Skip to main content
SpringerLink
Log in

Rice bran extract as an alternative nutritional supplement for Kluyveromyces marxianus

  • Original Article
  • Published:
Biomass Conversion and Biorefinery Aims and scope Submit manuscript

Abstract

The Kluyveromyces marxianus yeast has been arousing great interest as a biocatalyst for biorefineries due to its ability to assimilate different sugars, in addition to its rapid growth, thermotolerance, and GRAS status. In this research, different sources of nutrients, such as rice bran and extracts of malt, yeast, and peptone, were evaluated for the cultivation of K. marxianus ATCC 36,907 aiming at ethanol production in submerged fermentations conducted in a batch system. Mineral supplementation of the medium was also evaluated. The best results of process performance for production, yield, and productivity in ethanol were obtained in the medium supplemented with rice bran extract, calcium chloride, and ammonium sulfate (25.50 g/L; Y(P/S) 0.49 g/g; QP 2.13 g/Lh), and the medium supplemented only with yeast-malt extract peptone (YMP) (24.88 g/L; Y(P/S) 0.50 g/g; QP 2.06 g/Lh), after 12 h of cultivation. Supplementation of the medium with malt extract without adding mineral salts also contributed to similar values of production and yield in ethanol after 24 h of cultivation (25.59 g/L; Y(P/S) 0.50 g/g; QP 1.16 g/Lh−1). The results revealed no need for mineral supplementation of the media added with YMP or malt extract for ethanol production by the yeast. On the other hand, rice bran extract, mainly associated with calcium chloride and ammonium sulfate, represents an excellent and inexpensive source of nutrients for this yeast and has the potential to replace traditional commercial supplements.

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

Data availability

The datasets generated during the current study are available in the manuscript itself.

References

  1. OECD/FAO (2020) OECD-FAO Agricultural Outlook 2020–2029. In: Table C.1 - World Cereal Proj. OECD-FAO Agric. Outlook 2020–2029. https://www.oecd-ilibrary.org/agriculture-and-food/oecd-fao-agricultural-outlook-2020-2029_1112c23b-en. Accessed 1 Apr 2022

  2. Huang B, Huang C, Lyu Z et al (2018) Available energy and amino acid digestibility of defatted rice bran fed to growing pigs1. J Anim Sci 96:3138–3150. https://doi.org/10.1093/jas/sky191

    Article  Google Scholar 

  3. Bodie AR, Micciche AC, Atungulu GG, et al (2019) Current trends of rice milling byproducts for agricultural applications and alternative food production systems. Front Sustain Food Syst 3:Article 47. https://doi.org/10.3389/fsufs.2019.00047

  4. SpaggiariDall’Asta MC, Galaverna G, del Castillo Bilbao MD (2021) Rice bran by-product: from valorization strategies to nutritional perspectives. Foods 10:85. https://doi.org/10.3390/foods10010085

    Article  Google Scholar 

  5. Moriyama S, Fukumoto K, Taniguchi M et al (2013) Rice bran extract (RBE) as supplement for cell culture. BMC Proc 7:P106. https://doi.org/10.1186/1753-6561-7-S6-P106

    Article  Google Scholar 

  6. Seyoum Y, Humblot C, Baxter BA, et al (2022) Metabolomics of rice bran differentially impacted by fermentation with six probiotics demonstrates key nutrient changes for enhancing gut health. Front Nutr 8:Article 795334. https://doi.org/10.3389/fnut.2021.795334

  7. Narh C, Frimpong C, Mensah A, Wei Q (2018) Rice bran, an alternative nitrogen source for Acetobacter xylinum bacterial cellulose synthesis. BioResources 13:4346–4363. https://doi.org/10.15376/biores.13.2.4346-4363

    Article  Google Scholar 

  8. Moreira VR, Lebron YAR, Freire SJ et al (2019) Evaluation of rice bran as a supplement for production of bioethanol by Saccharomyces cerevisiae. Floresta e Ambient 26:e20180423. https://doi.org/10.1590/2179-8087.042318

    Article  Google Scholar 

  9. Mochidzuki K, Kobayashi S, Wang H et al (2015) Effect of rice bran as a nitrogen and carbohydrate source on fed-batch simultaneous saccharification and fermentation for the production of bioethanol from rice straw. J Japan Inst Energy 94:151–158. https://doi.org/10.3775/jie.94.151

