References
Boopathy R, Bokang H, Daniels L (1993) Biotransformation of furfural and 5-hydroxymethyl furfural by enteric bacteria. J Ind Microbiol 11:147–150
Hahn-Hagerdal B, Wahlbom CF, Gardony M, Van Zyl WH, Otero RRC, Jonsson LJ (2001) Metabolic engineering of Saccharomyces cerevisiae for xylose utilization. Adv Biochem Eng Biotechnol 73:53–84
Ho NWY, Chen Z, Brainard AP (1998) Genetically engineered Saccharomyces yeast capable of effective cofermentation of glucose and xylose. Appl Environ Microbiol 64:1852–1859
Jeffries TW, Shi N-Q (1999) Genetic engineering for improved fermentation by yeasts. Adv Biochem Eng Biotechnol 65:117–161
Kang SS, Okada H (1973) Alcohol dehydrogenase of Cephalosporium sp. induced by furfural alcohol. J Ferment Technol 51:118–124
Khan QA, Hadi SM (1994) Inactivation and repair of bacteriophage lambda by furfural. Biochem Mol Biol Int 32:379–385
Larsson S, Palmqvist E, Hahn-Hagerdal B, Tengborg C, Stenberg K, Zacchi G, Nilvebrant N-O (1999) The generation of inhibitors during dilute acid hydrolysis of softwood. Enzyme Microb Technol 24:151–159
Lewkowski J (2001) Synthesis, chemistry and applications of 5-hydroxymethylfurfural and its derivatives. Arkivoc 1:17–54
Martin C, Jonsson LJ (2003) Comparison of the resistance of industrial and laboratory strains of Saccharomyces and Zygosaccharomyces to lignocellulose-derived fermentation inhibitors. Enzyme Microb Technol 32:386–395
Modig T, Liden G, Taherzadeh MJ (2002) Inhibition effects of furfural on alcohol dehydrogenase, aldehyde dehydrogenase and pyruvate dehydrogenase. Biochem J 363:769–776
Morimoto S, Murakami M (1967) Studies on fermentation products from aldehyde by microorganisms: the fermentative production of furfural alcohol from furfural by yeasts (part I). J Ferment Technol 45:442–446
Morimoto S, Hirashima T, Ohashi M (1968) Studies on fermentation products from aldehyde by microorganisms: the fermentative production of furfural alcohol from furfural by yeasts (part II). J Ferment Technol 46:276–287
Nemirovskii VD, Kostenko VG (1991) Transformation of yeast growth inhibitors which occurs during biochemical processing of wood hydrolysates. Gidroliz Lesokhimm Prom-st 1:16–17
Nemirovskii VG, Gusarova LA, Rakhmilevich YaD, Sizov AI, Kostenko VG (1989) Furfural and hydroxymethylfurfural transformation route during culturing of nutrient yeasts. Biotekhnologiya 5:285–289
Ostergaard S, Olsson L, Nielsen J (2000) Metabolic engineering of Saccharomyces cerevisiae. Microbiol Mol Bio Rev 64:34–50
Palmqvist E, Almeida JS, Hahn-Hagerdal B (1999) Influence of furfural on anaerobic glycolytic kinetics of Saccharomyces cerevisiae in batch culture. Biotechnol Bioeng 62:447–454
Sanchez B, Bautista J (1988) Effects of furfural and 5-hydroxymethylfurfrual on the fermentation of Saccharomyces cerevisiae and biomass production from Candida guilliermondii. Enzyme Microb Technol 10:315–318
Schiavo V, Descotes G, Mentech J (1991) Catalytic hydrogenation of 5-hydroxymethylfurfural in aqueous medium. Bull Soc Chim Fr 128:704–711
Sherman F (2002) Getting started with yeast. In: Guthrie C, Fink GR (eds) Guide to yeast genetics and molecular biology. Academic, San Diego, pp 3–41
Taherzadeh MJ, Eklund R, Gustafsson L, Niklasson D, Liden G (1997) Characterization and fermentation of dilute-acid hydrolyzates from wood. Ind Eng Chem Res 36:4659–4665
Taherzadeh MJ, Gustafsson L, Niklasson C (2000) Physiological effects of 5-hydroxymethylfurfural on Saccharomyces cerevisiae. Appl Micorbiol Biotechnol 53:701–708
Wickerham LJ (1951) Taxonomy of Yeast. Tech Bull No 1029 US Dept Agric, Washington
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We thank Elena Terentieva for translation of Russian literature and are grateful for the technical assistance of Maureen Shea-Andersh, Patricia J. O’Bryan, Sandra M. Duval, and David Weisleder.
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Liu, Z.L., Slininger, P.J., Dien, B.S. et al. Adaptive response of yeasts to furfural and 5-hydroxymethylfurfural and new chemical evidence for HMF conversion to 2,5-bis-hydroxymethylfuran. J IND MICROBIOL BIOTECHNOL 31, 345–352 (2004). https://doi.org/10.1007/s10295-004-0148-3
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DOI: https://doi.org/10.1007/s10295-004-0148-3