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Thermotolerant Kluyveromyces marxianus and Saccharomyces cerevisiae strains representing potentials for bioethanol production from Jerusalem artichoke by consolidated bioprocessing

  • Bioenergy and Biofuels
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Abstract

Thermotolerant inulin-utilizing yeast strains are desirable for ethanol production from Jerusalem artichoke tubers by consolidated bioprocessing (CBP). To obtain such strains, 21 naturally occurring yeast strains isolated by using an enrichment method and 65 previously isolated Saccharomyces cerevisiae strains were investigated in inulin utilization, extracellular inulinase activity, and ethanol fermentation from inulin and Jerusalem artichoke tuber flour at 40 °C. The strains Kluyveromyces marxianus PT-1 (CGMCC AS2.4515) and S. cerevisiae JZ1C (CGMCC AS2.3878) presented the highest extracellular inulinase activity and ethanol yield in this study. The highest ethanol concentration in Jerusalem artichoke tuber flour fermentation (200 g L−1) at 40 °C achieved by K. marxianus PT-1 and S. cerevisiae JZ1C was 73.6 and 65.2 g L−1, which corresponded to the theoretical ethanol yield of 90.0 and 79.7 %, respectively. In the range of 30 to 40 °C, temperature did not have a significant effect on ethanol production for both strains. This study displayed the distinctive superiority of K. marxianus PT-1 and S. cerevisiae JZ1C in the thermotolerance and utilization of inulin-type oligosaccharides reserved in Jerusalem artichoke tubers. It is proposed that both K. marxianus and S. cerevisiae have considerable potential in ethanol production from Jerusalem artichoke tubers by a high temperature CBP.

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References

  • Abdel-Banat BMA, Hoshida H, Ano A, Nonklang S, Akada R (2010) High-temperature fermentation: how can processes for ethanol production at high temperatures become superior to the traditional process using mesophilic yeast? Appl Microbiol Biotechnol 85:861–867

    Article  CAS  Google Scholar 

  • Anasontzis GE, Zerva A, Stathopoulou PM, Haralampidis K, Diallinas G, Karagouni AD, Hatzinikolaou DG (2011) Homologous overexpression of xylanase in Fusarium oxysporum increases ethanol productivity during consolidated bioprocessing (CBP) of lignocellulosics. J Biotechnol 152:16–23

    Article  CAS  Google Scholar 

  • Bajpai P, Margaritis A (1987) The effect of temperature and pH on ethanol production by free and immobilized cells of Kluyveromyces marxianus grown on Jerusalem artichoke extract. Biotechnol Bioeng 30:306–313

    Article  CAS  Google Scholar 

  • Banat IM, Marchant R (1995) Characterization and potential industrial applications of five novel, thermotolerant, fementative, yeast strains. World J Microbiol Biotechnol 11:304–306

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bonciu C, Tabacaru C, Bahrim G (2010) Yeasts isolation and selection for bioethanol production from inulin hydrolysates. Innov Rom Food Biotechnol 6:29–34

    CAS  Google Scholar 

  • Cavaille D, Combes D (1995) Effect of temperature and pressure on yeast invertase stability: a kinetic and conformational study. J Biotechnol 43:221–228

    Article  CAS  Google Scholar 

  • Chi Z, Zhang T, Liu G, Yue L (2009) Inulinase-expressing microorganisms and applications of inulinases. Appl Microbiol Biotechnol 82:211–220

    Article  CAS  Google Scholar 

  • Chubey BB, Dorrell DG (1974) Jerusalem artichoke, a potential fructose crop for prairies. Can Inst Food Sci Technol J 7:98–106

    CAS  Google Scholar 

  • Dorrell DG, Chubey BB (1977) Irrigation, fertilizer, harvest dates and storage effects on reducing sugar and fructose concentrations of Jerusalem artichoke tubers. Can J Plant Sci 57:591–596

    Article  CAS  Google Scholar 

  • Gascón S, Neumann NP, Lampen O (1968) Comparative study of the properties of the purified internal and external invertases from yeast. J Biol Chem 243:1573–1577

    Google Scholar 

  • Gong F, Sheng J, Chi Z, Li J (2007) Inulinase production by a marine yeast Pichia guilliermondii and inulin hydrolysis by the crude inulinase. J Ind Microbiol Biotechnol 34:179–185

    Article  CAS  Google Scholar 

  • Gong F, Zhang T, Chi ZM, Sheng J, Li J, Wang XH (2008) Purification and characterization of extracellular inulinase from a marine yeast Pichia guilliermondii and inulin hydrolysis by the purified inulinase. Biotechnol Bioproc Eng 13:533–539

    Article  CAS  Google Scholar 

  • Jin MJ, Balan V, Gunawan C, Dale BE (2011) Consolidated bioprocessing (CBP) performance of Clostridium phytofermentans on AFEX-treated corn stover for ethanol production. Biotechnol Bioeng 108:1290–1297

