Skip to main content
SpringerLink
Log in

Genome-wide screening of Saccharomyces cerevisiae genes required to foster tolerance towards industrial wheat straw hydrolysates

  • Bioenergy/Biofuels/Biochemicals
  • Published:
Journal of Industrial Microbiology & Biotechnology

Abstract

The presence of toxic compounds derived from biomass pre-treatment in fermentation media represents an important drawback in second-generation bio-ethanol production technology and overcoming this inhibitory effect is one of the fundamental challenges to its industrial production. The aim of this study was to systematically identify, in industrial medium and at a genomic scale, the Saccharomyces cerevisiae genes required for simultaneous and maximal tolerance to key inhibitors of lignocellulosic fermentations. Based on the screening of EUROSCARF haploid mutant collection, 242 and 216 determinants of tolerance to inhibitory compounds present in industrial wheat straw hydrolysate (WSH) and in inhibitor-supplemented synthetic hydrolysate were identified, respectively. Genes associated to vitamin metabolism, mitochondrial and peroxisomal functions, ribosome biogenesis and microtubule biogenesis and dynamics are among the newly found determinants of WSH resistance. Moreover, PRS3, VMA8, ERG2, RAV1 and RPB4 were confirmed as key genes on yeast tolerance and fermentation of industrial WSH.

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

Similar content being viewed by others

References

  1. Almario MP, Reyes LH, Kao KC (2013) Evolutionary engineering of Saccharomyces cerevisiae for enhanced tolerance to hydrolysates of lignocellulosic biomass. Biotechnol Bioeng. doi:10.1002/bit.24938

    PubMed  Google Scholar 

  2. Almeida JR, Modig T, Petersson A, Hähn-Hägerdal B, Lidén G, Gorwa-Grauslund MF (2007) Increased tolerance and conversion of inhibitors in lignocellulosic hydrolysates by Saccharomyces cerevisiae. J Chem Technol Biotechnol 82:340–349. doi:10.1002/jctb.1676

    Article  CAS  Google Scholar 

  3. 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. doi:10.1186/1754-6834-6-22

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. Ayer A, Sanwald J, Pillay BA, Meyer AJ, Perrone GG, Dawes IW (2013) Distinct Redox Regulation in Sub-Cellular Compartments in Response to Various Stress Conditions in Saccharomyces cerevisiae. PLoS ONE 8:e65240. doi:10.1371/journal.pone.0065240

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Bajwa PK, Ho CY, Chan CK, Martin VJ, 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. doi:10.1007/s10482-013-9909-1

    Article  CAS  PubMed  Google Scholar 

  6. Dos Santos SC, Teixeira MC, Cabrito TR, Sa-Correia I (2013) Yeast toxicogenomics: genome-wide responses to chemical stresses with impact in environmental health, pharmacology, and biotechnology. Front Genet 3:63. doi:10.3389/fgene.2012.00063

    Google Scholar 

  7. Dunlop MJ (2011) Engineering microbes for tolerance to next-generation biofuels. Biotechnol Biofuels 4:32. doi:10.1186/1754-6834-4-32

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Endo A, Nakamura T, Ando A, Tokuyasu K, Shima J (2008) Genome-wide screening of the genes required for tolerance to vanillin, which is a potential inhibitor of bioethanol fermentation, in Saccharomyces cerevisiae. Biotechnol Biofuels. doi:10.1186/1754-6834-1-3

    Google Scholar 

  9. 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. doi:10.1007/s00253-005-0142-3

    Article  CAS  PubMed  Google Scholar 

  10. Heer D, Sauer U (2008) Identification of furfural as a key toxin in lignocellulosic hydrolysates and evolution of a tolerant yeast strain. Microbial Biotechnol 1:497–506. doi:10.1111/j.1751-7915.2008.00050.x

    Article  CAS  Google Scholar 

  11. Huang RL, Su RX, Qi W, He ZM (2011) Bioconversion of lignocellulose into bioethanol: process intensification and mechanism research. Bioenergy Res 4:225–245. doi:10.1007/s12155-011-9125-7

    Article  Google Scholar 

  12. Li BZ, Yuan YJ (2010) Transcriptome shifts in response to furfural and acetic acid in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 86:1915–1924. doi:10.1007/s00253-010-2518-2

    Article  CAS  PubMed  Google Scholar 

  13. Li M, Petteys BJ, McClure JM, Valsakumar V, Bekiranov S, Frank EL, Smith JS (2010) Thiamine biosynthesis in Saccharomyces cerevisiae is regulated by the NAD + -dependent histone deacetylase Hst1. Mol Cell Biol 30:3329–3341. doi:10.1128/MCB.01590-09

