Skip to main content
Log in

Valorization of apple pomace using bio-based technology for the production of xylitol and 2G ethanol

  • Research Paper
  • Published:
Bioprocess and Biosystems Engineering Aims and scope Submit manuscript

Abstract

Apple pomace was studied as a raw material for the production of xylitol and 2G ethanol, since this agroindustrial residue has a high concentration of carbohydrate macromolecules, but is still poorly studied for the production of fermentation bioproducts, such as polyols. The dry biomass was subjected to dilute-acid hydrolysis with H2SO4 to obtain the hemicellulosic hydrolysate, which was concentrated, detoxified and fermented. The hydrolyzate after characterization was submitted to submerged fermentations, which were carried out in Erlenmeyer flasks using, separately, the yeasts Candida guilliermondii and Kluyveromyces marxianus. High cellulose (32.62%) and hemicellulose (23.60%) contents were found in this biomass, and the chemical hydrolysis yielded appreciable quantities of fermentable sugars, especially xylose. Both yeasts were able to metabolize xylose, but Candida guilliermondii produced only xylitol (9.35 g L−1 in 96 h), while K. marxianus produced ethanol as the main product (10.47 g L−1 in 24 h) and xylitol as byproduct (9.10 g L−1 xylitol in 96 h). Maximum activities of xylose reductase and xylitol dehydrogenase were verified after 24 h of fermentation with C. guilliermondii (0.23 and 0.53 U/mgprot, respectively) and with K. marxianus (0.08 e 0.08 U/mgprot, respectively). Apple pomace has shown potential as a raw material for the fermentation process, and the development of a biotechnological platform for the integrated use of both the hemicellulosic and cellulosic fraction could add value to this residue and the apple production chain.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Vendruscolo F, Ribeiro CS, Espósito E, Ninow JL (2009) Tratamento biológico do bagaço de maçã e adição em dietas para alevinos. Rev Bras Eng Agric Ambient 13(4):487–493

    Google Scholar 

  2. Bai X, Ren H (2013) Antioxidant activity and HPLC analysis of polyphenol enriched extracts from industrial apple pomace. J Sci Food Agric 93(10):2502–2506

    CAS  PubMed  Google Scholar 

  3. Waghmare AG, Shalini SA (2013) Use of fruit by-products in the preparation of hypoglycemic thepla: Indian unleavened vegetable flat bread. J Food Process Preserv 38(3):1–9

    Google Scholar 

  4. Madrera RR, Bedriñana RP, Hevia AG, Arce MB, Valles BS (2013) Production of spirits from dry apple pomace and selected yeasts. Food Bioprod Process 91(4):623–631

    Google Scholar 

  5. Walia A, Mehta P, Chauhan A, Shircot CK (2013) Production of alkalophilic xylanases by Paenibacillus polymyxa CKWX1 isolated from decomposing wood. Proc Natl Acad Sci India Sect B Biol Sci 83(2):215–223

    CAS  Google Scholar 

  6. Walia A, Mehta P, Chauhan A, Shircot CK (2013) Optimization of cellulase-free xylanase production by alkaholic Cellulosimicrobium sp. CKMX1 in solid-state fermentation of apple pomace using central composite design and response surface methodology. Ann Microbiol 63(1):187–198

    CAS  Google Scholar 

  7. Yin JS, Liang KL, Li DM, Sun ZT (2013) Optimization of production conditions for β-mannanase using apple pomace as raw material in solid-state fermentation. Ann Microbiol 63(1):101–108

    CAS  Google Scholar 

  8. Hijosa-Valsero M, Paniagua-García AI, Díez-Antolínez R (2017) Biobutanol production from apple pomace: the importance of pretreatment methods on the fermentability of lignocellulosic agro-food wastes. Appl Microbiol Biotechnol 101(21):8041–8052

    CAS  PubMed  Google Scholar 

  9. Grigoras CG, Destandau E, Fougère L, Elfakir C (2013) Evaluation of apple pomace extracts as a source of bioactive compounds. Ind Crops Prod 49:794–804

