Skip to main content
SpringerLink
Log in

Bioethanol production from mulberry pomace by newly ısolated non-conventional yeast Hanseniaspora uvarum

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

Abstract

Lignocellulosic biomass as a cheap and abundant raw material offers great advantages in terms of biotechnological applications. The current study aimed to produce bioethanol from mulberry pomace by newly isolated xylose/glucose co-fermenter Hanseniaspora uvarum. For this purpose, the xylose consumption capacity of the yeast was first tested using the synthetic xylose-containing medium as a carbon source, and Hanseniaspora uvarum effectively fermented xylose into ethanol. Afterward, Hansenispora uvarum was used for the fermentation of the liquid hydrolysate obtained by dilute acid pretreatment of mulberry pomace. Furthermore, a subsequent enzymatic hydrolysis of the pretreated mulberry pomace was performed to investigate its effect. For this purpose, initial biomass concentration (50–500 g/L) for fermentation was optimized in two different mulberry pomace media containing nitrogen sources or mineral salts. Enzymatic hydrolysis of pretreated mulberry pomace was performed at 400 g/L initial biomass loading with or without soluble soy protein addition, and a significant increase in fermentable sugar concentrations was observed. The highest sugar concentration was observed as 159.6 g/L when 400 g/L biomass loading was used during dilute acid pretreatment, and subsequent enzymatic hydrolysis was performed using 15 FPU/g cellulose. Moreover, after dilute acid pretreatment and enzymatic hydrolysis, ethanol production of Hanseniaspora uvarum reached 61.3 g/L (0.153 g/gbiomass) which is a sufficient amount for efficient distillation according to literature. Results show that xylose/glucose co-fermenter Hanseniaspora uvarum and mulberry pomace can be considered for second-generation bioethanol production.

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
Fig. 3
Fig. 4

Similar content being viewed by others

Data Availability

Not applicable.

References

  1. Lugani Y, Rai R, Prabhu AA et al (2020) Recent advances in bioethanol production from lignocelluloses: a comprehensive review with a focus on enzyme engineering and designer biocatalysts. Biofuel Res J 7:1267–1295. https://doi.org/10.18331/BRJ2020.7.4.5

    Article  Google Scholar 

  2. Safaripour M, Ghanbari A, Seyedabadi E, Pourhashem G (2021) Investigation of environmental impacts of bioethanol production from wheat straw in Kermanshah, Iran. Biomass Convers Biorefinery. https://doi.org/10.1007/s13399-021-01676-7

  3. Jambo SA, Abdulla R, Mohd Azhar SH et al (2016) A review on third generation bioethanol feedstock. Renew Sustain Energy Rev 65:756–769. https://doi.org/10.1016/j.rser.2016.07.064

    Article  Google Scholar 

  4. Lennartsson PR, Erlandsson P, Taherzadeh MJ (2014) Integration of the first and second generation bioethanol processes and the importance of by-products. Bioresour Technol 165:3–8. https://doi.org/10.1016/j.biortech.2014.01.127

    Article  Google Scholar 

  5. Christiansen K, Raman DR, Hu G, Anex R (2018) First-order estimates of the costs, input-output energy analysis, and energy returns on investment of conventional and emerging biofuels feedstocks. Biofuel Res J 5:894–899. https://doi.org/10.18331/brj2018.5.4.4

    Article  Google Scholar 

  6. Yu HT, Chen BY, Li BY et al (2018) Efficient pretreatment of lignocellulosic biomass with high recovery of solid lignin and fermentable sugars using Fenton reaction in a mixed solvent. Biotechnol Biofuels 11:1–11. https://doi.org/10.1186/s13068-018-1288-4

    Article  Google Scholar 

  7. Haven MØ, Jørgensen H (2013) Adsorption of β-glucosidases in two commercial preparations onto pretreated biomass and lignin. Biotechnol Biofuels 6:1–14. https://doi.org/10.1186/1754-6834-6-165

    Article  Google Scholar 

  8. Bhagia S, Dhir R, Kumar R, Wyman CE (2018) Deactivation of cellulase at the air-liquid ınterface ıs the main cause of ıncomplete cellulose conversion at low enzyme loadings. Sci Rep 8:1–12. https://doi.org/10.1038/s41598-018-19848-3

    Article  Google Scholar 

  9. Luo X, Liu J, Zheng P et al (2019) Promoting enzymatic hydrolysis of lignocellulosic biomass by inexpensive soy protein. Biotechnol Biofuels 12:1–13. https://doi.org/10.1186/s13068-019-1387-x