    Article  Google Scholar 

  10. Martiniano SE, Philippini RR, Chandel AK et al (2014) Evaluation of rice bran extract as a nitrogen source for improved hemicellulosic ethanol production from sugarcane bagasse by new xylose-fermenting yeast strains isolated from Brazilian forests. Sugar Tech 16:1–8. https://doi.org/10.1007/s12355-013-0219-8

    Article  Google Scholar 

  11. da Silva DDV, de Cândido EJ, de Arruda PV et al (2014) New cultive medium for bioconversion of C5 fraction from sugarcane bagasse using rice bran extract. Brazilian J Microbiol 45:1469–1475. https://doi.org/10.1590/S1517-83822014000400043

    Article  Google Scholar 

  12. Lane MM, Burke N, Karreman R et al (2011) Physiological and metabolic diversity in the yeast Kluyveromyces marxianus. Antonie Van Leeuwenhoek 100:507–519. https://doi.org/10.1007/s10482-011-9606-x

    Article  Google Scholar 

  13. Ortiz-Merino RA, Varela JA, Coughlan AY, et al (2018) Ploidy variation in Kluyveromyces marxianus separates dairy and non-dairy isolates. Front Genet 9:Article 94. https://doi.org/10.3389/fgene.2018.00094

  14. Arora R, Behera S, Sharma NK, Kumar S (2019) Evaluating the pathway for co-fermentation of glucose and xylose for enhanced bioethanol production using flux balance analysis. Biotechnol Bioprocess Eng 24:924–933. https://doi.org/10.1007/s12257-019-0026-5

    Article  Google Scholar 

  15. Dasgupta D, Ghosh D, Bandhu S, Adhikari DK (2017) Lignocellulosic sugar management for xylitol and ethanol fermentation with multiple cell recycling by Kluyveromyces marxianus IIPE453. Microbiol Res 200:64–72. https://doi.org/10.1016/j.micres.2017.04.002

    Article  Google Scholar 

  16. Lane MM, Morrissey JP (2010) Kluyveromyces marxianus: a yeast emerging from its sister’s shadow. Fungal Biol Rev 24:17–26. https://doi.org/10.1016/j.fbr.2010.01.001

    Article  Google Scholar 

  17. Tseng C-C, Lin Y-J, Liu W et al (2020) Metabolic engineering probiotic yeast produces 3S, 3′S-astaxanthin to inhibit B16F10 metastasis. Food Chem Toxicol 135:110993. https://doi.org/10.1016/j.fct.2019.110993

    Article  Google Scholar 

  18. da Silva FL, de Oliveira CA, dos Santos DA et al (2018) Valorization of an agroextractive residue-Carnauba straw for the production of bioethanol by simultaneous saccharification and fermentation (SSF). Renew Energy 127:661–669. https://doi.org/10.1016/j.renene.2018.05.025

    Article  Google Scholar 

  19. da Costa Correia JA, de Sousa SJ, Gonçalves LRB, Rocha MVP (2020) Different design configurations of simultaneous saccharification and fermentation to enhance ethanol production from cashew apple bagasse pretreated with alkaline hydrogen peroxide applying the biorefinery concept. Biomass Convers Biorefinery. https://doi.org/10.1007/s13399-020-00796-w

    Article  Google Scholar 

  20. Lertwattanasakul N, Kosaka T, Hosoyama A et al (2015) Genetic basis of the highly efficient yeast Kluyveromyces marxianus: complete genome sequence and transcriptome analyses. Biotechnol Biofuels 8:47. https://doi.org/10.1186/s13068-015-0227-x

    Article  Google Scholar 

  21. Wang D, Wu D, Yang X, Hong J (2018) Transcriptomic analysis of thermotolerant yeast Kluyveromyces marxianus in multiple inhibitors tolerance. RSC Adv 8:14177–14192. https://doi.org/10.1039/C8RA00335A

    Article  Google Scholar 

  22. Mo W, Wang M, Zhan R et al (2019) Kluyveromyces marxianus developing ethanol tolerance during adaptive evolution with significant improvements of multiple pathways. Biotechnol Biofuels 12:63. https://doi.org/10.1186/s13068-019-1393-z

