Abstract
The tolerance of the pentose-fermenting yeast Meyerozyma guilliermondii to the inhibitors released after the biomass hydrolysis, such as acetic acid and furfural, was surveyed. We first verified the effects of acetic acid and cell concentrations and initial pH on the growth of a M. guilliermondii strain in a semi-synthetic medium containing acetic acid as the sole carbon source. Second, the single and combined effects of furfural, acetic acid, and sugars (xylose, arabinose, and glucose) on the sugar uptake, cell growth, and ethanol production were also analysed. Growth inhibition occurred in concentrations higher than 10.5 g l−1 acetic acid and initial pH 3.5. The maximum specific growth rate (µ) was 0.023 h−1 and the saturation constant (ks) was 0.75 g l−1 acetic acid. Initial cell concentration also influenced µ. Acetic acid (initial concentration 5 g l−1) was co-consumed with sugars even in the presence of 20 mg l−1 furfural without inhibition to the yeast growth. The yeast grew and fermented sugars in a sugar-based medium with acetic acid and furfural in concentrations much higher than those usually found in hemicellulosic hydrolysates.
Similar content being viewed by others
References
Aguilar R, Ramirez JA, Garrote G, Vazquez M (2002) 2) Kinetic study of the acid hydrolysis of sugar cane bagasse. J Food Eng 55:309–318
Allen SA, Clark W, McCaffery JM, Cail Z, Lanctot A, Slininger PJ, Liu ZL, Gorsich SW (2010) Furfural induces reactive oxygen species accumulation and cellular damage in Saccharomyces cerevisiae. Biotechnol Biofuels 3:1–10
Almeida JRM, Modig T, Petersson A, Hahn-Hagerdal B, Lidén G, Gorwa-Grauslund MF (2007) Increased tolerance and conversion of inhibitors in lignocellulosic hydrolysates by Saccharomyces cerevisiae. J Chem Technol Biotechnol 82:340–349
Antal MJ, Leesomboon T, Mok WS, Richards GN (1991) Mechanism of formation of 2-furaldehyde from D-xylose. Carbohydr Res 217:71–85
Arneborg N, Majbritt KM, Mogens J (1995) The effect of acetic acid and specific growth rate on acetic acid tolerance and trehalose content of Saccharomyces cerevisiae. Biotechnol Lett 17:1299–1304
Bellissimi E, van Dijken JP, Pronk JT, van Maris AJ (2009) Effects of acetic acid on the kinetic of xylose fermentation by an engineered, xylose-isomerase-based Saccharomyces cerevisiae strain. FEMS Yeast Res 9:358–364
Cadete RM, Santos RO, Melo MA, Mouro A, Gonçalves DL, Stambuk BU, Gomes FCO, Lachance MA, Rosa CA (2009) Spathaspora arboriae sp. nov., a D-xylose fermenting yeast species isolated from rotting wood in Brazil. FEMS Yeast Res 9:1338–1342
Capusoni C, Arioli S, Zambelli P, Moktaduzzaman M, Mora D, Compagno C (2016) Effects of oxygen availability on acetic acid tolerance and intracellular pH in Dekkera bruxellensis. Appl Environ Microbiol 82:4673–4681
Carvalheiro F, Duarte LC, Lopes S, Parajó JC, Pereira H, Gírio FM (2005) Evaluation of the detoxification of brewery’s spent grain hydrolysate for xylitol production by Debaryomyces hansenii CCMI 94. Process Biochem 40:1215–1223
Casal M, Cardoso H, Leão C (1996) Mechanisms regulating the transport of acetic acid in Saccharomyces cerevisiae. Microbiology 142:1385–1390
Casey E, Sedlak M, Ho NWY, Mosier NS (2010) Effect of acetic acid and pH on the cofermentation of glucose and xylose to ethanol by a genetically engineered strain of Saccharomyces cerevisiae. FEMS Yeast Res 10:385–393
