Abstract
Second generation ethanol has the prospect of becoming an important bioenergy alternative. The development of this technology is associated with the lignocellulosic materials' use, with emphasis on agricultural and agroindustrial by-products from which fermentable sugar can be produced. The acid hydrolysis depolymerizes the hemicellulose releasing mainly xylose. Subsequently, the cellulose can be converted into glucose by enzymatic hydrolysis. However, the acid hydrolysis produces toxic compounds, such as furan derivatives, phenolics, and organic acids, which are harmful to fermentative microorganisms. This study investigated different acid concentrations in the sulfuric acid hydrolysis of sugarcane bagasse (1– 5% m/v) and the use of adsorbents with the prerogative to improve the acid hydrolysate (AH) quality for microbial ethanolic fermentation. Cell growth and fermentative yield of Saccharomyces cerevisiae (PE-2) and Scheffersomyces stipitis (NRRL Y-7124) were evaluated. AH was used as a source of pentoses (17.7 g L−1) and molasses (ME) sugarcane as source of hexoses (47 g L−1). The following adsorbents were used: activated charcoal, clay, hydrotalcite and active and inactive cells of PE-2 and NRRL Y-7124, at concentrations ranging (1 – 8% m/v). Results of cell growth and chemical characterization allowed to select the most effective adsorbents with emphasis for active cells that removed 66% furfural and 51% 5-(hydroxymethyl) furfural) (5-HMF) and alcoholic productivity of 23.5 g L−1 in AH and ME substrates, in the presence of mixed culture. These results indicate the application of active yeast cells in the detoxification of acid hydrolysates of the sugarcane bagasse previously to the fermentation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aditiya HB, Mahlia TMI, Chong WT, Nur H, Sebayang AH (2016) Second generation bioethanol production: a critical review. Renew Sust Energy Rev 66:631–653. https://doi.org/10.1016/j.rser.2016.07.015
Almeida JRM, Modig T, Petersson A, Hägerdal BH, Lidén G, Gorwa-Grauslund MF (2007) Increased tolerance and conversion of inhibitors in lignocellulosic hydrolysates by Saccharomyces cerevisiae—mini-review. J Chem Technol Biotechnol 82:340–349. https://doi.org/10.1002/jctb.1676
Alvarez PA, Filho RM, Tovara LP, Maciel MRW (2015) Kinetics of the acid hydrolysis of sugarcane bagasse using different milling size, high solid load and low pretreatment temperature. Chem Eng Trans 43:625–630. https://doi.org/10.3303/CET1543105
Antunes FAF, Santos JC, Chandel AK, Milessi TSS, Peres GFD, da Silva SS (2016) Hemicellulosic ethanol production by immobilized wild Brazilian yeast Scheffersomyces shehatae UFMG-HM 52.2: effects of cell concentration and stirring rate. Curr Microbiol 72:133–138. https://doi.org/10.1007/s00284-015-0923-6
Antunes FAF, Chandel AK, Santos JC, Lacerda TM, Dussán KJM, Silva DDV, Tagliaferro GV, Milessi TSS, Marcelino PRF, Brumano LP, Terán-Hilares R, Silvio SS (2018) Bioethanol: An overview of production possibilities. In: M Brienzo (ed) Bioethanol and beyond—advances in production process and future directions. Nova Science Publishers, Inc. ISBN: 978-1-53613-478-0.