    Article  Google Scholar 

  23. Li P, Tan X, Fu X et al (2021) Metabolomic analysis reveals Kluyveromyces marxianus’s stress responses during high-temperature ethanol fermentation. Process Biochem 102:386–392. https://doi.org/10.1016/j.procbio.2021.01.024

    Article  Google Scholar 

  24. Tinôco D, da Silveira WB (2021) Kinetic model of ethanol inhibition for Kluyveromyces marxianus CCT 7735 (UFV-3) based on the modified Monod model by Ghose & Tyagi. Biologia (Bratisl) 76:3511–3519. https://doi.org/10.1007/s11756-021-00876-w

    Article  Google Scholar 

  25. Lang X, Besada-Lombana PB, Li M et al (2020) Developing a broad-range promoter set for metabolic engineering in the thermotolerant yeast Kluyveromyces marxianus. Metab Eng Commun 11:e00145. https://doi.org/10.1016/j.mec.2020.e00145

    Article  Google Scholar 

  26. Leonel LV, Arruda PV, Chandel AK et al (2021) Kluyveromyces marxianus: a potential biocatalyst of renewable chemicals and lignocellulosic ethanol production. Crit Rev Biotechnol 41:1131–1152. https://doi.org/10.1080/07388551.2021.1917505

    Article  Google Scholar 

  27. Proust L, Sourabié A, Pedersen M, et al (2019) Insights into the complexity of yeast extract peptides and their utilization by Streptococcus thermophilus. Front Microbiol 10:Article 906. https://doi.org/10.3389/fmicb.2019.00906

  28. Almeida ELM, Moreira e Silva G, Vassalli IA et al (2020) Effects of nitrogen supplementation on Saccharomyces cerevisiae JP14 fermentation for mead production. Food Sci Technol 40:336–343. https://doi.org/10.1590/fst.11219

    Article  Google Scholar 

  29. Busti S, Mapelli V, Tripodi F et al (2016) Respiratory metabolism and calorie restriction relieve persistent endoplasmic reticulum stress induced by calcium shortage in yeast. Sci Rep 6:27942. https://doi.org/10.1038/srep27942

    Article  Google Scholar 

  30. Guneser O, Yuceer YK, Hosoglu MI et al (2022) Production of flavor compounds from rice bran by yeasts metabolisms of Kluyveromyces marxianus and Debaryomyces hansenii. Brazilian J Microbiol. https://doi.org/10.1007/s42770-022-00766-6

    Article  Google Scholar 

  31. Camargo D, Gomes SD, Sene L (2014) Ethanol production from sunflower meal biomass by simultaneous saccharification and fermentation (SSF) with Kluyveromyces marxianus ATCC 36907. Bioprocess Biosyst Eng 37:2235–2242. https://doi.org/10.1007/s00449-014-1201-x

    Article  Google Scholar 

  32. Tavares B, Felipe MGA, dos Santos JC et al (2019) An experimental and modeling approach for ethanol production by Kluyveromyces marxianus in stirred tank bioreactor using vacuum extraction as a strategy to overcome product inhibition. Renew Energy 131:261–267. https://doi.org/10.1016/j.renene.2018.07.030

    Article  Google Scholar 

  33. AOAC International (2016) Official Methods of analysis, 20th ed. AOAC INTERNATIONAL, Rockville, MD

  34. Huang SC, Shiau CY, Liu TE et al (2005) Effects of rice bran on sensory and physico-chemical properties of emulsified pork meatballs. Meat Sci 70:613–619. https://doi.org/10.1016/j.meatsci.2005.02.009

    Article  Google Scholar 

  35. Ademola Za A, Ganiyat Ta O (2008) Comparative utilization of biodegraded rice husk in the diets of Clarias gariepinus. J Fish Aquat Sci 3:312–319. https://doi.org/10.3923/jfas.2008.312.319

    Article  Google Scholar 

  36. Palma M, Madeira SC, Mendes-Ferreira A, Sá-Correia I (2012) Impact of assimilable nitrogen availability in glucose uptake kinetics in Saccharomyces cerevisiae during alcoholic fermentation. Microb Cell Fact 11:99. https://doi.org/10.1186/1475-2859-11-99