Ceccato-Antonini SR, Codato CB, Martini C, Bastos RG, Tauk-Tornisielo SM (2017) Yeast for pentose fermentation: isolation, screening, performance, manipulation, and prospects. In: Buckeridge MS, de Souza AP (eds) Advances of basic science for second generation bioethanol from sugarcane. Springer, Berlin, pp 133–157
Chandel AK, Silva SS, Singh OV (2011) Detoxification of lignocellulosic hydrolysates for improved bioethanol production. In: Bernardes MAS (ed) Biofuel production—recent developments and prospects. InTech, Rijeka, pp 225–246
Chen Y, Stabryla L, Wei N (2016) Improved acetic acid resistance in Saccharomyces cerevisiae by overexpression of the WHI2 gene identified through inverse metabolic engineering. Appl Environ Microbiol 82:2156–2166
Converti A, Perego P, Torre P, Silva SS (2000) Mixed inhibitions by methanol, furfural and acetic acid on xylitol production by Candida guilliermondii. Biotechnol Lett 22:1861–1865
Ding MZ, Wang X, Yang Y, Yuan YJ (2011) Metabolomic study of interactive effects of phenol, furfural, and acetic acid on Saccharomyces cerevisiae. OMICS 15:647–653
Fonseca BG, Moutta RO, Ferraz FO, Vieira ER, Nogueira AS, Baratella BF, Rodrigues LC, Hou-Rui Z, Silva SS (2011) Biological detoxification of different hemicellulosic hydrolysates using Issatchenkia occidentalis CCTCC M 206097 yeast. J Ind Microbiol Biotechnol 38:199–207
Geros H, Cassio F, Leão C (2000) Utilization and transport of acetic acid in Dekkera anomala and their implications on the survival of the yeast in acidic environments. J Food Protect 1:96–101
Gonçalves BCM, Jesus JYFM, Peron LHB, Freitas WLC, Pagnocca FC, Silva SS (2013) Consumo de açúcares e ácido acético durante a destoxificação biológica de hidrolisado hemicelulósico pela levedura Issatchenkia occidentalis M. Biochem Biotechnol Rep 2:372–375
Greetham D (2014) Presence of low concentrations of acetic acid improves fermentations using Saccharomyces cerevisiae. J Bioprocess Biotechol 5:192. https://doi.org/10.4172/2155-9821.1000192
Hanly TJ, Henson MA (2014) Dynamic model-based analysis of furfural and HMF detoxification by pure and mixed batch cultures of S. cerevisiae and S. stipites. Biotechnol Bioeng 111:272–284
Heer D, Heine D, Sauer U (2009) Resistance of Saccharomyces cerevisiae to high furfural concentrations is based on NADPH-dependent reduction by at least two oxireductases. Appl Environ Microbiol 75:7631–7638
Horvath IS, Franzen CJ, Taherzadeh MJ, Niklasson C, Liden G (2003) Effects of furfural on the respiratory metabolism of Saccharomyces cerevisiae in limited chemostats. Appl Environ Microbiol 69:4076–4086
Kurtzman CP, Suzuki M (2010) Phylogenetic analysis of ascomycete yeasts that form coenzyme Q-9 and the proposal of the new genera Babjeviella, Meyerozyma, Millerozyma, Priceomyces, and Scheffersomyces. Mycoscience 51:2–14
Lima JR, Gonçalves LRB, Brandão LR, Rosa CA, Viana FMP (2012) Isolation, identification and activity in vitro of killer yeasts against Colletotrichum gloeosporioides isolated from tropical fruits. J Microbiol 52:1–10
Lu Y, Warner R, Sedlak M, Ho NWY, Mosier NS (2009) Comparison of glucose/xylose cofermentation of poplar hydrolysates processed by different pretreatment technologies. Biotechnol Progress 25:349–356
Luján-Rhenals ED, Moraw RO, Ricke SC (2014) Tolerance of Saccharomyces cerevisiae and Zymomonas mobilis to inhibitors produced during dilute acid hydrolysis of soybean meal. J Environ Sci Health 49:305–311
