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Xylose consumption and ethanol production by Pichia guilliermondii and Candida oleophila in the presence of furans, phenolic compounds, and organic acids commonly produced during the pre-treatment of plant biomass

  • Biotechnology and Industrial Microbiology - Short Communication
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Abstract

For 2G ethanol production, pentose fermentation and yeast tolerance to lignocellulosic hydrolyzate components are essential to improve biorefinery yields. Generally, physicochemical pre-treatment methodologies are used to facilitate access to cellulose and hemicellulose in plant material, which consequently can generate microbial growth inhibitory compounds, such as furans, weak acids, and phenolic compounds. Because of the unsatisfactory yield of wild-type Saccharomyces cerevisiae during pentose fermentation, the search for xylose-fermenting yeasts tolerant to microbial growth inhibitors has gained attention. In this study, we investigated the ability of the yeasts Pichia guilliermondii G1.2 and Candida oleophila G10.1 to produce ethanol from xylose and tolerate the inhibitors furfural, 5-hydroxymethylfurfural (HMF), acetic acid, formic acid, ferulic acid, and vanillin. We demonstrated that both yeasts were able to grow and consume xylose in the presence of all single inhibitors, with greater growth limitation in media containing furfural, acetic acid, and vanillin. In saline medium containing a mixture of these inhibitors (2.5–3.5 mM furfural and HMF, 1 mM ferulic acid, 1–1.5 mM vanillin, 10–13 mM acetic acid, and 5–7 mM formic acid), both yeasts were able to produce ethanol from xylose, similar to that detected in the control medium (without inhibitors). In future studies, the proteins involved in the transport of pentose and tolerance to these inhibitors need to be investigated.

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References

  1. Silva RR, Prista C, Dias MCL, Boscolo M, Da Silva R, Gomes E (2019) Improved utility of pentoses from lignocellulolytic hydrolysate: challenges and perspectives for enabling Saccharomyces cerevisiae. J Agric Food Chem 67(21):5919–5921

    Article  PubMed  Google Scholar 

  2. Rezania S, Oryani B, Cho J, Talaiekhozani A, Sabbagh F, Hashemi B, Rupani PF, Mohammadi AA (2020) Different pretreatment technologies of lignocellulosic biomass for bioethanol production: an overview. Energy 199:117457

    Article  CAS  Google Scholar 

  3. Robak K, Balcerek M (2018) Review of second generation bioethanol production from residual biomass. Food Technol Biotechnol 56:174–187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Sjulander N, Kikas T (2020) Origin, impact and control of lignocellulosic inhibitors in bioethanol production—a review. Energies 13:4751

    Article  CAS  Google Scholar 

  5. van der Maas L, Driessen JLSP, Mussatto SI (2021) Effects of inhibitory compounds present in lignocellulosic biomass hydrolysates on the growth of Bacillus subtilis. Energies 14:8419

    Article  Google Scholar 

  6. Alokika A, Kumar A, Kumar V, Singh B (2021) Cellulosic and hemicellulosic fractions of sugarcane bagasse: potential, challenges and future perspective. Int J Biol Macromol 169:564–582

    Article  CAS  PubMed  Google Scholar 

  7. Young EM, Tong A, Bui H, Spofford C, Alper HS (2014) Rewiring yeast sugar transporter preference through modifying a conserved protein motif. PNAS 111:131–136

    Article  PubMed  Google Scholar 

  8. Silva RR, Prista C, Dias MCL, Boscolo M, Da Silva R, Gomes E (2020) Prospecting for L-arabinose/D-xylose symporters from Pichia guilliermondii and Aureobasidium leucospermi. Braz J Microbiol 51:145–150

    Article  PubMed  Google Scholar 

  9. Narayanan V, Nogué VS, Van Niel EWJ, Gorwa-Grauslund MF (2016) Adaptation to low pH and lignocellulosic inhibitors resulting in ethanolic fermentation and growth of Saccharomyces cerevisiae. AMB Express 6:59

    Article  PubMed  PubMed Central  Google Scholar 

  10. Boekhout T, Amend AS, Baidouri F, Gabaldón T, Geml J, Mittelbach M, Robert V, Tan CS, Turchetti B, Vu D, Wang Q-M, Yurkov A (2022) Trends in yeast diversity discovery. Fungal Divers 114:491–537

    Article  Google Scholar 

  11. Boekhout T, Bai FY, Daniel HM, Groenewald M, Robert V, Tan CS, Yurkov A (2022) The Yeasts Trust Database. https://theyeasts.org

  12. Martins GM, Bocchini-Martins DA, Bezzerra-Bussolia C, Pagnocca FC, Boscolo M, Monteiro DA, Da Silva R, Gomes E (2018) The isolation of pentose-assimilating yeasts and their xylose fermentation potential. Braz J Microbiol 49:162–168

    Article  CAS  PubMed  Google Scholar 

  13. Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

    Article  CAS  Google Scholar 

  14. Almeida JRM, Runquist D, Nogué VS, Lidén G, Gorwa-Grauslund MF (2011) Stress-related challenges in pentose fermentation to ethanol by the yeast Saccharomyces cerevisiae. Biotechnol J 6:286–299

