Abstract
In this work, the newly isolated thermotolerant Kluyveromyces marxianus DBKKUY-103 exhibited a high ethanol fermentation efficiency at high temperatures using sweet sorghum juice (SSJ). The highest ethanol concentrations and productivities achieved under the optimum conditions using thermotolerant K. marxianus DBKKUY-103 were 85.16 g/l and 1.42 g/l.h at 37 °C and 83.46 g/l and 1.39 g/l.h at 40 °C, respectively. The expression levels of genes during ethanol fermentation at 40 °C were evaluated and the results found that the transcriptional levels of the RAD10, RAD14, RAD33, RAD50, ATPH, ATP4, ATP16, and ATP20 genes were up-regulated compared with those at 30 °C, suggesting that the high growth and high ethanol production efficiencies of K. marxianus DBKKUY-103 during high-temperature ethanol production associated with the genes involved in DNA repair and ATP production.
Similar content being viewed by others
References
Abdel-Fattah WR, Fadil M, Nigam P, Banat IM (2000) Isolation of thermotolerant ethanologenic yeasts and use of selected strains in industrial scale fermentation in an Egyptian distillery. Biotechnol Bioeng 68:531–535
Auesukaree C, Koedrith P, Saenpayavai P, Asvarak T, Benjaphokee S, Sugiyama M, Kaneko Y, Harashima S, Boonchird C (2012) Characterization and gene expression profiles of thermotolerant Saccharomyces cerevisiae isolates from Thai fruits. J Biosci Bioeng 114:144–149
Beltran G, Esteve-Zarzoso B, Rozès N, Mas A, Guillamón JM (2005) Influence of the timing of nitrogen additions during synthetic grape must fermentations on fermentation kinetics and nitrogen consumption. J Agric Food Chem 53:996–1002
Beltran G, Rozès N, Mas A, Guillamón JM (2007) Effect of low-temperature fermentation on yeast nitrogen metabolism. World J Microbiol Biotechnol 23:809–815
Charoensopharat K, Thanonkeo P, Thanonkeo S, Yamada M (2015) Ethanol production from Jerusalem artichoke tubers at high temperature by newly isolated thermotolerant inulin-utilizing yeast Kluyveromyces marxianus using consolidated bioprocessing. Antonie Van Leeuwenhoek J Microb 108:173–190
Ercan Y, Irfan T, Mustafa K (2013) Optimization of ethanol production from carob pod extract using immobilized Saccharomyces cerevisiae cells in a stirred tank bioreactor. Bioresour Technol 135:365–371
Friedberg EC, Walker GC, Siede W (1995) DNA repair and mutagenesis. American Society for Microbiology, Washington, DC
Gnansounou E, Dauriat A, Wyman CE (2005) Refining sweet sorghum to ethanol and sugar: economic trade-offs in the context of North China. Bioresour Technol 96:985–1002
Gross C, Watson K (1996) Heat shock protein synthesis and trehalose accumulation are not required for induced thermotolerance in depressed Saccharomyces cerevisiae. Biochem Biophys Res Commun 220:766–772
Hashem M, Zohri ANA, Ali MM (2013) Optimization of the fermentation conditions for ethanol production by new thermotolerant yeast strains of Kluyveromyces sp. Afr J Microbiol Res 7:4550–4561
Kim S, Kim YS, Kim H, Jin I, Yoon HS (2013) Saccharomyces cerevisiae KNU5377 stress response during high-temperature ethanol fermentation. Mol Cells 35:210–218
Laopaiboon L, Nuanpeng S, Srinophakun P, Klanrit P, Laopaiboon P (2009) Ethanol production from sweet sorghum juice using very high gravity technology: effects of carbon and nitrogen supplementations. Bioresour Technol 100:4176–4182
Lei JJ, Zhao XQ, Ge XM, Bai FW (2007) Ethanol tolerance and the variation of plasma membrane composition of yeast floc populations with different size distribution. J Biotechnol 131:270–273
Lertwattanasakul N, Kosaka T, Hosoyama A, Suzuki Y, Rodrussamee N, Matsutani M, Murata M, Fujimoto N, Suprayogi Tsuchikane K, Limtong S, Fujita N, Yamada M (2015) Genetic basis of the highly efficient yeast Kluyveromyces marxianus: complete genome sequence and transcriptome analyses. Biotechnol Biofuels 8:47
Limtong S, Sringiew C, Yongmanitchai W (2007) Production of fuel ethanol at high temperature from sugar cane juice by a newly isolated Kluyveromyces marxianus. Bioresour Technol 98:3367–3374
Lin Y, Zhang W, Li C, Sakakibara K, Tanaka S, Kong H (2012) Factors affecting ethanol fermentation using Saccharomyces cerevisiae BY4742. Biomass Bioenergy 47:395–401
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408
Maeda RN, Barcelos CA, Anna LMMS, Pereira N Jr (2013) Cellulase production by Penicillium funiculosum and its application in the hydrolysis of sugar cane bagasse for second generation ethanol production by fed batch operation. J Biotechnol 163:38–44
Mecozzi M (2005) Estimation of total carbohydrate amount in environmental samples by the phenol–sulphuric acid method assisted by multivariate calibration. Chemom Intell Lab 79:84–90
