Skip to main content
SpringerLink
Log in

Determinants of tolerance to inhibitors in hardwood spent sulfite liquor in genome shuffled Pachysolen tannophilus strains

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Genome shuffling was used to obtain Pachysolen tannophilus mutants with improved tolerance to inhibitors in hardwood spent sulfite liquor (HW SSL). Genome shuffled strains (GHW301, GHW302 and GHW303) grew at higher concentrations of HW SSL (80 % v/v) compared to the HW SSL UV mutant (70 % v/v) and the wild-type (WT) strain (50 % v/v). In defined media containing acetic acid (0.70–0.90 % w/v), GHW301, GHW302 and GHW303 exhibited a shorter lag compared to the acetic acid UV mutant, while the WT did not grow. Genome shuffled strains produced more ethanol than the WT at higher concentrations of HW SSL and an aspen hydrolysate. To identify the genetic basis of inhibitor tolerance, whole genome sequencing was carried out on GHW301, GHW302 and GHW303 and compared to the WT strain. Sixty single nucleotide variations were identified that were common to all three genome shuffled strains. Of these, 40 were in gene sequences and 20 were within 5 bp–1 kb either up or downstream of protein encoding genes. Based on the mutated gene products, mutations were grouped into functional categories and affected a variety of cellular functions, demonstrating the complexity of inhibitor tolerance in yeast. Sequence analysis of UV mutants (UAA302 and UHW303) from which GHW301, GHW302 and GHW303 were derived, confirmed the success of our cross-mating based genome shuffling strategy. Whole-genome sequencing analysis allowed identification of potential gene targets for tolerance to inhibitors in lignocellulosic hydrolysates.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aasland R, Gibson TJ, Stewart AF (1995) The PHD finger: implications for chromatin mediated transcriptional regulation. Trends Biochem Sci 20:56–59

    Article  CAS  PubMed  Google Scholar 

  • 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 3:2–11

    Article  PubMed Central  PubMed  Google Scholar 

  • Almeida B, Ohlmeier S, Almeida AJ, Madeo F, Leao C, Rodrigues F, Ludovico P (2009) Yeast protein expression profile during acetic acid-induced apoptosis indicates causal involvement of the TOR pathway. Proteomics 9:720–732

    Article  CAS  PubMed  Google Scholar 

  • Andre B (1995) An overview of membrane transport proteins in Saccharomyces cerevisiae. Yeast 11:1575–1611

    Article  CAS  PubMed  Google Scholar 

  • Ask M, Bettiga M, Duraiswamy VR, Olsson L (2013) Pulsed addition of HMF and furfural to batch-grown xylose-utilizing Saccharomyces cerevisiae results in different physiological responses in glucose and xylose consumption phase. Biotechnol Biofuels 6:181–195

    Article  PubMed Central  PubMed  Google Scholar 

  • Ask M, Bettiga M, Mapelli V, Olsson L (2013) The influence of HMF and furfural on redox-balance and energy-state of xylose-utilizing Saccharomyces cerevisiae. Biotechnol Biofuels 6:22–27

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bajwa PK, Shireen T, D’Aoust F, Pinel D, Martin VJJ, Trevors JT, Lee H (2009) Mutants of the pentose-fermenting yeast Pichia stipitis with improved tolerance to inhibitors in hardwood spent sulfite liquor. Biotechnol Bioeng 104:892–900

    Article  CAS  PubMed  Google Scholar 

  • Bajwa PK, Pinel D, Martin VJJ, Trevors JT, Lee H (2010) Strain improvement of the pentose-fermenting yeast Pichia stipitis by genome shuffling. J Microbiol Methods 81:179–186

    Article  CAS  PubMed  Google Scholar 

  • Bajwa PK, Phaenark C, Grant N, Zhang X, Paice M, Martin VJJ, Trevors JT, Lee H (2011) Ethanol production from selected lignocellulosic hydrolysates by genome shuffled strains of Scheffersomyces stipitis. Bioresour Technol 102:9965–9969

    Article  CAS  PubMed  Google Scholar 

  • Bajwa PK, Harner NK, Richardson TL, Sindu S, Habash MB, Trevors JT, Lee H (2013) Genome shuffling protocol for the pentose-fermenting yeast Scheffersomyces stipitis. In: Gupta VK, Tuohy MG, Ayyachamy M, Turner KM, O’Donovan A (eds) Laboratory protocols in fungal biology: current methods in fungal biology. Springer, New York, pp 447–454

