Abstract
Eight yeast isolates identified as Saccharomyces cerevisiae were recovered from molasses-using Cuban distilleries and discriminated by nucleotide sequence analysis of ITS locus. The isolates L/25-7-81 and L/25-7-86 showed the highest ethanol yield from sugarcane juice, while L/25-7-12 and L/25-7-79 showed high ethanol yield from sugarcane molasses. The isolate L/25-7-86 also displayed high fermentation capacity when molasses was diluted with vinasse. In addition, stress tolerance was evaluated on the basis of growth in the presence of inhibitors (acetic acid, lactic acid, 5-hydroxymethylfurfural and sulfuric acid) and the results indicated that L/25-7-77 and L/25-7-79 congregated the highest score for cross-tolerance and fermentation capacity. Hence, these isolates, especially L/25-7-77, could serve as potential biological platform for the arduous task of fermenting complex substrates that contain inhibitors. The use of these yeasts was discussed in the context of second-generation ethanol and the environmental and economic implications of the use of vinasse, saving the use of water for substrate dilution.
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References
Aguilar R, Ramírez JA, Garrote G, Vázquez M (2002) Kinetic study of the acid hydrolysis of sugar cane bagasse. J Food Eng 55:309–318. https://doi.org/10.1016/S0260-8774(02)00106-1
Almeida J, Modig T, Petersson A, Hähn-Hägerdal B, Lidé G, Gorwa-Grauslund MF (2008) Increased tolerance and conversion of inhibitors in lignocellulosic hydrolysates by Saccharomyces cerevisiae. J Chem Tech Biotechnol 82:340–349. https://doi.org/10.1002/jctb.1676
Barros de Souza R, de Menezes JA, Rodrigues de Souza RF, Dutra ED, de Morais MA (2015) Mineral composition of the sugarcane juice and its influence on the ethanol fermentation. Appl Biochem Biotechnol 175: 209–222. https://doi.org/10.1007/s12010-014-1258-7
Basílio ACM, Araújo PRL, Morais JOF, Silva-Filho EA, de Morais MA, Simões DA (2008) Detection and identification of wild yeast contaminants of the industrial fuel ethanol fermentation process. Curr Microbiol 56:322–326. https://doi.org/10.1007/s00284-007-9085-5
Basso LC, de Amorim HV, de Oliveira AJ, Lopes ML (2008) Yeast selection for fuel ethanol production in Brazil. FEMS Yeast Res 8:1155–1163. https://doi.org/10.1111/j.1567-1364.2008.00428.x
Basso TO, Gomes FS, Lopes ML, de Amorim HV, Eggleston G, Basso LC (2014) Homo- and heterofermentative lactobacilli differently affect sugarcane-based fuel ethanol fermentation. Antonie Van Leeuwenhoek 105:169–177. https://doi.org/10.1007/s10482-013-0063-6
Beckner M, Ivey M, Phister T (2011) Microbial contamination of fuel ethanol fermentations. Lett Appl Microbiol 53:387–394. https://doi.org/10.1111/j.1472-765X.2011.03124.x
Bischoff K, Liu S, Leathers TD, Worthington RE, Rich JO (2009) Modeling bacterial contamination of fuel ethanol fermentation. Biotechnol Bioeng 103:117–122. https://doi.org/10.1002/bit.22244
Christofoletti CA, Escher JP, Correia JE, Marinho JF, Fontanetti CS (2013) Sugarcane vinasse: environmental implications of its use. Waste Manag 33:2752–2761. https://doi.org/10.1016/j.wasman.2013.09.005
Da Silva-Filho E, Santos SK, Resende AM, Morais JO, de Morais MA, Simões DA (2005a) Yeast population dynamics of industrial fuel-ethanol fermentation process assessed by PCR fingerprinting. Antonie Van Leeuwenhoek 88:13–23. https://doi.org/10.1007/s10482-004-7283-8
Da Silva-Filho E, Melo HF, Antunes DF, dos Santos SK, Resende MA, Simões DA (2005b) Isolation by genetics and physiological characteristics of a fuel-ethanol fermentative S. cerevisiae strain with potential for genetic manipulation. J Ind Microbiol Biotechnol 32:481–486. https://doi.org/10.1007/s10295-005-0027-6
De Melo H, Bonini BM, Thevelein J, Simões DA, de Morais MA (2010) Physiological and molecular analysis of the stress response of Saccharomyces cerevisiae imposed by strong inorganic acid with implication to industrial fermentations. J Appl Microbiol 109:116–127. https://doi.org/10.1111/j.1365-2672.2009.04633.x
Della-Bianca BE1, Basso TO, Stambuk BU, Basso LC, Gombert AK (2013) What do we know about the yeast strains from the Brazilian fuel ethanol industry? Appl Microbiol Biotechnol 97:979–991. https://doi.org/10.1007/s00253-012-4631-x
Deparis Q, Claes A, Foulquié-Moreno MR, Thevelein JM (2017) Engineering tolerance to industrially relevant stress factors in yeast cell factories. FEMS Yeast Res 17:fox036. https://doi.org/10.1093/femsyr/fox036
Dutra E, Neto A, Barros R, de Morais MA, Tabosa JN, Simões R (2013) Ethanol production from the stem juice of different sweet sorghum cultivars in the state of Pernambuco, northeast of Brazil. Sugar Tech 15:316–321. https://doi.org/10.1007/s12355-013-0240-y
