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Saccharification of sunflower stalks using lignocellulases from a fungal consortium comprising Pholiota adiposa and Armillaria gemina

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Abstract

Lignocellulases from Armillaria gemina and Pholiota adiposa are efficient in hydrolyzing aspen and poplar biomass, respectively. In the present study, lignocellulosic enzymes obtained from a fungal consortium comprising P. adiposa and A. gemina were used for the saccharification of sunflower stalks. Sunflower stalks were thermochemically pretreated using 2 % NaOH at 50 °C for 24 h. The saccharification process parameters including substrate concentration, enzyme loading, pH, and temperature were optimized using response surface methodology to improve the saccharification yield. The highest enzymatic hydrolysis (84.3 %) was obtained using the following conditions: enzyme loading 10 FPU/g-substrate, substrate 5.5 %, temperature 50 °C, and pH 4.5. The hydrolysis yield obtained using the enzymes from the fungal consortium was equivalent to that obtained using a mixture of commercial enzymes Celluclast and Novozyme β-glucosidase. Addition of up to 500 ppm of heavy metal ions (As, Cu, Fe, Mn, Ni, Pb, and Zn) during saccharification did not significantly affect the saccharification yield. Thus, the biomass grown for phytoremediation of heavy metals can be used for the production of reducing sugars followed by ethanol fermentation.

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References

  1. Diaz MJ, Cara C, Ruiz E, Perez-Bonilla M, Castro E (2011) Hydrothermal pre-treatment and enzymatic hydrolysis of sunflower stalks. Fuel 90:3225–3229

    Article  CAS  Google Scholar 

  2. Pilanee V, Sinsupha C, Waraporn A (2009) Bioethanol production from enzymatically saccharified sunflower stalks using steam explosion as pretreatment. Int J Biol Life Sci 5:21–24

    Google Scholar 

  3. Ruiz E, Cara C, Manzanares P, Ballesteros M, Castro E (2008) Evaluation of steam explosion pre-treatment for enzymatic hydrolysis of sunflower stalks. Enzyme Microb Technol 42:160–166

    Article  CAS  Google Scholar 

  4. Sharma SK, Kalra KL, Kocher GS (2004) Fermentation of enzymatic hydrolysate of sunflower hulls for ethanol production and its scale-up. Biomass Bioenergy 27:399–402

    Article  CAS  Google Scholar 

  5. Monlau F, Latrille E, Da Costa AC, Steyer J-P, Carrere H (2012) Enhancement of methane production from sunflower oil cakes by dilute acid pretreatment. Appl Energy 112:1105–1113

    Google Scholar 

  6. Akpinar O, Levent O, Sabanci S, Uysal RS, Sapci B (2011) Optimization and comparison of dilute acid pretreatment of selected agricultural residues for recovery of xylose. Bio Resour 6:4103–4116

    CAS  Google Scholar 

  7. Akpinar O, Gunay K, Yilmaz Y, Levent O, Bostanci S (2010) Enzymatic processing and antioxidant activity of agricultural waste autohydrolysis liquors. BioResources 5:699–711

    CAS  Google Scholar 

  8. Caparros S, Ariza J, Lopez F, Nacimiento JA, Garrote G, Jimenez L (2008) Hydrothermal treatment and ethanol pulping of sunflower stalks. Bioresour Technol 99:1368–1372

    Article  CAS  Google Scholar 

  9. Franscisco L, Juan Carlos G, Antonio P, Javier MF, Minerva AMZ, Gil G (2010) Chemical and energetic characterization of species with a high-biomass production: Fractionation of their components. Environ Prog Sust Energy 29:499–509

    Article  CAS  Google Scholar 

  10. Sharma SK, Kalra KL, Grewal HS (2002) Fermentation of enzymatically saccharified sunflower stalks for ethanol production and its scale up. Bioresour Technol 85:31–33

    Article  CAS  Google Scholar 

  11. Lin C, Liu J, Liu L, Zhu T, Sheng L, Wang D (2009) Soil amendment application frequency contributes to phytoextraction of lead by sunflower at different nutrient levels. Environ Exp Botany 65:410–416

    Article  CAS  Google Scholar 

  12. Turgut C, Pepe MK, Cutright TJ (2004) The effect of EDTA and citric acid on phytoremediation of Cd, Cr, and Ni from soil using Helianthus annuus. Environ Pollution 131:147–154

    Article  CAS  Google Scholar 

  13. Adesodun J, Atayese M, Agbaje TA, Osadiaye B, Mafe OF, Soretire A (2010) Phytoremediation potentials of sunflowers (Tithonia diversifolia and Helianthus annuus) for metals in soils contaminated with zinc and lead nitrates. Water Air Soil Pollut 207:195–201

    Article  CAS  Google Scholar 

  14. Guo BLY, Zhu YG, Zhao FJ (2007) Role of salicylic acid in alleviating oxidative damage in rice roots (Oryza sativa) subjected to cadmium stress. Environ Pollut 147:743–749