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. 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. doi:10.1128/AEM.02594-08

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Liu ZL (2011) Molecular mechanisms of yeast tolerance and in situ detoxification of lignocellulose hydrolysates. Appl Microbiol Biotechnol 90:809–825. doi:10.1007/s00253-011-3167-9

    Article  CAS  PubMed  Google Scholar 

  16. Liu ZL (2006) Genomic adaptation of ethanologenic yeast to biomass conversion inhibitors. Appl Microbiol Biotechnol 73:27–36. doi:10.1007/s00253-006-0567-3

    Article  CAS  PubMed  Google Scholar 

  17. Liu ZL, Ma M, Song M (2009) Evolutionarily engineered ethanologenic yeast detoxifies lignocellulosic biomass conversion inhibitors by reprogrammed pathways. Mol Genet Genomics 282:233–244. doi:10.1007/s00438-009-0461-7

    Article  PubMed Central  PubMed  Google Scholar 

  18. Ma M, Liu LZ (2010) Quantitative transcription dynamic analysis reveals candidate genes and key regulators for ethanol tolerance in Saccharomyces cerevisiae. BMC Microbiol 10:169. doi:10.1186/1471-2180-10-169

    Article  PubMed Central  PubMed  Google Scholar 

  19. Madhavan A, Srivastava A, Kondo A, Bisaria VS (2012) Bioconversion of lignocellulose-derived sugars to ethanol by engineered Saccharomyces cerevisiae. Crit Rev Biotechnol 32:2–48. doi:10.3109/07388551.2010.539551

    Article  Google Scholar 

  20. Mira NP, Becker JD, Sa-Correia I (2010) Genomic expression program involving the Haa1p-regulon in Saccharomyces cerevisiae response to acetic acid. OMICS 14:587–601. doi:10.1089/omi.2010.0048

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Mira NP, Palma M, Guerreiro JF, Sa-Correia I (2010) Genome-wide identification of Saccharomyces cerevisiae genes required for tolerance to acetic acid. Microb Cell Fact 9:79. doi:10.1186/1475-2859-9-79

    Article  PubMed Central  PubMed  Google Scholar 

  22. Mira NP, Teixeira MC, Sá-Correia I (2010) Adaptative response and tolerance to weak acid stress in Saccharomyces cerevisiae: a genome-wide view. OMICS 14:525–540. doi:10.1089/omi.2010.0072

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Modig T, Almeida JR, Gorwa-Grauslund MF, Liden G (2008) Variability of the response of Saccharomyces cerevisiae strains to lignocellulose hydrolysate. Biotechnol Bioeng 100:423–429. doi:10.1002/bit.21789

    Article  CAS  PubMed  Google Scholar 

  24. Modig T, Liden G, Taherzadeh MJ (2002) Inhibition effects of furfural on alcohol dehydrogenase, aldehyde dehydrogenase and pyruvate dehydrogenase. Biochem J 363:769–776

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Mroczek S, Kufel J (2008) Apoptotic signals induce specific degradation of ribosomal RNA in yeast. Nucleic Acids Res 36:2874–2888. doi:10.1093/nar/gkm1100

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Mussatto SI, Dragone G, Guimaraes PM, Silva JP, Carneiro LM, Roberto IC, Vicente A, Domingues L, Teixeira JA (2000) Technological trends, global market, and challenges of bio-ethanol production. Biotechnol Adv 28:817–830. doi:10.1016/j.biotechadv.2010.07.001

    Article  Google Scholar 

  27. Palmqvist E, Hahn-Hagerdal B (2000) Fermentation of lignocellulosic hydrolysates. I: inhibition and detoxification. Bioress Technol 74:17–24. doi:10.1016/S0960-8524(99)00160-1

    Article  CAS  Google Scholar 

  28. Pereira FB, Gomes DG, Guimaraes PM, Teixeira JA, Domingues L (2011) Cell recycling during repeated very high gravity bio-ethanol fermentations using the industrial Saccharomyces cerevisiae strain PE-2. Biotechnol Lett 34:45–53. doi:10.1007/s10529-011-0735-0

    Article  PubMed  Google Scholar 

  29. Pereira FB, Guimaraes PM, Teixeira JA, Domingues L (2011) Robust industrial Saccharomyces cerevisiae strains for very high gravity bio-ethanol fermentations. J Biosci Bioeng 112:130–136. doi:10.1016/j.jbiosc.2011.03.022