Brienzo M, Ferreira S, Vicentim MP, Souza W, Sant’Anna C (2014) Comparison study on the biomass recalcitrance of different tissue fractions of sugarcane culm. Bioenergy Res 7:1454–1465. https://doi.org/10.1007/s12155-014-9487-8
Brienzo M, Abud Y, Ferreira S, Corrales RCNR, Ferreira-Leitão VS, Souza W, Sant’Anna C (2016) Characterization of anatomy, lignin distribution, and response to pretreatments of sugarcane culm node and internode. Ind Crop Prod 84:305–313. https://doi.org/10.1016/j.indcrop.2016.01.039
Canilha L, Carvalho W, Giulietti M, Felipe MDGA, Almeida e Silva JB, Giulietti M (2010) Ethanol production from sugarcane bagasse hydrolysate using Pichia stipitis. Appl Biochem Biotechnol 161:84–92. https://doi.org/10.1007/s12010-009-8792-8
Chandel AK, Chandrasekhar G, Radhika K, Ravinder R, Ravindra R (2011a) Bioconversion of pentose sugars into ethanol: A review and future directions. Biotechnol Mol Biol Rev 6(1):008–020
Chandel AK, Silva SS, Singh Om V (2011b) Detoxification of Lignocellulosic Hydrolysates for Improved Bioethanol Production. In: Bernardes MAS (ed) Biofuel production—recent developments and prospects. InTech Open, pp 225–246. https://doi.org/10.5772/16454
Chandel AK, Kapoor RK, Singh A, Kuhad RC (2007) Detoxification of sugarcane bagasse hydrolysate improves ethanol production by Candida shehatae NCIM 3501. Bioresour Technol 98:1947–1950. https://doi.org/10.1016/j.biortech.2006.07.047
CONAB – Companhia Nacional de Abastecimento (2019) Acomp. safra bras. cana, v. 5 - Safra 2018/19, n. 4 - Quarto levantamento, Brasília, p. 1–75.
Delgenes JP, Laplace JM, Moletta R, Navarro JM (1996) Comparative study of separated fermentations and cofermentation processes to produce ethanol from hardwood derived hydrolyzates. Biomass Bioenergy 11(4):353–360. https://doi.org/10.1016/0961-9534(96)00019-0
Dilarri G, Almeida EJR, Pecora HB, Corso CR (2016) Removal of Dye Toxicity from an Aqueous Solution Using an Industrial Strain of Saccharomyces cerevisiae (Meyen). Water Air Soil Pollut 227:269. https://doi.org/10.1007/s11270-016-2973-1
Dussán KJ, Silva DDV, Perez VH, Silva SS (2016) Evaluation of oxygen availability on ethanol production from sugarcane bagasse hydrolysate in a batch bioreactor using two strains of xylose-fermenting yeast. Renew Energy 87:703–710. https://doi.org/10.1016/j.renene.2015.10.065
Ferreira JM, Honorato da Silva FL, Alsina OLS, Oliveira CLS, Cavalcanti EB, Gomes WC (2007) Estudo do equilíbrio e cinética da biossorção do Pb2+ por Saccharomyces cerevisiae. Quim Nov 30(5):1188–1193. https://doi.org/10.1590/S0100-40422007000500026
Ferreira AD, Mussatto SI, Cadete RM, Rosa CA, Silva SS (2011) Ethanol production by a new pentose-fermenting yeast strain, Scheffersomyces stipitis UFMG-IMH 43.2, isolated from the Brazilian forest. Yeast 28:547–554. https://doi.org/10.1002/yea.1858
Fonseca BG, Moutta RO, Ferraz FO, Vieira ER, Nogueira AS, Baratella BF, Rodrigues LC, Hou-Rui Z, da Silva SS (2011) Biological detoxification of different hemicellulosic hydrolysates using Issatchenkia occidentalis CCTCC M 206097 yeast. J Ind Microbiol Biotechnol 38:199–207. https://doi.org/10.1007/s10295-010-0845-z
Fu Z, Holtzapple MT (2010) Anaerobic mixed-culture fermentation of aqueous ammonia-treated sugarcane bagasse in consolidated bioprocessing. Biotechnol Bioeng 106(2):216–227. https://doi.org/10.1002/bit.22679