    Chapter  Google Scholar 

  • Bajwa PK, Ho CY, Chan CK, Martin VJJ, Trevors JT, Lee H (2013) Transcriptional profiling of Saccharomyces cerevisiae T2 cells upon exposure to hardwood spent sulphite liquor: comparison to acetic acid, furfural and hydroxymethylfurfural. Antonie Van Leeuwenhoek 103:1281–1295

    Article  CAS  PubMed  Google Scholar 

  • Barbosa MDS, Lee H, Collins-Thompson DL (1990) Additive effects of alcohols, their acidic by-products, and temperature on the yeast Pachysolen tannophilus. Appl Environ Microbiol 56:545–550

    PubMed Central  CAS  Google Scholar 

  • Barbosa MDS, Lee H, Schneider H, Forsberg CW (1990) Temperature mediated changes of D-xylose metabolism in the yeast Pachysolen tannophilus. FEMS Microbiol Lett 72:35–40

    Article  CAS  Google Scholar 

  • Bauer BE, Rossington D, Mollapour M, Mamnun Y, Kuchler K, Piper PW (2003) Weak organic acid stress inhibits aromatic amino acid uptake by yeast, causing a strong influence of amino acid auxotrophies on the phenotypes of membrane transporter mutants. Eur J Biochem 270:3189–3195

    Article  CAS  PubMed  Google Scholar 

  • Bicho PA, Runnals PL, Cunningham JD, Lee H (1988) Induction of xylose reductase and xylitol dehydrogenase activities in Pachysolen tannophilus and Pichia stipitis on mixed sugars. Appl Environ Microbiol 54:50–54

    PubMed Central  CAS  PubMed  Google Scholar 

  • Biot-Pelletier D, Martin VJJ (2014) Evolutionary engineering by genome shuffling. Appl Microbiol Biotechnol 98:3877–3887

    Article  CAS  PubMed  Google Scholar 

  • Bose S, Dutko JA, Zitomer RS (2005) Genetic factors that regulate the attenuation of the general stress response of yeast. Genetics 169:1215–1226

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Choi Y, Sims GE, Murphy S, Miller JR, Chan AP (2012) Predicting the functional effect of amino acid substitutions and indels. PLoS One 7:1–13

    Google Scholar 

  • Clark T, Wedlock N, James AP, Deverell K, Thornton RJ (1986) Strain improvement of xylose-fermenting yeast Pachysolen tannophilus by hybridization of two mutant strains. Biotechnol Lett 8:801–806

    Article  CAS  Google Scholar 

  • Davierwala AP, Haynes J, Li ZJ, Brost RL, Robinson MD, Yu L, Mnaimneh S, Ding HM, Zhu HW, Chen YQ, Cheng X, Brown GW, Boone C, Andrews BJ, Hughes TR (2005) The synthetic genetic interaction spectrum of essential genes. Nat Genet 37:1147–1152

    Article  CAS  PubMed  Google Scholar 

  • Delley PA, Hall MN (1999) Cell wall stress depolarizes cell growth via hyperactivation of RHO1. J Cell Biol 147:163–174

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dinh TN, Nagahisa K, Yoshikawa K, Hirasawa T, Furusawa C, Shimizu H (2009) Analysis of adaptation to high ethanol concentration in Saccharomyces cerevisiae using DNA microarray. Bioprocess Biosyst Eng 32:681–688

    Article  CAS  PubMed  Google Scholar 

  • Dunlop MJ (2011) Engineering microbes for tolerance to next-generation biofuels. Biotechnol Biofuels 4:32–40

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Furukawa K, Kitano H, Mizoguchi H, Hara S (2004) Effect of cellular inositol content on ethanol tolerance of Saccharomyces cerevisiae in sake brewing. J Biosci Bioeng 98:107–113

    Article  CAS  PubMed  Google Scholar 

  • Gaber RF, Kielland-Brandt MC, Fink GR (1990) HOL1 mutations confer novel ion transport in Saccharomyces cerevisiae. Mol Cell Biol 10:643–652

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gandhi M, Goode BL (2008) Coronin: the double-edged sword of actin dynamics. Subcell Biochem 48:72–87

    Article  PubMed  Google Scholar 

  • Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241–4257

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Giudici P, Solieri L, Pulvirenti AM, Cassanelli S (2005) Strategies and perspectives for genetic improvement of wine yeasts. Appl Microbiol Biotechnol 66:622–628