    CAS  Google Scholar 

  10. Parra AFR, Sahagún M, Ribotta PD, Ferrero C, Gómez M (2019) Particle size and hydration properties of dried apple pomace: effect on dough viscoelasticity and quality of sugar-Snap cookies. Food Bioprocess Technol 12(7):1–10

    Google Scholar 

  11. Cunha MAA, Converti A, Santos JC, Silva SS (2006) Yeast immobilization in LentiKats®: a new strategy for xylitol bioproduction from sugarcane bagasse. World J Microbiol Biotechnol 22(1):65–72

    Google Scholar 

  12. Alcázar-Alay SC, Cardenas-Toro FP, Santos DT, Meireles MA (2015) Study of an extraction process as the pretreatment step for sugar production from acid hydrolysis. Food Public Health 5(2):47–55

    Google Scholar 

  13. Hernandez-Perez AF, Chaves-Villamil AC, Arruda PV, Santos JC, Felipe MGA (2019) Sugarcane syrup improves xylitol bioproduction from sugarcane bagasse and straw hemicellulosic hydrolysate. Waste Biomass Valoriz. https://doi.org/10.1007/s12649-019-00742-6

    Article  Google Scholar 

  14. Hernandez-Perez AF, Arruda PV, Sene L, Silva SS, Chandel AK, Felipe MGA (2019) Xylitol bioproduction: state-of-the-art, industrial paradigm shift, and opportunities for integrated biorefineries. Crit Rev Biotechnol. https://doi.org/10.1080/07388551.2019.1640658

    Article  Google Scholar 

  15. Webb SR, Lee H (1992) Characterization of xylose reductase from yeast Pichia stipitis: evidence for functional thiol and histidyl groups. J Gen Microbiol 138(9):1857–1863

    CAS  Google Scholar 

  16. Yablochkova EN, Bolotnikova OI, Mikhailova NP (2003) The activity of xylose reductase and xylitol dehydrogenase in yeasts. Microbiology 72(4):414–417

    CAS  Google Scholar 

  17. Papon N, Savine V, Lanoue A, Simkin AJ, Chrèche J, Giglioli-Guivarc’h N, Clastre M, Courdavault V, Sibirny AA (2013) Candida guilliermondii: biotechnological applications perspectives for biological control, emerging clinical importance and recent advances in genetics. Curr Genet 59(3):73–90

    CAS  PubMed  Google Scholar 

  18. Silva DDV, Arruda PV, Vicente FMCF, Sene L, Silva SS, Felipe MGA (2015) Evaluation of fermentative potential of Kluyveromyces marxianus ATCC 36907 in cellulosic and hemicellulosic sugarcane bagasse hydrolysates on xylitol and ethanol production. Ann Microbiol 65(2):687–694

    Google Scholar 

  19. Lorente B, Malpertuy A, Blandin G, Artiguenave F, Wincker P, Dujon B (2000) Genomic exploration of the hemiascomycetous yeasts: 12. Kluyveromyces marxianus var. marxianus. FEBS Lett 487(1):71–75

    Google Scholar 

  20. Banat IM, Nigam P, Marchant R (1992) Isolation of thermotolerant, fermentative yeasts growing at 52 °C and producing ethanol at 45 °C and 50 °C. World J Microbiol Biotechnol 8(3):259–263

    CAS  PubMed  Google Scholar 

  21. Wilkins MR, Muller M, Eichling R, Banat IM (2008) Fermentation of xylose by the thermotolerant yeast strains Kluyveromyces marxianus IMB2, IMB4, and IMB5 under anaerobic conditions. Process Biochem 43:346–350

    CAS  Google Scholar 

  22. Matsuzak C, Nakagawa A, Koyanagi T, Tanaka K, Minami H, Tamaki H, Katayama T, Yamamoto K, Kumagai H (2012) Kluyveromyces marxianus—based platform for direct ethanol fermentation and recovery from cellulosic materials under air-ventilated conditions. J Biosci Bioeng 113(5):604–607

    Google Scholar 

  23. Kanwar S, Kumar G, Sahgal M, Singh A (2012) Ethanol production through Saccharomyces based fermentation using apple pomace amended with molasses. Sugar Tech 14(3):304–311