Gírio FM, Fonseca C, Carvalheiro F, Duarte LC, Marques S, Bogel-Łukasik R (2010) Hemicelluloses for fuel ethanol: a review. Bioresour Technol 101:4775–4800. https://doi.org/10.1016/j.biortech.2010.01.088
Gombert AK, van Maris AJA (2015) Improving conversion yield of fermentable sugars into fuel ethanol in 1st generation yeast-based production processes. Curr Opin Biotechnol 33:81–86. https://doi.org/10.1016/j.copbio.2014.12.012
Gomes AC, Rodrigues MI, Passos DF, Castro AM, Santa Anna LMM, Pereira N Jr (2019) Acetone–butanol–ethanol fesrmentation from sugarcane bagasse hydrolysates: Utilization of C5 and C6 sugars. Electron J Biotechnol 42:16–22. https://doi.org/10.1016/j.ejbt.2019.10.004
Gutiérrez-Rivera B, Waliszewski-Kubiak K, Carvajal-Zarrabal O, Aguilar-Uscanga MG (2012) Conversion efficiency of glucose/xylose mixtures for ethanol production using Saccharomyces cerevisiae ITV01 and Pichia stipitis NRRL Y-7124. J Chem Technol Biotechnol 87:263–270. https://doi.org/10.1002/jctb.2709
Gutiérrez-Rivera B, Ortiz-Muniz B, Gómez-Rodríguez J, Cárdenas-Cagal A, González JMD, Aguilar-Uscanga MG (2015) Bioethanol production from hydrolyzed sugarcane bagasse supplemented with molasses “B” in a mixed yeast culture. Renew Energy 74:399–405. https://doi.org/10.1016/j.renene.2014.08.030
Gupta R, Hemansia GS, Shukla R, Kuhada RC (2017) Study of charcoal detoxification of acid hydrolysate from corncob and its fermentation to xylitol. J Environ Chem Eng 5:4573–4582. https://doi.org/10.1016/j.jece.2017.07.073
Hammer Ø, Harper DAT, Ryan DT (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):9
Hernández-Pérez AF, de Arruda PF, Almeida Felipe MG (2016) Sugarcane straw as a feedstock for xylitol production by Candida guilliermondii FTI 20037. Braz J Microbiol 47:489–496
Jönsson LJ, Alriksson B, Nilvebrant N (2013) Bioconversion of lignocellulose: inhibitors and detoxification. Biotechnol Biofuels 6:16. https://doi.org/10.1186/1754-6834-6-16
Jönsson LJ, Martín C (2016) Pretreatment of lignocellulose: formation of inhibitory by-products and strategies for minimizing their effects. Bioresour Technol 199:103–112. https://doi.org/10.1016/j.biortech.2015.10.009
Kahar P, Taku K, Tanaka S (2011) Enhancement of xylose uptake in 2-deoxyglucose tolerant mutant of Saccharomyces cerevisiae. J Biosci Bioeng 111(5):557–563. https://doi.org/10.1016/j.jbiosc.2010.12.020
Klasson T, Dien BS, Hector RE (2013) Simultaneous detoxification, saccharification, and ethanol fermentation of weak-acid hydrolyzates. Ind Crop Prod 49:292–298. https://doi.org/10.1016/j.indcrop.2013.04.059
Kumar AK, Sharma S (2017) Recent updates on different methods of pretreatment of lignocellulosic feed stocks: a review. Bioresour Bioprocess 4:7. https://doi.org/10.1186/s40643-017-0137-9
Lee H, Fischer BG (1990) Unusual fructose utilization by Pichia stipitis and its potential application. J Ferment Bioeng 69(2):79–82. https://doi.org/10.1016/0922-338X(90)90191-X
Lee H, Biely P, Latta RK, Barbosa MFS, Schneider H (1986) Utilization of xylan by yeasts and its conversion to ethanol by Pichia stipitis strains. Appl Environ Microbiol 52:320–324
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
Martini C, Tauk-Tornisielo SM, Codato CB, Bastos RG, Ceccato-Antonini SR (2016) A strain of Meyerozyma guilliermondii isolated from sugarcane juice is able to grow and ferment pentoses in synthetic and bagasse hydrolysate media. World J Microbiol Biotechnol 32:80. https://doi.org/10.1007/s11274-016-2036-1