    Article  CAS  PubMed  Google Scholar 

  • Gorsich SW, Dien BS, Nichols NN, Slininger PJ, Liu ZL, Skory CD (2006) Tolerance to furfural-induced stress is associated with pentose phosphate pathway genes ZWF1, GND1, RPE1, and TKL1 in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 71:339–349

    Article  CAS  PubMed  Google Scholar 

  • Gorsich SW, Slininger PJ, McCaffery JM (2006b) The fermentation inhibitor furfural causes cellular damage to Saccharomyces cerevisiae. In: Biotechnology for fuels and chemical symposium proceedings, Paper no. 4–17

  • Hao XC, Yang XS, Wan P, Tian S (2013) Comparative proteomic analysis of a new adaptive Pichia stipitis strain to furfural, a lignocellulosic inhibitory compound. Biotechnol Biofuels 6:34–42

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Harner NK, Bajwa PK, Habash MB, Trevors JT, Austin GD, Lee H (2014) Mutants of the pentose-fermenting yeast Pachysolen tannophilus tolerant to hardwood spent sulfite liquor and acetic acid. Antonie Van Leeuwenhoek 105:29–43

    Article  CAS  PubMed  Google Scholar 

  • Harner NK, Wen X, Bajwa PK, Austin GD, Ho CY, Habash MB, Trevors JT, Lee H (2015) Genetic improvement of native xylose-fermenting yeasts for ethanol production. J Ind Microbiol Biotechnol 42:1–20

    Article  CAS  PubMed  Google Scholar 

  • Hashikawa N, Mizukami Y, Imazu H, Sakurai H (2006) Mutated yeast heat shock transcription factor activates transcription independently of hyperphosphorylation. J Biol Chem 281:3936–3942

    Article  CAS  PubMed  Google Scholar 

  • James AP, Zahab DM (1982) A genetic system for Pachysolen tannophilus, a pentose-fermenting yeast. J Gen Microbiol 128:2297–2301

    Google Scholar 

  • James AP, Zahab DM (1983) The construction and genetic analysis of polyploids and aneuploids of the pentose-fermenting yeast, Pachysolen tannophilus. J Gen Microbiol 129:2489–2494

    Google Scholar 

  • Jeffries TW (1984) Mutants of Pachysolen tannophilus showing enhanced rates of growth and ethanol formation from d-xylose. Enzyme Microb Technol 6:254–258

    Article  CAS  Google Scholar 

  • Jiang H, Xie YQ, Houston P, Stemkehale K, Mortensen UH, Rothstein R, Kodadek T (1996) Direct association between the yeast Rad51 and Rad54 recombination proteins. J Biol Chem 271:33181–33186

    Article  CAS  PubMed  Google Scholar 

  • Kim DR, Gidvani RD, Ingalls BP, Duncker BP, McConkey BJ (2011) Differential chromatin proteomics of the MMS-induced DNA damage response in yeast. Proteome Sci 9:62–75

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kim HS, Kim NR, Kim W, Choi W (2012) Insertion of transposon in the vicinity of SSK2 confers enhanced tolerance to furfural in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 95:531–540

    Article  CAS  PubMed  Google Scholar 

  • Krogan NJ, Cagney G, Yu HY, Zhong GQ, Guo XH, Ignatchenko A, Li J, Pu SY, Datta N, Tikuisis AP, Punna T, Peregrin-Alvarez JM, Shales M, Zhang X, Davey M, Robinson MD, Paccanaro A, Bray JE, Sheung A, Beattie B, Richards DP, Canadien V, Lalev A, Mena F, Wong P, Starostine A, Canete MM, Vlasblom J, Wu S, Orsi C, Collins SR, Chandran S, Haw R, Rilstone JJ, Gandi K, Thompson NJ, Musso G, St Onge P, Ghanny S, Lam MHY, Butland G, Altaf-Ui AM, Kanaya S, Shilatifard A, O’Shea E, Weissman JS, Ingles CJ, Hughes TR, Parkinson J, Gerstein M, Wodak SJ, Emili A, Greenblatt JF (2006) Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440:637–643

    Article  CAS  PubMed  Google Scholar 

  • Künzler M, Trueheart J, Sette C, Hurt E, Thorner J (2001) Mutations in the YRB1 gene encoding yeast Ran-binding-protein-1 that impair nucleocytoplasmic transport and suppress yeast mating defects. Genetics 157:1089–1105

    PubMed Central  PubMed  Google Scholar 

  • Kuranda MJ, Robbins PW (1991) Chitinase is required for cell separation during growth of Saccharomyces cerevisiae. J Biol Chem 266:19758–19767