    CAS  Google Scholar 

  24. Mahawar MK, Singh A, Kumbhar BK, Sehgal M (2013) Optimization of ethanol production from apple pomace through solid-state fermentation using enzymes and yeasts combination through response surface methodology. Afr J Agric Res 8(24):3136–3145

    Google Scholar 

  25. Rodrigues THS, Rocha MVP, Macedo GR, Gonçalves LRB (2011) Ethanol production from cashew apple bagasse: improvement of enzymatic hydrolysis by microwave-assisted alkali pretreatment. Appl Biochem Biotechnol 164(6):929–943

    CAS  PubMed  Google Scholar 

  26. Parmar I, Rupasinghe HPV (2013) Bio-conversion of apple pomace into ethanol and acetic acid: enzymatic hydrolysis and fermentation. Biores Technol 130:613–620

    CAS  Google Scholar 

  27. Gama R, Van Dijk JS, Pletschke BI (2015) Optimization of enzymatic hydrolysis of apple pomace for production of biofuel and biorefinery chemicals using commercial enzymes. 3Biotech 5(6):1075–1087

    Google Scholar 

  28. Rocha GFM, Silva FT, Curvelo AAS, Araujo GT (1997) A fast and accurate method for determination of cellulose and polyoses by HPLC. In: Brazilian symposium on the chemistry of lignins and other wood components, Curitiba, Brazil, 31 August to 5 September 1997

  29. Gouveia ER, Nascimento RT, Souto-Maior AM, Rocha GJM (2009) Validação de metodologia para a caracterização química do bagaço de cana-de-açúcar. Quím Nova 32(6):1500–1503

    CAS  Google Scholar 

  30. Pessoa Júnior A, Mancilha IM, Sato S (1997) Acid hydrolysis of hemicellulose from surgarcane bagasse. Braz J Chem Eng 14(3):291–297

    Google Scholar 

  31. Marton JM, Felipe MGA, Almeida e Silva JB, Pessoa A Jr (2006) Evaluation of the activated charcoals and adsorption conditions used in the treatment of sugarcane bagasse hydrolysate for xylitol production. Braz J Chem Eng 23(1):9–21

    CAS  Google Scholar 

  32. Felipe MGA, Vitolo M, Mancilha IM, Silva SS (1997) Environmental parameters affecting xylitol production from sugarcane bagasse hemicellulosic hydrolyzate by Candida guilliermondii. J Ind Microbiol Biotechnol 18(4):251–254

    CAS  Google Scholar 

  33. Gurpilhares DB, Hasmann FA, Pessoa A Jr, Roberto IC (2009) The behavior of key enzymes of xylose metabolism on the xylitol production by Candida guilliermondii grown in hemicellulosic hydrolysate. J Ind Microbiol Biotechnol 36(1):87–93

    CAS  PubMed  Google Scholar 

  34. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254

    CAS  Google Scholar 

  35. Melikoğlu AY, Bilek SE, Cesur S (2019) Optimum alkaline treatment parameters for the extraction of cellulose and production of cellulose nanocrystals from apple pomace. Carbohyd Polym 215(1):330–337

    Google Scholar 

  36. Guerrero MRB, da Silva PMM, Zaragoza MM, Gutiérrez JS, Velderrain VG, Ortiz AL, Collins-Martínez V (2014) Thermogravimetric study on the pyrolysis kinetics of apple pomace as waste biomass. Int J Hydrog Energy 39(29):16619–16627

    CAS  Google Scholar 

  37. Moraes EJC, Silva DDV, Dussán KJ, Tesche LZ, Silva JBA, Rai M, Felipe MGA (2018) Xylitol-sweetener production from barley straw: optimization of acid hydrolysis condition with the energy consumption simulation. Waste Biomass Valoriz. https://doi.org/10.1007/s12649-018-0501-9

    Article  Google Scholar 

  38. Manaf SFA, Jahim JM, Harum S, Luthfi AAI (2018) Fractionation of oil palm fronds (OPF) hemicellulose using dilute nitric acid for fermentative production of xylitol. Ind Crops Prod 115:6–15

    Google Scholar 

  39. Santana NB, Teixeira Dias JCT, Rezende RP, Franco M, Oliveira LKS, Souza LO (2018) Production of xylitol and bio-detoxification of cocoa pod husk hemicellulose hydrolysate by Candida boidinii XM02G. PLoS ONE 13(4):11–15

