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Pulp and paper industry side-stream materials as feed for the oleaginous yeast species Lipomyces starkeyi and Rhodotorula toruloides

  • Shiromini Gamage , Sara Norström , Madelen Olofsson , Dan Bylund , Mojtaba Asadollahi and Erik Hedenström ORCID logo EMAIL logo
Published/Copyright: January 10, 2025
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Abstract

The pulp and paper industry in Sweden annually produce millions of tons of side-stream materials as black liquor, pulp and paper mill sludge, sulfite liquor and lignosulfonate. These lignocellulosic based materials can be more utilized today in biorefinery processes with microorganisms to produce high-value products as lipids, proteins and biofuels. In this work, we used five side-stream materials as carbon source in fermentation with two oleaginous yeasts, Lipomyces starkeyi and Rhodotorula toruloides. We analyzed lipid production, fatty acid profiles, inhibitors, phenolics, free sugars and metals before and after batch fermentation in 2 L bioreactors. Steam-exploded hardwood media was used as reference as it’s known to be a good substrate for the oleaginous yeast species and after fermentation the lipid yield for R. toruloides was 17 % (w/w) and for L. starkeyi 13 % (w/w). The side-stream materials contained less than 30 % of free sugar compared to the reference media and the total lipid yield was thus less than 2.7 %, (w/w). R. toruloides utilized various sugars during fermentation and L. starkeyi mostly consumed glucose and xylose. Both yeast species also showed a possible ability to utilize various phenolics indicating their metabolic potential to convert depolymerized lignin along with wood-based sugars to lipids and proteins.


Corresponding author: Erik Hedenström, Department of Natural Science, Design, and Sustainable Development, Mid Sweden University, SE-851 70 Sundsvall, Sweden, E-mail:

Award Identifier / Grant number: 20201022

Acknowledgments

We gratefully acknowledge the financial support of the European Regional Development Fund, the Knowledge Foundation and Colabit AB. We also thank Domsjö Fabriker AB, Örnsköldsvik for the lignosulfonate sample and the sulfite liquor sample, SEKAB Biofuels and Chemicals AB, Örnsköldsvik for the steam exploded hardwood mixture, Iggesund Paper Mill, Iggesund for the Chemical sludge sample, SCA-Ortviken Paper Mill, Sundsvall for the bio sludge sample and SCA Östrand Pulp Mill, Timrå for the black liquor sample. We also acknowledge Per-Johan Alzen for input on the description of side-stream materials.

  1. Research ethics: Not applicable.

  2. Informed consent: Not applicable.

  3. Author contributions: The author(s) have (has) accepted responsibility for the entire content of this manuscript and approved its submission. Shiromini Gamage: Writing manuscript, planning, conducting the fermentation experiments and lipid extraction, GC analysis, HPLC analysis. Sara Norström: Conducting metal analysis and part of phenolic compounds analysis and reviewing the manuscript. Madelen Olofsson: Conducting phenolic compounds analysis and reviewing manuscript. Dan Bylund: Reviewing and editing the manuscript. Mojtaba Asadollahi: Reviewing and editing the manuscript. Erik Hedenström: Supervising guiding and editing manuscript.

  4. Use of Large Language Models, AI and Machine Learning Tools: None declared.

  5. Conflict of interest: The author(s) state(s) no conflict of interest.

  6. Research funding: We gratefully acknowledge the financial support of the European Regional Development Fund, the Knowledge Foundation and Colabit AB.

  7. Data availability: The raw data can be obtained on request from the corresponding author.

References

Adeboye, P.T., Bettiga, M., and Olsson, L. (2014). The chemical nature of phenolic compounds determines their toxicity and induces distinct physiological responses in Saccharomyces cerevisiae in lignocellulose hydrolysates. AMB Express 4: 46, https://doi.org/10.1186/s13568-014-0046-7.Search in Google Scholar PubMed PubMed Central

Arevalo-Gallegos, A., Ahmad, Z., Asgher, M., Parra-Saldivar, R., and Iqbal, H.M.N. (2017). Lignocellulose: a sustainable material to produce value-added products with a zero waste approach—a review. Int. J. Biol. Macromol. 99: 308–318, https://doi.org/10.1016/j.ijbiomac.2017.02.097.Search in Google Scholar PubMed

Bonturi, N., Matsakas, L., Nilsson, R., Christakopoulos, P., Miranda, E., Berglund, K., and Rova, U. (2015). Single cell oil producing yeasts Lipomyces starkeyi and Rhodosporidium toruloides: selection of extraction strategies and biodiesel property prediction. Energies 8: 5040–5052, https://doi.org/10.3390/en8065040.Search in Google Scholar

Borrero-López, A.M., Valencia, C., and Franco, J.M. (2022). Lignocellulosic materials for the production of biofuels, biochemicals and biomaterials and applications of lignocellulose-based polyurethanes: a review. Polymers 14: 881, https://doi.org/10.3390/polym14050881.Search in Google Scholar PubMed PubMed Central