    Article  CAS  Google Scholar 

  • Kang HW, Kim Y, Kim SW, Choi GW (2011) Cellulosic ethanol production on temperature-shift simultaneous saccharification and fermentation using the thermostable yeast Kluyveromyces marxianus CHY1612. Bioprocess Biosyst Eng. doi:10.1007/s00449-011-0621-0

  • Kim CH, Rhee SK (1990) Ethanol-production from Jerusalem artichoke by inulinase and Zymomonas mobilis. Appl Biochem Biotechnol 23:171–180

    Article  CAS  Google Scholar 

  • Kim K, Hamdy MK (1986) Acid-hydrolysis of Jerusalem-artichoke for ethanol fermentation. Biotechnol Bioeng 28:138–141

    Article  CAS  Google Scholar 

  • Kushi RT, Monti R, Contiero J (2000) Production, purification and characterization of an extracellular inulinase from Kluyveromyces marxianus var. bulgaricus. J Ind Microbiol Biotechnol 25:63–69

    Article  CAS  Google Scholar 

  • Lane MM, Burke N, Karreman R, Wolfe KH, O’Byrne CP, Morrissey JP (2011) Physiological and metabolic diversity in the yeast Kluyveromyces marxianus. Antonie van Leeuwenhoek 100:507–519

    Article  CAS  Google Scholar 

  • Li SZ, Chan-Halbrendt C (2009) Ethanol production in (the) People’s Republic of China: potential and technologies. Appl Energy 86:S162–S169

    Article  CAS  Google Scholar 

  • Lim SH, Ryu JM, Lee H, Jeon JH, Sok DE, Choi ES (2011) Ethanol fermentation from Jerusalem artichoke powder using Saccharomyces cerevisiae KCCM50549 without pretreatment for inulin hydrolysis. Bioresour Technol 102:2109–2111

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Lu HZ, Ca YM, Wu ZW, Jia JH, Bai FY (2004) Kazachstania aerobia sp nov., an ascomycetous yeast species from aerobically deteriorating corn silage. Int J Syst Evol Microbiol 54:2431–2435

    Article  CAS  Google Scholar 

  • Lynd LR, van Zyl WH, McBride JE, Laser M (2005) Consolidated bioprocessing of cellulosic biomass: an update. Curr Opin Biotechnol 16:577–583

    Article  CAS  Google Scholar 

  • Makimura K, Murayama SY, Yamaguchi H (1994) Detection of a wide-range of medically important fungi by the polymerase chain-reaction. J Med Microbiol 40:358–364

    Article  CAS  Google Scholar 

  • Margaritis A, Bajpai P (1982a) Continuous ethanol-production from Jerusalem artichoke tubers. 1. Use of free-cells of Kluyveromyces marxianus. Biotechnol Bioeng 24:1473–1482

    Article  CAS  Google Scholar 

  • Margaritis A, Bajpai P (1982b) Continuous ethanol-production from Jerusalem artichoke tubers. 2. Use of immobilized cells of Kluyveromyces marxianus. Biotechnol Bioeng 24:1483–1493

    Article  CAS  Google Scholar 

  • Masuko T, Minami A, Iwasaki N, Majima T, Nishimura SI, Lee YC (2005) Carbohydrate analysis by a phenol–sulfuric acid method in microplate format. Anal Biochem 339:69–72

    Article  CAS  Google Scholar 

  • Nonklang S, Abdel-Banat BM, Cha-aim K, Moonjai N, Hoshida H, Limtong S, Yamada M, Akada R (2008) High-temperature ethanol fermentation and transformation with linear DNA in the thermotolerant yeast Kluyveromyces marxianus DMKU3-1042. Appl Environ Microbiol 74:7514–7521

    Article  CAS  Google Scholar 

  • Pandey A, Soccol CR, Selvakumar P, Soccol VT, Krieger N, Fontana JD (1999) Recent developments in microbial inulinases—its production, properties, and industrial applications. Appl Biochem Biotechnol 81:35–52

    Article  CAS  Google Scholar 

  • Pessani NK, Atiyeh HK, Wilkins MR, Bellmer DD, Banat IM (2011) Simultaneous saccharification and fermentation of Kanlow switchgrass by thermotolerant Kluyveromyces marxianus IMB3: the effect of enzyme loading, temperature and higher solid loadings. Bioresour Technol 102:10618–21064

    Article  CAS  Google Scholar 

  • Rojey A, Monot F (2010) Biofuels: production and applications. Wiley, Weinheim

    Google Scholar 

  • Rocha SN, Abrahão-Neto J, Gombert AK (2011) Physiological diversity within the Kluyveromyces marxianus species. Antonie Van Leeuwenhoek 100:619–630