    CAS  PubMed  Google Scholar 

  • Larsson S, Palmqvist E, Hahn-Hagerdal B, Tengborg C, Stenberg K, Zacchi G, Nilvebrant NO (1999) The generation of fermentation inhibitors during dilute acid hydrolysis of softwood. Enzyme Microb Technol 24:151–159

    Article  CAS  Google Scholar 

  • Lee H, James AP, Zahab DM, Mahmourides G, Maleszka R, Schneider H (1986) Mutants of Pachysolen tannophilus with improved production of ethanol D-xylose. Appl Environ Microbiol 51:1252–1258

    PubMed Central  CAS  PubMed  Google Scholar 

  • Li BZ, Yuan YJ (2010) Transcriptome shifts in response to furfural and acetic acid in Saccharomyces cerevisiae. Appl Microbiol Boitechnol 86:1915–1924

    Article  CAS  Google Scholar 

  • Ligthelm ME, Prior BA, du Preez JC, Brandt V (1988) An investigation of D-{1-13C} xylose metabolism in Pichia stipitis under aerobic and anaerobic conditions. Appl Microbiol Biotechnol 28:293–296

    Article  CAS  Google Scholar 

  • Lin FM, Qiao B, Yuan YJ (2009) Comparative proteomic analysis of tolerance and adaptation of ethanologenic Saccharomyces cerevisiae to furfural, a lignocellulosic inhibitory compound. Appl Environ Microbiol 75:3765–3776

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lindberg L, Santos AXS, Riezman H, Olsson L, Bettiga M (2013) Lipidomic profiling of Saccharomyces cerevisiae and Zygosaccharomyces bailii reveals critical changes in lipid composition in response to acetic acid stress. PLoS One 8:1–12

    Google Scholar 

  • Liu ZL (2011) Molecular mechanisms of yeast tolerance and in situ detoxification of lignocellulose hydrolysates. Appl Microbiol Biotechnol 90:809–825

    Article  CAS  PubMed  Google Scholar 

  • Liu ZL, Slininger PJ (2006) Transcriptome dynamics of ethanologenic yeast in response to 5-hydroxymethylfurfural stress related to biomass conversion to ethanol. In: Mendez-Vilas A (ed) Modern multidisciplinary applied microbiology: exploiting microbes and their interactions. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, pp 679–684

  • Liu ZL, Ma MG, Song MZ (2009) Evolutionarily engineered ethanologenic yeast detoxifies lignocellulosic biomass conversion inhibitors by reprogrammed pathways. Mol Genet Genomics 282:233–244

    Article  PubMed Central  PubMed  Google Scholar 

  • Liu XY, Kaas RS, Jensen PR, Workman M (2012) Draft genome sequence of the yeast Pachysolen tannophilus CBS 4044/NRRL Y-2460. Eukaryot Cell 11:827

    Article  PubMed Central  PubMed  Google Scholar 

  • Lohmeier-Vogel EM, Sopher CR, Lee H (1998) Intracellular acidification as a mechanism for the inhibition by acid hydrolysis-derived inhibitors of xylose fermentation by yeasts. J Ind Microbiol Biotechnol 20:75–81

    Article  CAS  Google Scholar 

  • Ma MG, Liu LZ (2010) Quantitative transcription dynamic analysis reveals candidate genes and key regulators for ethanol tolerance in Saccharomyces cerevisiae. BMC Microbiol 10:169–188

    Article  PubMed Central  PubMed  Google Scholar 

  • Ma MG, Liu ZL (2010) Comparative transcriptome profiling analyses during the lag phase uncover YAP1, PDR1, PDR3, RPN4, and HSF1 as key regulatory genes in genomic adaptation to the lignocellulose derived inhibitor HMF for Saccharomyces cerevisiae. BMC Genomics 11:660–678

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • MacPherson S, Larochelle M, Turcotte B (2006) A fungal family of transcriptional regulators: the zinc cluster proteins. Microbiol Mol Biol Rev 70:583–604

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Maleszka R, Schneider H (1982) Concurrent production and consumption of ethanol by cultures of Pahcysolen tannophilus growing on d-xylose. Appl Environ Microbiol 44:909–912

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mira NP, Becker JD, Sá-Correia I (2010) Genomic expression program involving the Haa1p-regulon in Saccharomyces cerevisiae response to acetic acid. OMICS 14:587–601