Mensonides FIC, Brul S, Hellingwerf KJ, Bakker BM, Teixeira de Mattos MJ (2014) A kinetic model of catabolic adaptation and protein reprofiling in Saccharomyces cerevisiae during temperature shifts. FEBS J 281:825–841
Narendranath NV, Power R (2005) Relationship between pH and medium dissolved solids in terms of growth and metabolism of Lactobacilli and Saccharomyces cerevisiae during ethanol production. Appl Environ Microbiol 71:2239–2243
Nuanpeng S, Thanonkeo S, Yamada M, Thanonkeo P (2016) Ethanol production from sweet sorghum juice at high temperatures using a newly isolated thermotolerant yeast Saccharomyces cerevisiae DBKKU Y-53. Energies 9:253
Ozmihci S, Kargi F (2007) Effects of feed sugar concentration on continuous ethanol fermentation of cheese whey powder solution (CWP). Enzym Microb Technol 41:876–880
Pereira FB, Guimarães PMR, Teixeira JA, Domingues L (2010) Optimization of low-cost medium for very high gravity ethanol fermentations by Saccharomyces cerevisiae using statistical experimental designs. Bioresour Technol 101:7856–7863
Piper PW (1995) The heat-shock and ethanol stress responses of yeast exhibit extensive similarity and functional overlap. FEMS Microbiol Lett 134:121–127
Pratt-Marshall PL, Bryce JH, Stewart GG (2003) The effects of osmotic pressure and ethanol on yeast viability and morphology. J Inst Brew 109:218–228
Soini J, Falschlehner C, Mayer C, Böhm D, Weinel S, Panula J, Vasala A, Neubauer P (2005) Transient increase of ATP as a response to temperature up-shift in Escherichia coli. Microb Cell Fact 4:9
Stanley D, Bandara A, Fraser S, Chambers PJ, Stanley GA (2010) The ethanol stress response and ethanol tolerance of Saccharomyces cerevisiae. J Appl Microbiol 109:13–24
Techaparin A, Thanonkeo P, Klanrit P (2017a) High-temperature ethanol production using thermotolerant yeast newly isolated from Greater Mekong Subregion. Braz J Microbiol 48:461–475
Techaparin A, Thanonkeo P, Klanrit P (2017b) Gene expression profiles of the thermotolerant yeast Saccharomyces cerevisiae strain KKU-VN8 during high-temperature ethanol fermentation using sweet sorghum juice. Biotechnol Lett 39:1521–1527
ter Schure EG, van Riel AAW, Verrips CT (2000) The role of ammonia metabolism in nitrogen catabolite repression in Saccharomyces cerevisiae. FEMS Microbiol Rev 24:67–83
Thomas KC, Hynes SH, Ingledew WM (2002) Influence of medium buffering capacity on inhibition of Saccharomyces cerevisiae growth by acetic and lactic acids. Appl Environ Microbiol 68:1616–1623
Tofighi A, Assadi MM, Asadirad MHA, Karizi SZ (2014) Bio-ethanol production by a novel autochthonous thermo-tolerant yeast isolated from wastewater. J Env Health Sci Eng 12:107
Tomkinson AE, Bardwell AJ, Bardwell L, Tappe NJ, Friedberg EC (1993) Yeast DNA repair and recombination proteins Rad1 and Rad10 constitute a single-strand-DNA endonuclease. Nature 362:860–862
Walker GM (1994) The roles of magnesium in biotechnology. Crit Rev Biotechnol 14:311–354
Walker GM (1998) Yeast physiology and biotechnology. Wiley, New York
Wang Z, Wei S, Reed SH, Wu X, Svejstrup JQ, Feaver WJ, Kornberg RD, Friedberg EC (1997) The RAD7, RAD10, and RAD23 genes of Saccharomyces cerevisiae: requirement for transcription-independent nucleotide excision repair in vitro and interactions between the gene products. Mol Cell Biol 17:635–643
Yue G, Yu J, Zhang X, Tan T (2012) The influence of nitrogen sources on ethanol production by yeast from concentrated sweet sorghum juice. Biomass Bioenergy 39:48–52
Zoecklein B, Fugelsang KC, Gump B, Nury FS (1995) Wine analysis and production. Springer Science & Business Media, New York
Acknowledgements
This research was financially supported by the National Research Universities (NRU) Grant Number BiF-2553-Ph.d-01. A portion of this work was also supported by the Fermentation Research Center for Value Added Agricultural Products (FerVAAP).
Author information
Authors and Affiliations
Contributions
W. Pilap carried out the experiments and analyzed the data. S. Thanonkeo participated in the data analysis of the raw material (SSJ). P. Klanrit contributed to the design of the gene expression analysis and participated in drafting the manuscript. P. Thanonkeo contributed to the design of the experiments, conducted the experiments, analyzed the data and revised the manuscript. All of the authors read, corrected and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Pilap, W., Thanonkeo, S., Klanrit, P. et al. The potential of the newly isolated thermotolerant Kluyveromyces marxianus for high-temperature ethanol production using sweet sorghum juice. 3 Biotech 8, 126 (2018). https://doi.org/10.1007/s13205-018-1161-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-018-1161-y