    Article  CAS  Google Scholar 

  • Rosa MF, Correia IS, Novais JM (1987) Production of ethanol at high temperature in the fermentation of Jerusalem artichoke juice and a simple medium by Kluyveromyces marxianus. Biotechnol Lett 9:441–444

    Article  CAS  Google Scholar 

  • Saber WIA, El-Naggar NE (2009) Optimization of fermentation conditions for the biosynthesis of inulinase by the new source; Aspergillus tamarii and hydrolysis of some inulin containing agro-wastes. Biotechnology 8:425–433

    Article  CAS  Google Scholar 

  • Slimestad R, Seljaasen R, Meijer K, Skar SL (2010) Norwegian-grown Jerusalem artichoke (Helianthus tuberosus L.): morphology and content of sugars and fructo-oligosaccharides in stems and tubers. J Sci Food Agric 90:956–964

    CAS  Google Scholar 

  • Spiro RG (1966) Analysis of sugars found in glycoproteins. Methods Enzymol 8:3–26

    Article  CAS  Google Scholar 

  • Swanton CJ, Cavers PB, Clements DR, Moore MJ (1992) The biology of Canadian weeds. 101. Helianthus tuberosus L. Can J Plant Sci 72:1367–1382

    Article  Google Scholar 

  • Torandiaz I, Jain VK, Allais JJ, Baratti J (1985) Effect of acid or enzymatic-hydrolysis on ethanol-production by Zymomonas mobilis growing on Jerusalem artichoke juice. Biotechnol Lett 7:527–530

    Article  CAS  Google Scholar 

  • van Zyl WH, Lynd LR, den Haan R, McBride JE (2007) Consolidated bioprocessing for bioethanol production using Saccharomyces cerevisiae. Adv Biochem Eng Biotechnol 108:205–235

    Google Scholar 

  • Wack M, Blaschek W (2006) Determination of the structure and degree of polymerisation of fructans from Echinacea purpurea roots. Carbohydr Res 341:1147–1153

    Article  CAS  Google Scholar 

  • Wang SA, Bai FY (2008) Saccharomyces arboricolus sp. nov., a yeast species from tree bark. Int J Syst Evol Microbiol 58:510–514

    Article  CAS  Google Scholar 

  • Yanase S, Hasunuma T, Yamada R, Tanaka T, Ogino C, Fukuda H, Kondo A (2010) Direct ethanol production from cellulosic materials at high temperature using the thermotolerant yeast Kluyveromyces marxianus displaying cellulolytic enzymes. Appl Microbiol Biotechnol 88:381–388

    Article  CAS  Google Scholar 

  • Yuan B, Hu N, Sun J, Wang SA, Li FL (2012) Purification and characterization of a novel extracellular inulinase from a new yeast species Candida kutaonensis sp. nov. KRF1T. Appl Microbiol Biotech. doi:10.1007/s00253-012-4108-y

  • Yuan WJ, Chang BL, Ren JG, Liu JP, Bai FW, Li YY (2011) Consolidated bioprocessing strategy for ethanol production from Jerusalem artichoke tubers by Kluyveromyces marxianus under high gravity conditions. J Appl Microbiol 112:38–44

    Article  Google Scholar 

  • Yuan WJ, Zhao XQ, Ge XM, Bai FW (2008) Ethanol fermentation with Kluyveromyces marxianus from Jerusalem artichoke grown in salina and irrigated with a mixture of seawater and freshwater. J Appl Microbiol 105:2076–2083

    Article  CAS  Google Scholar 

  • Zhang T, Chi Z, Parrou JL, Gong F (2010) Expression of the inulinase gene from the marine-derived Pichia guilliermondii in Saccharomyces sp. W0 and ethanol production from inulin. Microb Biotechnol 3:576–582

    Article  CAS  Google Scholar 

  • Zhang T, Gong F, Chi Z, Liu GL, Chi ZM, Sheng J, Li J, Wang XH (2009) Cloning and characterization of the inulinase gene from a marine yeast Pichia guilliermondii and its expression in Pichia pastoris. Antonie Van Leeuwenhoek 95:13–22

    Article  CAS  Google Scholar 

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Acknowledgments

This study was supported by China Agriculture Research System (No. CARS-35), the National Natural Science Foundation of China (NSFC, No. 30900007), and Chinese Academy of Sciences (KSCX2-EW-J-10).

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Correspondence to Juan Sun or Shi-An Wang.

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Hu, N., Yuan, B., Sun, J. et al. Thermotolerant Kluyveromyces marxianus and Saccharomyces cerevisiae strains representing potentials for bioethanol production from Jerusalem artichoke by consolidated bioprocessing. Appl Microbiol Biotechnol 95, 1359–1368 (2012). https://doi.org/10.1007/s00253-012-4240-8

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  • DOI: https://doi.org/10.1007/s00253-012-4240-8

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