Calvey, C.H., Su, Y.-K., Willis, L.B., McGee, M.S., and Jeffries, T.J. (2016). Nitrogen limitation, oxygen limitation, and lipid accumulation in Lipomyces starkeyi. Bioresour. Technol. 200: 780–788, https://doi.org/10.1016/j.biortech.2015.10.104.Search in Google Scholar PubMed

Dzurendova, S., Zimmermann, B., Tafintseva, V., Kohler, A., Horn, S.J., and Shapaval, V. (2020). Metal and phosphate ions show remarkable influence on the biomass production and lipid accumulation in oleaginous mucor circinelloides. J. Fungi 6: 260, https://doi.org/10.3390/jof6040260.Search in Google Scholar PubMed PubMed Central

Fickers, P., Benetti, P., Wache, Y., Marty, A., Mauersberger, S., Smit, M., and Nicaud, J. (2005). Hydrophobic substrate utilisation by the yeast Yarrowia lipolytica, and its potential applications. FEMS Yeast Res. 5: 527–543, https://doi.org/10.1016/j.femsyr.2004.09.004.Search in Google Scholar PubMed

Guo, Z., Khoomrung, S., Nielsen, J., and Olsson, L. (2018). Changes in lipid metabolism convey acid tolerance in Saccharomyces cerevisiae. Biotechnol. Biofuels 11: 297, https://doi.org/10.1186/s13068-018-1295-5.Search in Google Scholar PubMed PubMed Central

Hu, C., Zhao, X., Zhao, J., Wu, S., and Zhao, Z.K. (2009). Effects of biomass hydrolysis by-products on oleaginous yeast Rhodosporidium toruloides. Bioresour. Technol. 100: 4843–4847, https://doi.org/10.1016/j.biortech.2009.04.041.Search in Google Scholar PubMed

Huang, C., Wu, H., Liu, Z., Cai, J., Lou, W., and Zong, M. (2012). Effect of organic acids on the growth and lipid accumulation of oleaginous yeast Trichosporon fermentans. Biotechnol. Biofuels 5: 4, https://doi.org/10.1186/1754-6834-5-4.Search in Google Scholar PubMed PubMed Central

Iram, A., Berenjian, A., and Demirci, A. (2021). A review on the utilization of lignin as a fermentation substrate to produce lignin-modifying enzymes and other value-added products. Molecules 26: 2960, https://doi.org/10.3390/molecules26102960.Search in Google Scholar PubMed PubMed Central

Isikgor, F.H. and Becer, C.R. (2015). Lignocellulosic biomass: a sustainable platform for the production of bio-based chemicals and polymers. Polym. Chem. 6: 4497–4559, https://doi.org/10.1039/C5PY00263J.Search in Google Scholar

Lei, Y., Wang, X., Sun, S., He, B., Sun, W., Wang, K., Chen, Z., Guo, Z., and Li, Z. (2024). A review of lipid accumulation by oleaginous yeasts: culture mode. Sci. Total Environ. 919: 170385, https://doi.org/10.1016/j.scitotenv.2024.170385.Search in Google Scholar PubMed

Lyu, L., Chu, Y., Zhang, S., Zhang, Y., Huang, Q., Wang, S., and Zhao, Z.K. (2021). Engineering the oleaginous yeast Rhodosporidium toruloides for improved resistance against inhibitors in biomass hydrolysates. Front. Bioeng. Biotechnol. 9: 768934, https://doi.org/10.3389/fbioe.2021.768934.Search in Google Scholar PubMed PubMed Central

Morrison, W.R. and Smith, L.M. (1964). Preparation of fatty acid methyl esters and dimethylacetals from lipids with boron fluoride–methanol. J. Lipid Res. 5: 600–608, https://doi.org/10.1016/S0022-2275(20)40190-7.Search in Google Scholar

Moeltner, L. and Schallhart, V. (2020). Potential of biomass to liquid-hydrotreated vegetable oils- and fatty acid methyl esters-blends for diesel engines in passenger cars. Front. Mech. Eng. 6: 576155, https://doi.org/10.3389/fmech.2020.576155.Search in Google Scholar

Olofsson, M.A., Norström, S.H., and Bylund, D. (2014). Evaluation of sampling and sample preparation procedures for the determination of aromatic acids and their distribution in a podzol soil using liquid chromatography–tandem mass spectrometry. Geoderma 232–234: 373–380, https://doi.org/10.1016/j.geoderma.2014.06.005.Search in Google Scholar

Osorio‐González, C.S., Hegde, K., Brar, S.K., Kermanshahipour, A., and Avalos‐Ramírez, A. (2019). Challenges in lipid production from lignocellulosic biomass using Rhodosporidium sp.; a look at the role of lignocellulosic inhibitors. Biofuels, Bioprod. Biorefining 13: 740–759, https://doi.org/10.1002/bbb.1954.Search in Google Scholar