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mira NP, Palma M, Guerreiro JF, Sá-Correia I (2010) Genome-wide identification of Saccharomyces cerevisiae genes required for tolerance to acetic acid. Microb Cell Fact 9:79–91

    Article  PubMed Central  PubMed  Google Scholar 

  • Moran GR (2005) 4-hydroxyphenylpyruvate dioxygenase. Arch Biochem Biophys 433:117–128

    Article  CAS  PubMed  Google Scholar 

  • Nygard Y, Mojzita D, Toivari M, Penttila M, Wiebe MG, Ruohonen L (2014) The diverse role of Pdr12 in resistance to weak organic acids. Yeast 31:219–232

    Article  CAS  PubMed  Google Scholar 

  • Oud B, van Maris AJA, Daran JM, Pronk JT (2012) Genome-wide analytical approaches for reverse metabolic engineering of industrially relevant phenotypes in yeast. FEMS Yeast Res 12:183–196

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Oud B, Guadalupe-Medina V, Nijkamp JF, de Ridder D, Pronk JT, van Maris AJA, Daran JM (2013) Genome duplication and mutations in ACE2 cause multicellular, fast-sedimenting phenotypes in evolved Saccharomyces cerevisiae. Proc Natl Acad Sci USA 110:4223–4231

    Article  Google Scholar 

  • Patnaik R, Louie S, Gavrilovic V, Perry K, Stemmer WPC, Ryan CM, del Cardayre S (2002) Genome shuffling of Lactobacillus for improved acid tolerance. Nat Biotechnol 20:707–712

    Article  CAS  PubMed  Google Scholar 

  • Pinel D, D’Aoust F, del Cardayre SB, Bajwa PK, Lee H, Martin VJJ (2011) Saccharomyces cerevisiae genome shuffling through recursive population mating leads to improved tolerance to spent sulfite liquor. Appl Environ Microbiol 77:4736–4743

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pinel D, Colatriano D, Jiang H, Lee H, Martin VJJ (2015) Deconstructing the genetic basis of spent sulfite liquor tolerance using deep sequencing of genome shuffled yeast. Biotech Biofuels 8:53. doi:10.1186/s13068-015-0241-z

    Article  Google Scholar 

  • Piper P, Mahe Y, Thompson S, Pandjaitan R, Holyoak C, Egner R, Muhlbauer M, Coote P, Kuchler K (1998) The Pdr12 ABC transporter is required for the development of weak organic acid resistance in yeast. EMBO J 17:4257–4265

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Quan XX, Tsoulos P, Kuritzky A, Zhang R, Stochaj U (2006) The carrier Msn5p/Kap142p promotes nuclear export of the hsp70 Ssa4p and relocates in response to stress. Mol Microbiol 62:592–609

    Article  CAS  PubMed  Google Scholar 

  • Rastogi RP, Kumar A, Tyagi MB, Sinha RP (2010) Molecular mechanisms of ultraviolet radiation-induced DNA damage and repair. J Nucleic Acids 2010:1–32

    Article  Google Scholar 

  • Reinhold R, Kruger V, Meinecke M, Schulz C, Schmidt B, Grunau SD, Guiard B, Wiedemann N, van der Laan M, Wagner R, Rehling P, Dudek J (2012) The channel-forming Sym1 protein is transported by the TIM23 complex in a presequence-independent manner. Mol Cell Biol 32:5009–5021

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Richardson TL, Harner NK, Bajwa PK, Trevors JT, Lee H (2011) Approaches to deal with toxic inhibitors during fermentation of lignocellulosic substrates. In: Zhu JJY, Zhang X, Pan XJ (eds) Sustainable production of fuels, chemicals, and fibers from forest biomass. ACS Symposium Series; American Chemical Society, Washington, pp 171–202

    Chapter  Google Scholar 

  • Sá-Correia I, dos Santos SC, Teixeira MC, Cabrito TR, Mira NP (2009) Drug: H+ antiporters in chemical stress response in yeast. Trends Microbiol 17:22–31

    Article  PubMed  Google Scholar 

  • Saavedra CA, Hammell CM, Heath CV, Cole CN (1997) Yeast heat shock mRNAs are exported through a distinct pathway defined by Rip1p. Genes Dev 11:2845–2856

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sasano Y, Watanabe D, Ukibe K, Inai T, Ohtsu I, Shimoi H, Takagi H (2012) Overexpression of the yeast transcription activator Msn2 confers furfural resistance and increases the initial fermentation rate in ethanol production. J Biosci Bioeng 113:451–455