    Article  Google Scholar 

  10. Walker GM, Basso TO (2020) Mitigating stress in industrial yeasts. Fungal Biol 124:387–397. https://doi.org/10.1016/j.funbio.2019.10.010

    Article  Google Scholar 

  11. Tse TJ, Wiens DJ (2021) Production of bioethanol—a review of factors affecting ethanol yield. Fermantation 7:1–18. https://doi.org/10.3390/fermentation7040268

    Article  Google Scholar 

  12. Koppram R, Tomás-Pejó E, Xiros C, Olsson L (2014) Lignocellulosic ethanol production at high-gravity: challenges and perspectives. Trends Biotechnol 32:46–53. https://doi.org/10.1016/j.tibtech.2013.10.003

    Article  Google Scholar 

  13. Ye G, Zeng D, Zhang S et al (2018) Ethanol production from mixtures of sugarcane bagasse and Dioscorea composita extracted residue with high solid loading. Bioresour Technol 257:23–29. https://doi.org/10.1016/j.biortech.2018.02.008

    Article  Google Scholar 

  14. Imran M, Khan H, Shah M et al (2010) Chemical composition and antioxidant activity of certain Morus species. J Zhejiang Univ Sci B 11:973–980. https://doi.org/10.1631/jzus.B1000173

    Article  Google Scholar 

  15. Minhas MA, Begum A, Hamid S et al (2016) Evaluation of antibiotic and antioxidant activity of morus nigra (black mulberry) extracts against soil borne, food borne and clinical human pathogens. Pak J Zool 48:1381–1388

    Google Scholar 

  16. Yuan Q, Zhao L (2017) The Mulberry (Morus alba L.) Fruit – a review of characteristic components and health benefits. J Agric Food Chem 65:10383–10394. https://doi.org/10.1021/acs.jafc.7b03614

    Article  Google Scholar 

  17. Aidynova R, Arslan N, Aydoğan MN (2020) Use of mulberry pomace as substrate for cıtrıc acıd productıon by Aspergillus niger MT-4. Trak Univ J Nat Sci 21:159–165. https://doi.org/10.23902/trkjnat.670859

    Article  Google Scholar 

  18. Baeyens J, Kang Q, Appels L et al (2015) Challenges and opportunities in improving the production of bio-ethanol. Prog Energy Combust Sci 47:60–88. https://doi.org/10.1016/j.pecs.2014.10.003

    Article  Google Scholar 

  19. Goshima T, Tsuji M, Inoue H et al (2013) Bioethanol production from lignocellulosic biomass by a novel Kluyveromyces marxianus strain. Biosci Biotechnol Biochem 77:1505–1510. https://doi.org/10.1271/bbb.130173

    Article  Google Scholar 

  20. Zaky AS, Greetham D, Tucker GA, Du C (2018) The establishment of a marine focused biorefinery for bioethanol production using seawater and a novel marine yeast strain. Sci Rep 8:1–14. https://doi.org/10.1038/s41598-018-30660-x

    Article  Google Scholar 

  21. Ben Atitallah I, Ntaikou I, Antonopoulou G et al (2020) Evaluation of the non-conventional yeast strain Wickerhamomyces anomalus (Pichia anomala) X19 for enhanced bioethanol production using date palm sap as renewable feedstock. Renew Energy 154:71–81. https://doi.org/10.1016/j.renene.2020.03.010

    Article  Google Scholar 

  22. Pramateftaki PV, Kouvelis VN, Lanaridis P, Typas MA (2006) The mitochondrial genome of the wine yeast Hanseniaspora uvarum: a unique genome organization among yeast/fungal counterparts. FEMS Yeast Res 6:77–90. https://doi.org/10.1111/j.1567-1364.2005.00018.x

    Article  Google Scholar 

  23. Pietrafesa A, Capece A, Pietrafesa R et al (2020) Saccharomyces cerevisiae and Hanseniaspora uvarum mixed starter cultures: ınfluence of microbial/physical interactions on wine characteristics. Yeast 37:609–621. https://doi.org/10.1002/yea.3506

    Article  Google Scholar 

  24. Matraxia M, Alfonzo A, Prestianni R et al (2021) Non-conventional yeasts from fermented honey by-products: focus on Hanseniaspora uvarum strains for craft beer production. Food Microbiol 99:103806. https://doi.org/10.1016/j.fm.2021.103806

    Article  Google Scholar 

  25. Barros EM, Rodrigues THS, Pinheiro ADT et al (2014) A yeast ısolated from cashew apple juice and ıts ability to produce first- and second-generation ethanol. Appl Biochem Biotechnol 174:2762–2776. https://doi.org/10.1007/s12010-014-1224-4