Putra, F.J.N., Kahar, P., Kondo, A., and Ogino, C. (2022). Valorization of lignin and its derivatives using yeast. Processes 10: 2004, https://doi.org/10.3390/pr10102004.Search in Google Scholar

Robles-Iglesias, R., Naveira-Pazos, C., Ferna ndez-Blanco, C., Veiga, M.C., and Kennes, C. (2023). Factors affecting the optimisation and scale-up of lipid accumulation in oleaginous yeasts for sustainable biofuels production. Renew. Sustain. Energy Rev. 171: 113043, https://doi.org/10.1016/j.rser.2022.113043.Search in Google Scholar

Saini, R., Hegde, K., Osorio-Gonzalez, C.S., Brar, S.K., and Vezina, P. (2020). Evaluating the potential of Rhodosporidium toruloides-1588 for high lipid production using undetoxified wood hydrolysate as a carbon source. Energies 13: 5960, https://doi.org/10.3390/en13225960.Search in Google Scholar

Saini, R.K., Prasad, P., Sreedhar, R.V., Naidu, K.A., Shang, X., and Keum, Y.-S. (2021). Omega-3 polyunsaturated fatty acids (PUFAs): emerging plant and microbial sources, oxidative stability, bioavailability, and health benefits—a review. Antioxidants 10: 1627, https://doi.org/10.3390/antiox10101627.Search in Google Scholar PubMed PubMed Central

Sharma, T., Sailwal, M., Dasgupta, D., Hazra, S., Bhaskar, T., and Ghosh, D. (2021). Effect of lignocellulosic biomass inhibitors on oleaginous yeast cultivation in multistage fermentation system. Bioresour. Technol. Rep. 15: 100791, https://doi.org/10.1016/j.biteb.2021.100791.Search in Google Scholar

Sitepu, I., Selby, T., Lin, T., Zhu, S., and Boundy-Mills, K. (2014). Carbon source utilization and inhibitor tolerance of 45 oleaginous yeast species. J. Ind. Microbiol. Biotechnol. 41: 1061–1070, https://doi.org/10.1007/s10295-014-1447-y.Search in Google Scholar PubMed PubMed Central

Sluiter, A.D., Hames, B.R., Ruiz, R.O., Scarlata, C.J., Sluiter, J., Templeton, D.W., and Crocker, D.P. (2004). Determination of structural carbohydrates and lignin in biomass, Avialable at: <https://api.semanticscholar.org/CorpusID:100361490>.Search in Google Scholar

Udeh, H.O., Kgatla, T.E., and Jideani, A.I.O. (2014). Effect of mineral ion addition on yeast performance during very high gravity worth fermentation. Int. J. Biol. Biomol. Agricult. Food Biotechnol. Eng. 8: 1208–1216.Search in Google Scholar

Wang, W., Lemaire, R., Bensakhria, A., and Luart, D. (2022). Review on the catalytic effects of alkali and alkaline earth metals (AAEMs) including sodium, potassium, calcium and magnesium on the pyrolysis of lignocellulosic biomass and on the co-pyrolysis of coal with biomass. J. Anal. Appl. Pyrolysis 163: 105479, https://doi.org/10.1016/j.jaap.2022.105479.Search in Google Scholar

Wiebe, M.G., Koivuranta, K., Penttilä, M., and Ruohonen, L. (2012). Lipid production in batch and fed-batch cultures of Rhodosporidium toruloidesfrom 5 and 6 carbon carbohydrates. BMC Biotechnol. 12: 26, https://doi.org/10.1186/1472-6750-12-26.Search in Google Scholar PubMed PubMed Central

Yaegashi, J., Kirby, J., Ito, M., Sun, J., Dutta, T., Mirsiaghi, M., Sundstrom, E.R., Rodriguez, A., Baidoo, E., Tanjore, D., et al.. (2017). Rhodosporidium toruloides: a new platform organism for conversion of lignocellulose into terpene biofuels and bioproducts. Biotechnol. Biofuels 10: 241, https://doi.org/10.1186/s13068-017-0927-5.Search in Google Scholar PubMed PubMed Central

Yang, S., Franden, M.A., Yang, Q., Chou, Y.-C., Zhang, M., and Pienkos, P.T. (2018). Identification of inhibitors in lignocellulosic slurries and determination of their effect on hydrocarbon-producing microorganisms. Front. Bioeng. Biotechnol. 6: 23, https://doi.org/10.3389/fbioe.2018.00023.Search in Google Scholar PubMed PubMed Central


Supplementary Material

This article contains supplementary material (https://doi.org/10.1515/npprj-2024-0039).


Received: 2024-05-15
Accepted: 2024-12-23
Published Online: 2025-01-10
Published in Print: 2025-03-26

© 2024 Walter de Gruyter GmbH, Berlin/Boston

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