Meyrial V, Delgenes JP, Romieu C, Moletta R, Gounot AM (1995) Ethanol tolerance and activity of plasma membrane ATPase in Pichia stipitis grown on D-xylose or on D-glucose. Enzyme Microbial Technol 17:535–540. https://doi.org/10.1016/0141-0229(94)00065-Y
Milanez AY, Nyko D, Valente MS, Sousa LC, Bonomi AMFLJ, Jesus CDF, Watanabe MDB, Chagas MF, Rezende MCAF, Cavalett O, Junqueira TL, Gouvêia VLR (2015) De promessa a realidade: como o etanol celulósico pode revolucionar a indústria da cana-de-açúcar: uma avaliação do potencial competitivo e sugestões de política pública. BNDES Setorial. Rio de Janeiro n 41:237–294
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428. https://doi.org/10.1021/ac60147a030
Mitter EK, Corso CR (2013) FT-IR analysis of acid black dye biodegradation using Saccharomyces cerevisiae immobilized with treated sugarcane bagasse. Water Air Soil Pollut 224:1607. https://doi.org/10.1007/s11270-013-1607-0
Mussato SI, Roberto JC (2004) Alternatives for detoxification of diluted-acid lignocellulosic hydrolyzates for use in fermentative process: a review. Bioresour Technol 93:1–10. https://doi.org/10.1016/j.biortech.2003.10.005
Nakanishi SC, Soares LB, Biazi LE, Nascimento VM, Costa AC, Rocha GJM, Ienczak JL (2017) Ethanol Production From Sugarcane Bagasse Hydrolyzate by Pathaspora passalidarum and Scheffersomyces stipitis. Biotechnol Bioeng. https://doi.org/10.1002/bit.26357
Ogeda TL, Petri DFS (2010) Hidrólise Enzimática da Biomassa Hidrólise Enzimática da Biomassa. Quim Nov 33:1549–1558
Palmqvist E, Almeida JS, Hahn-Hägerdal B (1999) Biotechnol Bioeng 62(4):447–454
Palmqvist E, Hahn-Hägerdal B (2000) Fermentation of lignocellulosic hydrolysates. II: inhibitors and mechanisms of inhibition. Bioresour Technol 74:25–33. https://doi.org/10.1016/S0960-8524(99)00161-3
Passoth V, Sandgren M (2019) Biofuel production from straw hydrolysates: current achievements and perspectives. Appl Microbiol Biotechnol 103:5105–5116. https://doi.org/10.1007/s00253-019-09863-3
Perna MSC, Bastos RG, Cecatto-Antonini SR (2018) Single and combined effects of acetic acid, furfural, and sugars on the growth of the pentose-fermenting yeast Meyerozyma guilliermondii. 3Biotech 8:119. https://doi.org/10.1007/s13205-018-1143-0
Perrone GG, Tan SX, Dawes IW (2008) Reactive oxygen species and yeast apoptosis. Biochim Biophys Acta 1783:1354–1368. https://doi.org/10.1016/j.bbamcr.2008.01.023
Rech FR, Fontana RC, Rosa CA, Camassola M, Ayub MAZ, Dillon AJP (2019) Fermentation of hexoses and pentoses from sugarcane bagasse hydrolysates into ethanol by Spathaspora hagerdaliae. Bioproc Biosyst Eng 42:83–92. https://doi.org/10.1007/s00449-018-2016-y
Rocha GJM, Nascimento VM, Gonçalves AR, Silva VFN, Martın C (2015) Influence of mixed sugarcane bagasse samples evaluated by elemental and physical chemical composition. Ind Crop Prod 64:52–58. https://doi.org/10.1016/j.indcrop.2014.11.003
Sanchez G, Pilcher L, Roslander C, Modig T, Galbe M, Liden G (2004) Dilute-acid hydrolysis for fermentation of the Bolivian straw material Paja Brava. Bioresour Technol 93:249–256. https://doi.org/10.1016/j.biortech.2003.11.003
Santos CC, Souza W, Sant’Anna C, Brienzo M (2018) Elephant grass leaves have lower recalcitrance to acid pretreatment than stems, with higher potential for ethanol production. Ind Crop Prod 111:193–200. https://doi.org/10.1016/j.indcrop.2017.10.013
Silva JP, Mussatto SI, Roberto IC, Teixeira JÁ (2012) Fermentation medium and oxygen transfer conditions that maximize the xylose conversion to ethanol by Pichia stipitis. Renew Energy 3:259–265. https://doi.org/10.1016/j.renene.2011.06.032