    Article  CAS  PubMed  Google Scholar 

  • Schauer A, Knauer H, Ruckenstuhl C, Fussi H, Durchschlag M, Potocnik U, Frohlich KU (2009) Vacuolar functions determine the mode of cell death. Biochem Biophys Acta 1793:540–545

    Article  CAS  PubMed  Google Scholar 

  • Schneider H, Wang PY, Chan YK, Maleszka R (1981) Conversion of d-xylose into ethanol by the yeast Pachysolen tannophilus. Biotechnol Lett 3:82–92

    Article  Google Scholar 

  • Slininger PJ, Bothast RJ, Van Cauwenberge JE, Kurtzman CP (1982) Conversion of d-xylose to ethanol by the yeast Pachysolen tannophilus. Biotechnol Bioeng 24:371–384

    Article  CAS  PubMed  Google Scholar 

  • Sugiyama M, Akase SP, Nakanishi R, Horie H, Kaneko Y, Harashima S (2014) Nuclear localization of Haa1, which is linked to its phosphorylation status, mediates lactic acid tolerance in Saccharomyces cerevisiae. Appl Environ Microbiol 80:3488–3495

    Article  PubMed Central  PubMed  Google Scholar 

  • Takahashi T, Shimoi H, Ito K (2001) Identification of genes required for growth under ethanol stress using transposon mutagenesis in Saccharomyces cerevisiae. Mol Genet Genomics 265:1112–1119

    Article  CAS  PubMed  Google Scholar 

  • Tanaka K, Ishii Y, Ogawa J, Shima J (2012) Enhancement of acetic acid tolerance in Saccharomyces cerevisiae by overexpression of the HAA1 gene, encoding a transcriptional activator. Appl Environ Microbiol 78:8161–8163

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Theander O (1991) Chemical analysis of lignocellulose materials. Anim Feed Sci Technol 32:35–44

    Article  CAS  Google Scholar 

  • Trott A, Morano KA (2004) SYM1 is the stress-induced Saccharomyces cerevisiae ortholog of the mammalian kidney disease gene Mpv17 and is required for ethanol metabolism and tolerance during heat shock. Eukaryot Cell 3:620–631

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Warner JR (1999) The economics of ribosome biosynthesis in yeast. Trends Biochem Sci 24:437–440

    Article  CAS  PubMed  Google Scholar 

  • Webb SR, Lee H (1990) Regulation of d-xylose utilization by hexoses in pentose-fermenting yeasts. Biotechnol Adv 8:685–697

    Article  CAS  PubMed  Google Scholar 

  • Wright MB, Howell EA, Gaber RF (1996) Amino acid substitutions in membrane-spanning domains of Hol1, a member of the major facilitator superfamily of transporters, confer nonselective cation uptake in Saccharomyces cerevisiae. J Bacteriol 178:7197–7205

    PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the NSERC Bioconversion Network and BioFuelNet. We thank Cletus Kurtzman (USDA ARS, Peoria, IL, USA) for providing P. t annophilus NRRL Y-2460, Frank Giust (Tembec Inc., Témiscaming, QC, Canada) for providing the HW SSL and Mike Rushton (formerly of Lignol, Burnaby, BC, Canada) for providing the aspen hydrolysate.

Author information

Author notes

  1. Glen D. Austin

    Present address: AB Mauri, St. Louis, MO, 63110, USA

Authors and Affiliations

  1. School of Environmental Sciences, University of Guelph, Guelph, ON, N1G 2W1, Canada

    Nicole K. Harner, Paramjit K. Bajwa, Philip A. Formusa, Marc B. Habash, Jack T. Trevors & Hung Lee

  2. BP Biofuels, San Diego, CA, 92121, USA

    Glen D. Austin

  3. Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, ON, M5G 1X5, Canada

    Chi-Kin Chan & Chi-Yip Ho

Authors
  1. Nicole K. Harner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paramjit K. Bajwa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Philip A. Formusa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Glen D. Austin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marc B. Habash
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jack T. Trevors
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Chi-Kin Chan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Chi-Yip Ho
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hung Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hung Lee.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (docx 58 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Harner, N.K., Bajwa, P.K., Formusa, P.A. et al. Determinants of tolerance to inhibitors in hardwood spent sulfite liquor in genome shuffled Pachysolen tannophilus strains. Antonie van Leeuwenhoek 108, 811–834 (2015). https://doi.org/10.1007/s10482-015-0537-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-015-0537-9

Keywords

Search

Navigation