    Article  CAS  PubMed  Google Scholar 

  15. Ran H, Zhang J, Gao Q, Lin Z, Bao J (2014) Analysis of biodegradation performance of furfural and 5-hydroxymethylfurfural by Amorphotheca resinae ZN1. Biotechnol Biofuels 7:51

    Article  PubMed  PubMed Central  Google Scholar 

  16. Kim D (2018) Physico-chemical conversion of lignocellulose: inhibitor effects and detoxification strategies: a mini review. Molecules 23:309

    Article  PubMed  PubMed Central  Google Scholar 

  17. Senatham S, Chamduang T, Kaewchingduang Y, Thammasittirong A, Srisodsuk M, Elliston A, Roberts IN, Waldron KW, Thammasittirong SN-R (2016) Enhanced xylose fermentation and hydrolysate inhibitor tolerance of Scheffersomyces shehatae for efficient ethanol production from non-detoxified lignocellulosic hydrolysate. SpringerPlus 5:1040

    Article  PubMed  PubMed Central  Google Scholar 

  18. Zhao M, Shi D, Lu X, Zong H, Zhuge B, Ji H (2019) Ethanol fermentation from non-detoxified lignocellulose hydrolysate by a multi-stress tolerant yeast Candida glycerinogenes mutant. Bioresour Technol 273:634–640

    Article  CAS  PubMed  Google Scholar 

  19. Konzock O, Zaghen S, Norbeck J (2021) Tolerance of Yarrowia lipolytica to inhibitors commonly found in lignocellulosic hydrolysates. BMC Microbiol 21:77

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. López PC, Peng C, Arneborg N, Junicke H, Gernaey KV (2021) Analysis of the response of the cell membrane of Saccharomyces cerevisiae during the detoxification of common lignocellulosic inhibitors. Sci Rep 11:6853

    Article  PubMed  PubMed Central  Google Scholar 

  21. Bhavana BK, Mudliar SN, Bokade VV, Debnath S (2022) Efect of furfural, acetic acid and 5-hydroxymethylfurfural on yeast growth and xylitol fermentation using Pichia stipitis NCIM 3497. Biomass Convers Biorefnery. https://doi.org/10.1007/s13399-022-02758-w

  22. Caspeta L, Castillo T, Nielsen J (2015) Modifying yeast tolerance to inhibitory conditions of ethanol production processes. Front Bioeng Biotechnol 3:184. https://doi.org/10.3389/fbioe.2015.00184

    Article  PubMed  PubMed Central  Google Scholar 

  23. Wang S, Cheng G, Joshua C, He Z, Sun X, Li R, Liu L, Yuan Q (2016) Furfural tolerance and detoxification mechanism in Candida tropicalis. Biotechnol Biofuels 9:250

    Article  PubMed  PubMed Central  Google Scholar 

  24. Palma M, Guerreiro JF, Sá-Correia I (2018) Adaptive response and tolerance to acetic acid in Saccharomyces cerevisiae and Zygosaccharomyces bailii: a physiological genomics perspective. Front Microbiol 9:274. https://doi.org/10.3389/fmicb.2018.00274

    Article  PubMed  PubMed Central  Google Scholar 

  25. Shen Y, Li H, Wang X, Zhang X, Hou J, Wang L, Gao N, Bao X (2014) High vanillin tolerance of an evolved Saccharomyces cerevisiae strain owing to its enhanced vanillin reduction and antioxidative capacity. J Ind Microbiol Biotechnol 41:1637–1645

    Article  CAS  PubMed  Google Scholar 

  26. Liang Z, Wang X, Bao X, Wei T, Hou J, Liu W, Shen Y (2021) Newly identified genes contribute to vanillin tolerance in Saccharomyces cerevisiae. Microb Biotechnol 14:503–516

    Article  CAS  PubMed  Google Scholar 

  27. Nandal P, Sharma S, Arora A (2020) Bioprospecting non-conventional yeasts for ethanol production from rice straw hydrolysate and their inhibitor tolerance. Renew. Energy 147:1694e1703

    Google Scholar 

  28. Cheng K-K, Wu J, Lin Z-N, Zhang J-A (2014) Aerobic and sequential anaerobic fermentation to produce xylitol and ethanol using non-detoxified acid pretreated corncob. Biotechnol Biofuels 7:166

    Article  PubMed  PubMed Central  Google Scholar 

  29. Perna MSC, Bastos RG, Ceccato-Antonini SR (2018) Single and combined efects of acetic acid, furfural, and sugars on the growth of the pentose-fermenting yeast Meyerozyma guilliermondii. Biotech 3(8):119

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Funding

Financial support is provided by Fundação de Amparo à Pesquisa do Estado de São Paulo-FAPESP (processes 2017/06399-3 and 2017/06066-4) and Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq (process 166496/2020-0).

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Correspondence to Ronivaldo Rodrigues da Silva.

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da Silva, R.R., Zaiter, M.A., Boscolo, M. et al. Xylose consumption and ethanol production by Pichia guilliermondii and Candida oleophila in the presence of furans, phenolic compounds, and organic acids commonly produced during the pre-treatment of plant biomass. Braz J Microbiol 54, 753–759 (2023). https://doi.org/10.1007/s42770-023-00937-z

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  • DOI: https://doi.org/10.1007/s42770-023-00937-z

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