Sindhu R, Kuttiraja M, Binod P, UshaJanu K, Sukumaran RK, Pandey A (2011) Dilute acid pretreatment and enzymatic saccharification of sugarcane tops for bioethanol production. Bioresour Technol 102:10915–10921. https://doi.org/10.1016/j.biortech.2011.09.066
Sindhu R, Gnansounou E, Binod P, Pandey A (2016) Bioconversion of sugarcane crop residue for value added products—an overview. Renew Energy 98:203–215. https://doi.org/10.1016/j.renene.2016.02.057
Sritrakul N, Nitisinprasert N, Keawsompong S (2017) Evaluation of dilute acid pretreatment for bioethanol fermentation from sugarcane bagasse pith. Agric Nat Resour 51(6):512–519. https://doi.org/10.1016/j.anres.2017.12.006
Taherzadeh MJ, Niklasson C, Liden G (2000) On-line control of fed-batch fermentation of dilute-acid hydrolyzates. Biotechnol Bioeng 69:330–338. https://doi.org/10.1002/1097-0290(20000805)69:33.0.CO;2-Q
Tomasella RC, Oliveira EG, Angelis DF, Garcia ML (2015) Evaluation of the potential of natural compounds (clay, peat and activated carbon) for the removal of lead and toxicity of an industrial effluent. Eng Sanit Ambient 20(n.2):251–258. https://doi.org/10.1590/S1413-41522015020000125291
Vallejos ME, Chade M, Mereles EB, Bengoechea DI, Brizuela JG, Felissia FE, Area MC (2016) Strategies of detoxification and fermentation for biotechnological production of xylitol from sugarcane bagasse. Ind Crop Prod 91:161–169. https://doi.org/10.1016/j.indcrop.2016.07.007
van der Pol EC, Bakker RR, Baets P, Eggink G (2014) By-products resulting from lignocellulose pretreatment and their inhibitory effect on fermentations for (bio) chemicals and fuels. Appl Microbiol Biotechnol 98:9579–9593. https://doi.org/10.1007/s00253-014-6158-9
van Zyl B, Prior BA, du Preez JC (1991) Acetic acid inhibition of D-xylose fermentation by Pichia stipitis. Enzyme Microb Technol 13:82–86. https://doi.org/10.1016/0141-0229(91)90193-E
van Zyl C, Prior BA, Kilian SG, Vincent B (1993) Role of D-ribose as a cometabolite in D-xylose metabolism by Saccharomyces cerevisiae. Appl Environ Microbiol 59(5):1487–1494
Zheng Y, Pan Z, Zhang R (2009) Overview of biomass pretreatment for cellulosic ethanol production. Int J Agric Biol Eng 2:51. https://doi.org/10.3965/j.issn.1934-6344.2009.03.051-068
Wang Z, Dien BS, Rausch KD, Tumbleson ME, Singh V (2018) Fermentation of undetoxified sugarcane bagasse hydrolyzates using a two stage hydrothermal and mechanical refining pretreatment. Bioresour Technol 261:313–321. https://doi.org/10.1016/j.biortech.2018.04.018
Acknowledgements
The authors would like to thank Sandra Regina Cecatto-Antonini and Ines Conceição Roberto for the strains of yeasts.
Funding
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001 and Brazilian Council for Research and Development (CNPq, process 401900/2016-9).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there are no conflict of interest.
Research involving human participants or animals
This article does not contain any studies with human participants or animals.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Candido, J.P., Claro, E.M.T., de Paula, C.B.C. et al. Detoxification of sugarcane bagasse hydrolysate with different adsorbents to improve the fermentative process. World J Microbiol Biotechnol 36, 43 (2020). https://doi.org/10.1007/s11274-020-02820-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11274-020-02820-7