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.
References
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
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
Robak K, Balcerek M (2018) Review of second generation bioethanol production from residual biomass. Food Technol Biotechnol 56:174–187
Sjulander N, Kikas T (2020) Origin, impact and control of lignocellulosic inhibitors in bioethanol production—a review. Energies 13:4751
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
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
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
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
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
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
Boekhout T, Bai FY, Daniel HM, Groenewald M, Robert V, Tan CS, Yurkov A (2022) The Yeasts Trust Database. https://theyeasts.org
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
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428
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
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
Kim D (2018) Physico-chemical conversion of lignocellulose: inhibitor effects and detoxification strategies: a mini review. Molecules 23:309
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
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
Konzock O, Zaghen S, Norbeck J (2021) Tolerance of Yarrowia lipolytica to inhibitors commonly found in lignocellulosic hydrolysates. BMC Microbiol 21:77
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
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
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
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
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
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
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
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
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
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
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).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Responsible Editor: Luis Augusto Nero
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42770-023-00937-z