    Google Scholar 

  40. Hernandez-Perez AF, Arruda PV, Felipe MGA (2016) Sugarcane straw as a feedstock for xylitol production by Candida guilliermondii FTI 20037. Braz J Microbiol 47(2):489–496

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Albuquerque TL, Gomes SDL, Marques Júnior JE, Silva Júnior IJS, Rocha MVP (2015) Xylitol production from cashew apple bagasse by Kluyveromyces marxianus CCA510. Catal Today 255:33–40

    Google Scholar 

  42. Camargo D, Sene L, Variz DI, Felipe MGA (2015) Xylitol bioproduction in hemicellulosic hydrolysate obtained from sorghum forage biomass. Appl Biochem Biotechnol 175(8):3628–3642

    CAS  PubMed  Google Scholar 

  43. Camargo D, Sene L (2014) Production of ethanol from the hemicellulosic fraction of sunflower meal biomass. Biomass Convers Biorefinery 4(2):87–93

    CAS  Google Scholar 

  44. Canilha L, Carvalho W, Almeida e Silva JB (2006) Xylitol bioproduction from wheat straw: hemicellulose hydrolysis and hydrolyzate fermentation. J Sci Food Agric 86(9):1371–1376

    CAS  Google Scholar 

  45. Mussatto SI, Roberto IC (2004) Optimal experimental conditions for hemicellulosic hydrolyzate treatment with activated charcoal for xylitol production. Biotechnol Prog 20(1):134–139

    CAS  PubMed  Google Scholar 

  46. Santos JC, Antunes FAF, Cunha MAA, Milessi TSS, Dussán KJ, Silva DDV, Silva SS (2016) Biomass pretreatment with oxalic acid for value-added products. In: Mussatto SI (ed) Biomass fractionation technologies for a lignocellulosic feedstock based biorefinery. Elsevier, Amsterdam, pp 187–208

    Google Scholar 

  47. Sene L, Arruda PV, Oliveira SMM, Felipe MGA (2011) Evaluation of sorghum straw hemicellulosic hydrolysate for biotechnological production of xylitol by Candida guilliermondii. Braz J Microbiol 42:1141–1146

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Santos JC, Marton JM, Felipe MGA (2014) Continuous system of combined columns of ion exchange resins and activated charcoal as a new approach for the removal of toxics from sugarcane bagasse hemicellulosic hydrolysate. Ind Eng Chem Res 53:16494–16501

    CAS  Google Scholar 

  49. Chaud LCS, Arruda PV, Sene L, Felipe MGA (2010) Comparison of detoxification methodologies for sugarcane bagasse hemicellulosic hydrolysate based on active charcoal and vegetal polymer aiming at biotechnological xylitol production. J Biotechnol 150(S):S365

    Google Scholar 

  50. Converti A, Perego P, Torre P, Silva SS (2000) Mixed inhibitions by methanol, furfural and acetic acid in xylitol production by Candida guilliermondii. Biotech Lett 22(23):1861–1865

    CAS  Google Scholar 

  51. Mussatto SI, Dragone G, Roberto IC (2005) Influence of the toxic compounds present in brewer’s spent grain hemicellulosic hydrolysate on xylose—to—xylitol bioconversion by Candida guilliermondii. Process Biochem 40:3801–3806

    CAS  Google Scholar 

  52. Oliva JM, Sáez F, Ballesteros I, González A, Negro MJ, Manzanares P, Ballesteros M (2003) Effect of lignocellulosic degradation compounds from steam explosion pretreatment on ethanol fermentation by thermotolerant yeast Kluyveromyces marxianus. Appl Biochem Biotechnol 105(1–3):141–153

    PubMed  Google Scholar 

  53. Sanchez B, Bautista J (1988) Effects of furfural and 5-hydroxymethylfurfural on the fermentation of Saccharomyces cerevisiae and biomass production from Candida guilliermondii. Enzym Microb Technol 10(5):315–318