Ma M, Wang X, Zhang X, Zhao X (2013) Alcohol dehydrogenases from Scheffersomyces stipitis involved in the detoxification of aldehyde inhibitors derived from lignocelullosic biomass conversion. Appl Microbiol Biotechnol 97:8411–8425
Martini C (2014) Isolamento, identificação e caracterização de linhagem de levedura quanto ao crescimento e fermentação utilizando meios sintéticos com pentoses e hidrolisado de bagaço de cana-de-açúcar. Thesis, Universidade Estadual Paulista Julio de Mesquita Filho, Brazil
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
Matos ITSR, Cassa-Barbosa LA, Medeiros Galvão RS, Nunes-Silva CG, Astolfi Filho S (2014) Isolation, taxonomic identification and investigation of the biotechnological potential of wild-type Meyerozyma guilliermondii associated with Amazonian termites able to ferment D-xylose. Biosci J 30:260–266
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428
Moktaduzzaman M, Galafassi S, Vigentini I, Foschino R, Corte L, Cardinali G, Piskur J, Compagno C (2016) Strain-dependent tolerance to acetic in Dekkera bruxellensis. Ann Microbiol 66:351–359
Mollapour M, Piper PW (2008) Weak organic acid resistance of spoilage yeasts. In: Avery SV, Stratford M, van West P (eds) Stress in yeasts and filamentous fungi. Elsevier, Oxford, pp 143–155
Mussatto SI, Teixeira JA (2010) Lignocellulose as raw material in fermentation processes. In: Méndez-Vilas A (ed) Current research, technology and education topics in applied microbiology and microbial biotechnology. Formatex, Badajoz, pp 897–907
Nogué V, Bettiga M, Gorwa-Grauslund MF (2012) Isolation and characterization of a resident tolerant Saccharomyces cerevisiae strain from a spent sulfite liquor fermentation plant. AMB Express 2:68. https://doi.org/10.1186/2191-0855-2-68
Noronha LL, Fonseca CR, Silva CC, Silva MB, Faria LFF (2010) Utilização de diferentes tipos de policloretos de alumínio para purificação de hidrolizado de bagaço de cana através da técnica de coagulação e floculação. Quim Nova 33:1698–1702
Palmqvist E, Hahn-Hagerdal B (2000) Fermentation of lignocellulosic hydrolysates. II: Inhibitors and mechanisms of inhibition. Bioresour Technol 74:25–33
Palmqvist E, Grage H, Meinander NQ, Hahn-Hagerdal B (1999) Main and interaction effects of acetic acid, furfural, and p-hydroxybenzoic acid on growth and ethanol productivity of yeasts. Biotechnol Bioeng 63:46–55
Pampulha ME, Loureiro-Dias MC (1989) Combined effect of acetic acid, pH and ethanol on intracellular pH of fermenting yeast. Appl Microbiol Biotechnol 31:547–550
Papon N, Savini V, Lanoue A, Simkin AJ, Crèche J, Giglioli-Guivarćh 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 59:73–90
Pereira RS, Mussatto SI, Roberto IC (2011) Inhibitory action of toxic compounds present in lignocellulosic hydrolysates on xylose to xylitol bioconversion by Candida guilliermondii. J Ind Microbiol Biotechnol 38:71–78
Perrone GG, Tan SX, Dawes IW (2008) Reactive oxygen species and yeast apoptosis. Biochem Biophys Acta 1783:1354–1368
Raele R, Boaventura JMG, Fischmann AA, Sarturi G (2014) Scenarios for the second generation ethanol in Brazil. Technol Forec Soc Chang 87:205–223
Rao DG (2010) Introduction to biochemical engineering. Tata McGraw Hill, New Delhi, p 2010
Rodrigues RCLB, Sene L, Matos GS, Roberto IC, Pessoa A Jr, Felipe MG (2006) Enhanced xylitol production by precultivation of Candida guilliermondii cells in sugarcane bagasse hemicellulosic hydrolysate. Curr Microbiol 53:53–59