    Article  Google Scholar 

  26. Hong YA, Park HD (2013) Role of non-Saccharomyces yeasts in Korean wines produced from Campbell Early grapes: potential use of Hanseniaspora uvarum as a starter culture. Food Microbiol 34:207–214. https://doi.org/10.1016/j.fm.2012.12.011

    Article  Google Scholar 

  27. Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330. https://doi.org/10.1128/aem.61.4.1323-1330.1995

    Article  Google Scholar 

  28. Wistara NJ, Pelawi R, Fatriasari W (2016) The effect of lignin content and freeness of pulp on the bioethanol productivity of Jabon wood. Waste and Biomass Valorization 7:1141–1146. https://doi.org/10.1007/s12649-016-9510-8

    Article  Google Scholar 

  29. Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428. https://doi.org/10.1021/ac60147a030

    Article  Google Scholar 

  30. Aksu Z, Dönmez G (2000) The use of molasses in copper(II) containing wastewaters: effects on growth and copper(II) bioaccumulation properties of Kluyveromyces marxianus. Process Biochem 36:451–458. https://doi.org/10.1016/S0032-9592(00)00234-X

    Article  Google Scholar 

  31. Kim TH, Lee YY (2007) Pretreatment of corn stover by soaking in aqueous ammonia at moderate temperatures. Appl Biochem Biotechnol 136:81–82

    Google Scholar 

  32. Roca C, Olsson L (2003) Increasing ethanol productivity during xylose fermentation by cell recycling of recombinant Saccharomyces cerevisiae. Appl Microbiol Biotechnol 60:560–563. https://doi.org/10.1007/s00253-002-1147-9

    Article  Google Scholar 

  33. Günan Yücel H, Aksu Z (2015) Ethanol fermentation characteristics of Pichia stipitis yeast from sugar beet pulp hydrolysate: use of new detoxification methods. Fuel 158:793–799. https://doi.org/10.1016/j.fuel.2015.06.016

    Article  Google Scholar 

  34. Petravić-Tominac V, Zechner-Krpan V, Berković K et al (2011) Rheological properties, water-holding and oil-binding capacities of particulate β-glucans isolated from spent Brewer’s yeast by three different procedures. Food Technol Biotechnol 49:56–64

    Google Scholar 

  35. Jagtap SS, Rao CV (2018) Microbial conversion of xylose into useful bioproducts. Appl Microbiol Biotechnol 102:9015–9036. https://doi.org/10.1007/s00253-018-9294-9

    Article  Google Scholar 

  36. Langenberg A, Bink FJ, Wolff L et al (2017) Glycolytic functions are conserved in the genome of the wine yeast. Appl Environ Microbiol 83:1–20

    Article  Google Scholar 

  37. Thomson JM, Gaucher EA, Burgan MF et al (2005) Resurrecting ancestral alcohol dehydrogenases from yeast. Nat Genet 37:630–635. https://doi.org/10.1038/ng1553

    Article  Google Scholar 

  38. Raamsdonk LM, Diderich JA, Kuiper A et al (2002) Erratum: co-consumption of sugars or ethanol and glucose in a Saccharomyces cervisiae strain deleted in the HXK2 gene (Yeast (2001) vol. 18 (11) (1023-1033)). Yeast 19:183. https://doi.org/10.1002/yea.836

  39. de Moura Ferreira MA, da Silveira FA, da Silveira WB (2022) Ethanol stress responses in Kluyveromyces marxianus: current knowledge and perspectives. Appl Microbiol Biotechnol 106:1341–1353. https://doi.org/10.1007/s00253-022-11799-0

    Article  Google Scholar 

  40. Sanchez A, Hernández-Sánchez P, Puente R (2019) Hydration of lignocellulosic biomass. Modelling and experimental validation. Ind Crop Prod 131:70–77. https://doi.org/10.1016/j.indcrop.2019.01.029

    Article  Google Scholar 

  41. Phuttaro C, Sawatdeenarunat C, Surendra KC et al (2019) Anaerobic digestion of hydrothermally-pretreated lignocellulosic biomass: ınfluence of pretreatment temperatures, inhibitors and soluble organics on methane yield. Bioresour Technol 284:128–138. https://doi.org/10.1016/j.biortech.2019.03.114

    Article  Google Scholar 

  42. López-Linares JC, Romero I, Cara C et al (2014) Bioethanol production from rapeseed straw at high solids loading with different process configurations. Fuel 122:112–118. https://doi.org/10.1016/j.fuel.2014.01.024