    Article  Google Scholar 

  37. Ciesarová Z, Šmogrovičová D, Dömény Z (1996) Enhancement of yeast ethanol tolerance by calcium and magnesium. Folia Microbiol (Praha) 41:485–488. https://doi.org/10.1007/BF02814663

    Article  Google Scholar 

  38. Castillo-Plata AK, Sigala JC, Lappe-Oliveras P, Le Borgne S (2021) KCl/KOH supplementation improves acetic acid tolerance and ethanol production in a thermotolerant strain of Kluyveromyces marxianus isolated from henequen (Agave fourcroydes). Rev Mex Ing Química 21:1–18. https://doi.org/10.24275/rmiq/Bio2567

    Article  Google Scholar 

  39. Santos J, Sousa MJ, Leão C (2012) Ammonium is toxic for aging yeast cells, inducing death and shortening of the chronological lifespan. PLoS One 7:e37090. https://doi.org/10.1371/journal.pone.0037090

    Article  Google Scholar 

  40. de Melo AT, Martho KF, Roberto TN et al (2019) The regulation of the sulfur amino acid biosynthetic pathway in Cryptococcus neoformans: the relationship of Cys3, Calcineurin, and Gpp2 phosphatases. Sci Rep 9:11923. https://doi.org/10.1038/s41598-019-48433-5

    Article  Google Scholar 

  41. Leonel LV, Sene L, da Cunha MAA et al (2020) Valorization of apple pomace using bio-based technology for the production of xylitol and 2G ethanol. Bioprocess Biosyst Eng 43:2153–2163. https://doi.org/10.1007/s00449-020-02401-w

    Article  Google Scholar 

  42. Milessi TSS, Antunes FAF, Chandel AK, Silva SS (2013) Rice bran extract: an inexpensive nitrogen source for the production of 2G ethanol from sugarcane bagasse hydrolysate. 3 Biotech 3:373–379. https://doi.org/10.1007/s13205-012-0098-9

    Article  Google Scholar 

  43. Zarei I, Brown DG, Nealon NJ, Ryan EP (2017) Rice bran metabolome contains amino acids, vitamins & cofactors, and phytochemicals with medicinal and nutritional properties. Rice 10:24. https://doi.org/10.1186/s12284-017-0157-2

    Article  Google Scholar 

  44. Oda Y, Nakamura K, Shinomiya N, Ohba K (2010) Ethanol fermentation of sugar beet thick juice diluted with crude cheese whey by the flex yeast Kluyveromyces marxianus KD-15. Biomass Bioenerg 34:1263–1266. https://doi.org/10.1016/j.biombioe.2010.03.014

    Article  Google Scholar 

  45. Clarke KG (2013) Microbiology. In: Clarke KG (ed) Bioprocess Engineering. Elsevier, pp 7–24

    Chapter  Google Scholar 

  46. Demiray E, Ertuğrul Karatay S, Dönmez G (2020) Efficient bioethanol production from pomegranate peels by newly isolated Kluyveromyces marxianus. Energy Sources Part A Recover Util Environ Eff 42:709–718. https://doi.org/10.1080/15567036.2019.1600621

    Article  Google Scholar 

  47. Jiang Y, Shi Y, Li R et al (2021) The peptides in oat and malt extracts that are preferentially absorbed by Lactobacillus plantarum and stimulates its proliferation in milk. Int J Food Sci Technol 56:4690–4699. https://doi.org/10.1111/ijfs.15140

    Article  Google Scholar 

  48. Pentjuss A, Stalidzans E, Liepins J et al (2017) Model-based biotechnological potential analysis of Kluyveromyces marxianus central metabolism. J Ind Microbiol Biotechnol 44:1177–1190. https://doi.org/10.1007/s10295-017-1946-8

    Article  Google Scholar 

  49. Sakihama Y, Hidese R, Hasunuma T, Kondo A (2019) Increased flux in acetyl-CoA synthetic pathway and TCA cycle of Kluyveromyces marxianus under respiratory conditions. Sci Rep 9:5319. https://doi.org/10.1038/s41598-019-41863-1

    Article  Google Scholar 

  50. Silva GM, Giordano RLC, Cruz AJG, Ramachandriya KD et al (2015) Ethanol production from sugarcane bagasse using SSF process and thermotolerant yeast. Trans ASABE 58:193–200. https://doi.org/10.13031/trans.58.11024