    CAS  Google Scholar 

  54. Silva DDV, Felipe MGA (2006) Effect of glucose:xylose ratio on xylose reductase and xylitol dehydrogenase activities from Candida guilliermondii in sugarcane bagasse hydrolysate. J Chem Technol Biotechnol 81(7):1294–1300

    Google Scholar 

  55. Arruda PV, Santos JC, Rodrigues RCLB, Silva DDV, Yamakawa CK, Rocha GJM, Nolasco J Jr, Pradella JGC, Rossell CEV, Felipe MGA (2017) Scale up of xylitol production from sugarcane bagasse hemicellulosic hydrolysate by Candida guilliermondii FTI 20037. J Ind Eng Chem 47:297–302

    Google Scholar 

  56. Signori L, Passolunghi S, Ruohonen L, Porro D, Branduardi P (2014) Effect of oxygenation and temperature on glucose-xylose fermentation in Kluyveromyces marxianus CBS712 strain. Microb Cell Fact 13(1):51. https://doi.org/10.1186/1475-2859-13-51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Fonseca GG, Carvalho NMB, Gombert AK (2013) Growth of the yeast Kluyveromyces marxianus CBS6556 on different sugar combinations as sole carbon and energy source. Appl Microb Cell Physiol 97(11):5055–5067

    CAS  Google Scholar 

  58. Tavares B, Felipe MGA, Santos JC, Pereira FM, Gomes SD, Sene L (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

    CAS  Google Scholar 

  59. Flores CL, Rodriguez C, Petit T, Gancedo C (2000) Carbohydrate and energy-yielding in non-conventional yeast. FEMS Microbiol Rev 24(4):507–529

    CAS  PubMed  Google Scholar 

  60. Rouhollah H, Iraj N, Giti E, Sorah A (2007) Mixed sugar fermentation by Pichia stipitis, Saccharomyces cerevisiae and an isolated xylose-fermenting Kluyveromyces marxianus and their cocultures. Afr J Biotech 6(9):1110–1114

    CAS  Google Scholar 

  61. Rodrussamee N, Lertwattanasakul N, Hirata K, Suprayogi LS, Kosaka T, Yamada M (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(4):1573–1576

    CAS  PubMed  Google Scholar 

  62. Arruda PV, Rodrigues RDCLB, Silva DDV, Felipe MGDA (2011) Evaluation of hexose and pentose in pre-cultivation of Candida guilliermondii on the key enzymes for xylitol production in sugarcane hemicellulosic hydrolysate. Biodegradation 22(4):815–822

    CAS  PubMed  Google Scholar 

  63. Zhang B, Zhang L, Wang D, Gao X, Hong J (2011) Identification of a xylose reductase gene in the xylose metabolic pathway of Kluyveromyces marxianus NBRC1777. J Ind Microbiol Biotechnol 38(12):2001–2010

    CAS  PubMed  Google Scholar 

  64. Nitiyon S, Keo-Oudone C, Murata M, Lertwattanasakul N, Limtong S, Kosaka T, Yamada M (2016) Efficient conversion of xylose to ethanol by stress-tolerant Kluyveromyces marxianus BUNL-21. SpringerPlus 5:185

    PubMed  PubMed Central  Google Scholar 

  65. Lee H, Sopher CR, Yau KYF (1996) Induction of xylose reductase and xylitol dehydrogenase activities on mixed sugars in Candida guilliermondii. J Chem Technol Biotechnol 65(4):375–379

    CAS  Google Scholar 

  66. Lima LH, Felipe MGA, Vitolo M, Torres FA (2004) Effect of acetic acid present in bagasse hydrolysate on the activities of xylose reductase and xylitol dehydrogenase in Candida guilliermondii. Appl Microbiol Biotechnol 65(6):734–738

    CAS  PubMed  Google Scholar 

  67. Kwon DH, Park JB, Hong E, Ha S-J (2019) Ethanol production from xylose is highly increased by the Kluyveromyces marxianus mutant 17694-DH1. Bioprocess Biosyst Eng 42(1):63–70

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Coordenação de Aperfeiçoamento de Pessoal de Nível superior (CAPES) and Fischer S/A Agroindustria.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maria das Graças de Almeida Felipe.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00449-020-02401-w

Keywords

Navigation