    Article  Google Scholar 

  43. Sindhu R, Binod P, Pandey A (2016) A novel sono-assisted acid pretreatment of chili post harvest residue for bioethanol production. Bioresour Technol 213:58–63. https://doi.org/10.1016/j.biortech.2016.02.079

    Article  Google Scholar 

  44. Germec M, Demirel F, Tas N et al (2017) Microwave-assisted dilute acid pretreatment of different agricultural bioresources for fermentable sugar production. Cellulose 24:4337–4353. https://doi.org/10.1007/s10570-017-1408-5

    Article  Google Scholar 

  45. Mohd Zakria R, Gimbun J, Asras MFF, Chua GK (2017) Magnesium sulphate and Β-alanine enhanced the ability of Kluyveromyces marxianus producing bioethanol using oil palm trunk sap. Biofuels 8:595–603. https://doi.org/10.1080/17597269.2016.1242690

    Article  Google Scholar 

  46. Slininger PJ, Dien BS, Gorsich SW, Liu ZL (2006) Nitrogen source and mineral optimization enhance D-xylose conversion to ethanol by the yeast Pichia stipitis NRRL Y-7124. Appl Microbiol Biotechnol 72:1285–1296. https://doi.org/10.1007/s00253-006-0435-1

    Article  Google Scholar 

  47. Hu K, Jin GJ, Xu YH et al (2019) Enhancing wine ester biosynthesis in mixed Hanseniaspora uvarum/Saccharomyces cerevisiae fermentation by nitrogen nutrient addition. Food Res Int 123:559–566. https://doi.org/10.1016/j.foodres.2019.05.030

    Article  Google Scholar 

  48. Liu R, Li J, Shen F (2008) Refining bioethanol from stalk juice of sweet sorghum by immobilized yeast fermentation. Renew Energy 33:1130–1135. https://doi.org/10.1016/j.renene.2007.05.046

    Article  Google Scholar 

  49. Shahirah MNN, Gimbun J, Pang SF et al (2015) Influence of nutrient addition on the bioethanol yield from oil palm trunk sap fermented by Saccharomyces cerevisiae. J Ind Eng Chem 23:213–217. https://doi.org/10.1016/j.jiec.2014.08.018

    Article  Google Scholar 

  50. Birch RM, Walker GM (2000) Influence of magnesium ions on heat shock and ethanol stress responses of Saccharomyces cerevisiae. Enzyme Microb Technol 26:678–687. https://doi.org/10.1016/S0141-0229(00)00159-9

    Article  Google Scholar 

  51. Demiray E, Kut A, Ertuğrul Karatay S, Dönmez G (2021) Usage of soluble soy protein on enzymatically hydrolysis of apple pomace for cost-efficient bioethanol production. Fuel 289:1–9. https://doi.org/10.1016/j.fuel.2020.119785

    Article  Google Scholar 

  52. Lee I, Yu JH (2020) The production of fermentable sugar and bioethanol from acacia wood by optimizing dilute sulfuric acid pretreatment and post treatment. Fuel 275:117943. https://doi.org/10.1016/j.fuel.2020.117943

    Article  Google Scholar 

Download references

Funding

This study was supported by the Ankara University Research Foundation. Project Number: 21L0430012.

Author information

Authors and Affiliations

  1. Biology Department, Science Faculty, Ankara University, 06100, Beşevler, Ankara, Turkey

    Hüseyin Kaan Kabadayı, Sevgi Ertuğrul Karatay & Gönül Dönmez

  2. Medical Laboratory Techniques Department, Health Services Vocational High School, Ankara Yıldırım Beyazıt University, Ankara, 06760, Çubuk, Turkey

    Ekin Demiray

Authors
  1. Hüseyin Kaan Kabadayı
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ekin Demiray
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sevgi Ertuğrul Karatay
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gönül Dönmez
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Hüseyin Kaan Kabadayı conducted the experiments. Ekin Demiray conducted the experiments and wrote the original draft. Sevgi Ertuğrul Karatay conceived and designed research, reviewed and edited the manuscript, and provided funding. Gönül Dönmez provided funding.

Corresponding author

Correspondence to Sevgi Ertuğrul Karatay.

Ethics declarations

Ethical approval

Not applicable.

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.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) 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

Kabadayı, H.K., Demiray, E., Karatay, S.E. et al. Bioethanol production from mulberry pomace by newly ısolated non-conventional yeast Hanseniaspora uvarum. Biomass Conv. Bioref. 14, 10611–10620 (2024). https://doi.org/10.1007/s13399-023-04340-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13399-023-04340-4

Keywords

Search

Navigation