    Article  Google Scholar 

  51. Van Urk H, Voll WSL, Scheffers WA, Van Dijken JP (1990) Transient-state analysis of metabolic fluxes in crabtree-positive and crabtree-negative yeasts. Appl Environ Microbiol 56:281–287. https://doi.org/10.1128/aem.56.1.281-287.1990

    Article  Google Scholar 

  52. Pessani NK, Atiyeh HK, Wilkins MR et al (2011) Simultaneous saccharification and fermentation of Kanlow switchgrass by thermotolerant Kluyveromyces marxianus IMB3: The effect of enzyme loading, temperature and higher solid loadings. Bioresour Technol 102:10618–10624. https://doi.org/10.1016/j.biortech.2011.09.011

    Article  Google Scholar 

  53. Fu X, Li P, Zhang L, Li S (2019) Understanding the stress responses of Kluyveromyces marxianus after an arrest during high-temperature ethanol fermentation based on integration of RNA-Seq and metabolite data. Appl Microbiol Biotechnol 103:2715–2729. https://doi.org/10.1007/s00253-019-09637-x

    Article  Google Scholar 

  54. Saini P, Beniwal A, Malik RK, Vij S (2017) Comparative physiology of Kluyveromyces marxianus and Saccharomyces cerevisiae during batch cultivation on glucose as a sole carbon source. Indian J Dairy Sci 70:427–433

    Google Scholar 

  55. Rodrussamee N, Lertwattanasakul N, Hirata K et al (2011) Growth and ethanol fermentation ability on hexose and pentose sugars and glucose effect under various conditions in thermotolerant yeast Kluyveromyces marxianus. Appl Microbiol Biotechnol 90:1573–1586. https://doi.org/10.1007/s00253-011-3218-2

    Article  Google Scholar 

  56. Madeira-Jr JV, Gombert AK (2018) Towards high-temperature fuel ethanol production using Kluyveromyces marxianus: on the search for plug-in strains for the Brazilian sugarcane-based biorefinery. Biomass Bioenerg 119:217–228. https://doi.org/10.1016/j.biombioe.2018.09.010

    Article  Google Scholar 

  57. Costa DA, de Souza CJA, Costa PS et al (2014) Physiological characterization of thermotolerant yeast for cellulosic ethanol production. Appl Microbiol Biotechnol 98:3829–3840. https://doi.org/10.1007/s00253-014-5580-3

    Article  Google Scholar 

  58. Arora R, Behera S, Sharma NK, Kumar S (2017) Augmentation of ethanol production through statistically designed growth and fermentation medium using novel thermotolerant yeast isolates. Renew Energy 109:406–421. https://doi.org/10.1016/j.renene.2017.03.059

    Article  Google Scholar 

Download references

Funding

The authors are grateful to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for funding the scholarship of T.C. Pintro and L.V. Leonel (Financing Code 001).

Author information

Authors and Affiliations

  1. Center of Exact and Technological Sciences, Western Paraná State University, Cascavel, Paraná, Brazil

    Luciane Sene, Tania Claudia Pintro & Lillian Vieira Leonel

  2. Medical and Pharmaceutical Sciences Center, Western Paraná State University, Cascavel, Paraná, Brazil

    Suzana Bender

  3. Chemistry Department, Federal University of Technology - Paraná, Pato Branco, Paraná, Brazil

    Mário Antônio Alves da Cunha

Authors
  1. Luciane Sene
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tania Claudia Pintro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lillian Vieira Leonel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Suzana Bender
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mário Antônio Alves da Cunha
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

L. Sene and T.C. Pintro: experiment design; T.C. Pintro, L.V. Leonel, and S. Bender: investigation and laboratory analysis. T.C. Pintro: data analysis. L. Sene and T.C. Pintro: writing (original draft). L. Sene and M.A.A. Cunha: writing (review and editing).

Corresponding author

Correspondence to Luciane Sene.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

All the authors have read and understood the editorial policies for publication.

Competing interests

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.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 23 KB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sene, L., Pintro, T.C., Leonel, L.V. et al. Rice bran extract as an alternative nutritional supplement for Kluyveromyces marxianus. Biomass Conv. Bioref. 14, 11479–11489 (2024). https://doi.org/10.1007/s13399-022-03252-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13399-022-03252-z

Keywords

Search

Navigation