    Article  CAS  PubMed  Google Scholar 

  30. Pereira FB, Guimaraes PM, Gomes DG, Mira NP, Teixeira MC, Sa-Correia I, Domingues L (2011) Identification of candidate genes for yeast engineering to improve bioethanol production in very high gravity and lignocellulosic biomass industrial fermentations. Biotechnol Biofuels 4:57. doi:10.1186/1754-6834-4-57

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Ruiz HA, Ruzene DS, Silva DP, da Silva FF, Vicente AA, Teixeira JA (2011) Development and characterization of an environmentally friendly process sequence (autohydrolysis and organosolv) for wheat straw delignification. Appl Biochem Biotechnol 164:629–641. doi:10.1007/s12010-011-9163-9

    Article  CAS  PubMed  Google Scholar 

  32. Siegers K, Waldmann T, Leroux MR, Grein K, Shevchenko A, Schiebel E, Hartl FU (1999) Compartmentation of protein folding in vivo: sequestration of non-native polypeptide by the chaperonin–GimC system. EMBO J 18:75–84. doi:10.1093/emboj/18.1.75

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Taylor MP, Mulako I, Tuffin M, Cowan D (2012) Understanding physiological responses to pre-treatment inhibitors in ethanologenic fermentations. Biotechnol J 7:1169–1181. doi:10.1002/biot.201100335

    Article  CAS  PubMed  Google Scholar 

  34. Teixeira MC, Raposo LR, Mira NP, Lourenco AB, Sa-Correia I (2009) Genome-wide identification of Saccharomyces cerevisiae genes required for maximal tolerance to ethanol. Appl Environ Microbiol 75:5761–5772. doi:10.1128/AEM.00845-09

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Teixeira MC, Raposo LR, Palma M, Sa-Correia I (2010) Identification of genes required for maximal tolerance to high-glucose concentrations, as those present in industrial alcoholic fermentation media, through a chemogenomics approach. OMICS 14:201–210. doi:10.1089/omi.2009.0149

    Article  CAS  PubMed  Google Scholar 

  36. Teixeira MC, Mira NP, Sa-Correia I (2010) A genome-wide perspective on the response and tolerance to food-relevant stresses in Saccharomyces cerevisiae. Curr Opin Biotechnol 22:150–156. doi:10.1016/j.copbio.2010.10.011

    Article  PubMed  Google Scholar 

  37. York JD, Odom AR, Murphy R, Ives EB, Wente SR (1999) A phospholipase C-dependent inositol polyphosphate kinase pathway required for efficient messenger RNA export. Science 285:96–100. doi:10.1126/science.285.5424.96

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Juan Carlos Parajó and Héctor Ruíz for assistance in the pre-treatment of lignocellulose biomass. Research described in this article was financially supported by FEDER and “Fundação para a Ciência e a Tecnologia” (FCT) (Contracts PEst-OE/EQB/LA0023/2011, PTDC/BIO/66151/2006, PTDC/AGR-ALI/102608/2008 and ERA-IB/0002/2010 and PhD grant (SFRH/BD/64776/2009) to FP).

Conflict of interests

The authors declare that they have no competing interests.

Author information

Authors and Affiliations

  1. CEB-Centre of Biological Engineering, Universidade do Minho, Campus de Gualtar, 4710-057, Braga, Portugal

    Francisco B. Pereira & Lucília Domingues

  2. Department of Bioengineering, Centre for Biological and Chemical Engineering, Instituto Superior Técnico, IBB-Institute for Biotechnology and Bioengineering, Universidade de Lisboa, Avenida Rovisco Pais, 1049-001, Lisbon, Portugal

    Miguel C. Teixeira, Nuno P. Mira & Isabel Sá-Correia

Authors
  1. Francisco B. Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Miguel C. Teixeira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nuno P. Mira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Isabel Sá-Correia
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lucília Domingues
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lucília Domingues.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 79 kb)

Supplementary material 2 (XLSX 74 kb)

10295_2014_1519_MOESM3_ESM.pdf

Supplementary material 3 (PDF 17 kb) Figure S1. Venn diagram representing the intersection of yeast determinants of a wheat straw hydrolysate (WSH) and synthetic hydrolysate (SH) resistance; b Synthetic hydrolysate (SH) and acetic acid [21] or furfural resistance [9]; c wheat straw hydrolysate (WSH) and acetic acid [21] or furfural resistance [9]

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pereira, F.B., Teixeira, M.C., Mira, N.P. et al. Genome-wide screening of Saccharomyces cerevisiae genes required to foster tolerance towards industrial wheat straw hydrolysates. J Ind Microbiol Biotechnol 41, 1753–1761 (2014). https://doi.org/10.1007/s10295-014-1519-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10295-014-1519-z

Keywords

Search

Navigation