Rodrigues F, Sousa MJ, Ludovico P, Santos H, Corte-Real M, Leão C (2012) The fate of acetic acid during glucose co-metabolism by the spoilage yeast Zygosaccharomyces bailii. PLoS ONE 7:e52402. https://doi.org/10.1371/journal.pone.0052402
Senatham S, Chamduang T, Kaewchingduang Y, Thammasittirong A, Srisodsuk M, Elliston A, Roberts IN, Waldron KW, Thammasittirong SNR (2016) Enhanced xylose fermentation and hydrolysate inhibitor tolerance of Scheffersomyces shehatae for efficient ethanol production from non-detoxified lignocellulosic hydrolysate. SpringerPlus 5:1040. https://doi.org/10.1186/s400064-016-2713-4
Sene L, Vitolo M, Felipe MGA, Silva SS (2000) Effects of environmental conditions on xylose reductase and xylitol dehydrogenase production by Candida guilliermondii. In: Finkelstein M, Davison BH (eds) Biotechnology for fuels and chemicals. Springer, New York, pp 371–380
Silveira FA (2014) Seleção de leveduras fermentadoras de xilose e análise do exometaboloma de Meyerozyma guilliermondii UFV-1. Dissertation, Universidade Federal de Viçosa, Brazil
Sousa MJ, Miranda L, Corte-Real M, Leão C (1996) Transport of acetic acid in Zygosaccharomyces bailii: effects of ethanol and their implication on the resistance of the yeast to acidic environments. Appl Environ Microbiol 62:3152–3157
Sousa MJ, Rodrigues F, Corte-Real M, Leão C (1998) Mechanisms underlying the transport and intracelular metabolism of acetic acid in the presence of glucose in the yeast Zygosaccharomyces bailii. Microbiology 144:665–670
Verduyn C, Postma E, Scheffers WA, van Dijken JP (1990) Energetics of Saccharomyces cerevisiae in anaerobic glucose-limited chemostat cultures. J Gen Microbiol 136:405–412
Wei N, Quarterman J, Kim SR, Cate JHD, Jin YS (2013) Enhanced biofuel production through coupled acetic acid and xylose consumption by engineered yeast. Nat Commun 4:2580. https://doi.org/10.1038/ncomms3580
Ylitervo P, Frazen CJ, Taherzadeh MJ (2014) Continuous ethanol production with a membrane bioreactor at high acetic acid concentrations. Membranes 4:372–387
Zhang DP, Spadaro D, Valente S, Garibaldi A, Gullino ML (2011) Cloning, characterization and expression of an exo-1,3-betaglucanase gene from the antagonistic yeast, Pichia guilliermondii strain M8 against grey mold on apples. Biol Control 59:284–293
Zhao J, Wang M, Yang Z, Gong Q, Lu Y, Yang Z (2005) Mediated electrochemical measurement of the inhibitory effects of furfural and acetic acid on Saccharomyces cerevisiae and Candida shehatae. Biotechnol Lett 27:207–211
Funding
M.S.C. Perna planned and performed the experiments, analysed, and interpreted the data, drafted, and commented the manuscript. R.G. Bastos analysed and interpreted the data and revised critically the manuscript. S.R. Ceccato-Antonini made the study conception and design, analysed and interpreted the data, and revised critically the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest in the publication.
Rights and permissions
About this article
Cite this article
Perna, M.d.C., Bastos, R.G. & Ceccato-Antonini, S.R. Single and combined effects of acetic acid, furfural, and sugars on the growth of the pentose-fermenting yeast Meyerozyma guilliermondii. 3 Biotech 8, 119 (2018). https://doi.org/10.1007/s13205-018-1143-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-018-1143-0