García R, Otero M (2015) Almacenamiento de mieles: reacciones de deterioro y sus consecuencias para el crecimiento microbiano. In: Aprovechamiento de las mieles de la caña de azúcar. Conocimientos y potencial. ICIDCA, Havana, 1–6
Guo Z, Olsson L (2014) Physiological response of Saccharomyces cerevisiae to weak acids present in lignocellulosic hydrolysate. FEMS Yeast Res 14:1234–1248. https://doi.org/10.1111/1567-1364.12221
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids 41:95–98
Jönsson LJ, Martín C (2016) Pretreatment of lignocellulose: formation of inhibitory by-products and strategies for minimizing their effects. Biores Technol 199:103–112. https://doi.org/10.1016/j.biortech.2015.10.009
Kausal N, Phutela R (2015) Ethanol production from molasses and sugarcane: inoculum effects and costing. J Energy Res Environ Technol (JERET) 2:385–388
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lancheros S, Morales D, Velásquez M (2015) Increase in second generation ethanol production by different nutritional conditions from sugarcane bagasse hydrolysate using a Saccharomyces cerevisiae native strain. Chem Eng Trans 43:223–228. https://doi.org/10.3303/CET1543038
Larsson S, Palmqvist E, Hahn-Hägerdal B, Tengborg C, Stenberg K, Zacchi G, Nilvebrant N (1999) The generation of inhibitors during dilute acid hydrolysis of softwood. Enz Microb Technol 24:151–159. https://doi.org/10.1016/S0141-0229(98)00101-X
Liu Z (2006) Genomic adaptation of ethanologenic yeast to biomass conversion inhibitors. Appl Microbiol Biotechnol 73:27–36. https://doi.org/10.1007/s00253-006-0567-3
Liu Z, Moon J (2009) A novel NADPH-dependent aldehyde reductase gene from Saccharomyces cerevisiae NRRL Y-12632 involved in the detoxification of aldehyde inhibitors derived from lignocellulosic biomass conversion. Gene 446:1–10. https://doi.org/10.1016/j.gene.2009.06.018
Lucena B, dos Santos BM, Moreira JLS, Moreira APB, Nunes AC, Azevedo V, Miyoshi A, Thompson FL, de Morais MA (2010) Diversity of lactic acid bacteria of the bioethanol process. BMC Microbiol 10:298. https://doi.org/10.1186/1471-2180-10-298
Makanjuola D, Springham D (1984) Identification of lactic acid bacteria isolated from different stages of malt and whisky distillery fermentations. J Inst Brew 90:13–19. https://doi.org/10.1002/j.2050-0416.1984.tb04226.x
Modig T, Liden G, Taherzadeh M (2002) Inhibition effects of furfural on alcohol dehydrogenase, aldehyde dehydrogenase and pyruvate dehydrogenase. Biochem J 363:769–776. https://doi.org/10.1042/bj3630769
Naik S, Goud V, Rout P, Dalai A (2010) Production of first- and second-generation biofuels: A comprehensive review. Renew Sustain Energy Rev 14:578–597. https://doi.org/10.1016/j.rser.2009.10.003
Pereira J, Verheijen P, Straathof A (2016) Growth inhibition of S. cerevisiae. B. subtilis and E. coli by lignocellulosic and fermentation products. Appl Microbiol Biotechnol 100:9069–9080. https://doi.org/10.1007/s00253-016-7642-1
Sanchez B, Bautista J (1988) Effects of furfural and 5-hydroxymethylfurfural on the fermentation of Saccharomyces cerevisiae and biomass production from Candida guilliermondii. Enz Microb Technol 10(5):315–318. https://doi.org/10.1016/0141-0229(88)90135-4
Sehnem N, Machado AS, Leite FC, Pita WB, de Morais MA, Ayub MA (2013) 5-Hydroxymethylfurfural induces ADH7 and ARI1 expression in tolerant industrial Saccharomyces cerevisiae strain P6H9 during bioethanol production. Biores Technol 133:190–196. https://doi.org/10.1016/j.biortech.2013.01.063
Steensels J, Snoek T, Meersman E, Picca Nicolino M, Voordeckers K, Verstrepen KJ (2014) Improving industrial yeasts strain: exploiting natural and artificial diversity. FEMS Microbiol Rev 38:947–995. https://doi.org/10.1111/1574-6976.12073
Taherzadeh M, Gustafsson L, Niklasson C (2000) Physiological effects of 5-hydroxymethylfurfural on Saccharomyces cerevisiae. Appl Microbiol Biotechnol 53(6):701–708. https://doi.org/10.1007/s002530000328
Acknowledgements
K. T. was supported by the United Nations University (UNU-BIOLAC Biotechnology for Latin America and The Caribbean) and by the Pérez-Guerrero Trust Fund for South–South Cooperation of UNDP in the frameworks of projects INT/13/K08 and INT/16/K10. This work was partially sponsored by UNU-BIOLAC program and by the Bioethanol Research Network of the State of Pernambuco (CNPq-FACEPE/PRONEM APQ-1452-2.01/10).
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Cabañas, K.T., Peña-Moreno, I.C., Parente, D.C. et al. Selection of Saccharomyces cerevisiae isolates for ethanol production in the presence of inhibitors. 3 Biotech 9, 6 (2019). https://doi.org/10.1007/s13205-018-1541-3
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DOI: https://doi.org/10.1007/s13205-018-1541-3