    Article  CAS  Google Scholar 

  15. Alkorta I, Allica JH, Becerril JM, Amezaga I, Albizu I, Garbisu C (2004) Recent findings on the phytoremediation of soils contaminated with environmentally toxic heavy metals and metalloids such as zinc, cadmium, lead, and arsenic. Rev Environ Sci Bio-Technol 3:71–90

    Article  CAS  Google Scholar 

  16. Ullah RBJ, Shafi M, Iqbal M, Khan A, Saeed M (2011) Phyto-accumulation of heavy metals by sunflower (Helianthus annuus L.) grown on contaminated soil. Afr J Biotech 10:17192–17198

    CAS  Google Scholar 

  17. Han Y, Chen H (2010) Synergism between hydrophobic proteins of corn stover and cellulase in lignocellulose hydrolysis. Biochem Eng J 48:218–224

    Article  CAS  Google Scholar 

  18. Kim E, Lee HJ, Bang, WG, Choi IG, Kim, KH (2009) Functional characterization of a bacterial expansin from Bacillus subtilis for enhanced enzymatic hydrolysis of cellulose. Biotechnol Bioeng 102:1342–1353

  19. Dashtban M, Schraft H, Qin W (2009) Fungal bioconversion of lignocellulosic residues; opportunities and perspectives. Int J Biol Sci 5:578–595

    Article  CAS  Google Scholar 

  20. Jagtap SS, Dhiman SS, Kim TS, Li J, Lee JK, Kang YC (2013) Enzymatic hydrolysis of aspen biomass into fermentable sugars by using lignocellulases from Armillaria gemina. Bioresour Technol 133:307–314

    Article  CAS  Google Scholar 

  21. Jagtap SS, Dhiman SS, Jeya M, Kang YC, Choi JH, Lee JK (2012) Saccharification of poplar biomass by using lignocellulases from Pholiota adiposa. Bioresour Technol 120:264–272

    Article  CAS  Google Scholar 

  22. Sluiter A, Hames B, Ruiz R, Scarlata C, Sluiter J, Templeton D, Crocker D (2008) Determination of structural carbohydrates and lignin in biomass. National Renewable Energy Laboratory, Golden

    Google Scholar 

  23. Dhiman SS, Haw JR, Kalyani D, Kalia VC, Kang YC, Lee JK (2014) Simultaneous pretreatment and saccharification: Green technology for enhanced sugar yields from biomass using a fungal consortium. Bioresour Technol 179:50–57

    Article  Google Scholar 

  24. Jagtap SS, Dhiman SS, Kim TS, Kim IW, Lee JK (2014) Characterization of a novel endo-β-1,4-glucanase from Armillaria gemina and its application in biomass hydrolysis. Appl Microbiol Biotechnol 98:661–669

    Article  CAS  Google Scholar 

  25. Lee KM, Kalyani D, Tiwari MK, Kim TS, Dhiman SS, Lee JK, Kim IW (2012) Enhanced enzymatic hydrolysis of rice straw by removal of phenolic compounds using a novel laccase from yeast Yarrowia lipolytica. Bioresour Technol 123:636–645

    Article  CAS  Google Scholar 

  26. Lee KM, Moon HJ, Kalyani D, Kim H, Kim IW, Jeya M, Lee JK (2011) Characterization of cellobiohydrolase from a newly isolated strain of Agaricus arvencis. J Microbiol Biotechnol 21(7):711–718

    Article  Google Scholar 

  27. Patel SK, Kalia VC, Choi JH, Haw JR, Kim IW, Lee JK (2014) Immobilization of laccase on SiO2 nano-carriers improves its stability and reusability. J Microbiol Biotechnol 24:639–647

    Article  CAS  Google Scholar 

  28. Zhao Z, Ramachandran P, Choi JH, Lee JK, Kim IW (2013) Purification and characterization of a novel β-1,3/1,4-glucanase from Sistotrema brinkmannii HQ717718. J Korean Soc Appl Biochem 56:263–270

    Article  CAS  Google Scholar 

  29. Taniguchi M, Suzuki H, Watanabe D, Sakai K, Hoshino K, Tanaka T (2005) Evaluation of pretreatment with Pleurotus ostreatus for enzymatic hydrolysis of rice straw. J Biosci Bioeng 100:637–643

    Article  CAS  Google Scholar 

  30. Ghosh TK (1987) Measurement of cellulase activities. Pure Appl Chem 59:257–268

    Google Scholar 

  31. Joo AR, Jeya M, Lee KM, Sim WI, Kim JS, Kim IW et al (2009) Purification and characterization of a β-1,4-glucosidase from a newly isolated strain of Fomitopsis pinicola. Appl Microbiol Biotechnol 83:285–294

    Article  CAS  Google Scholar 

  32. Bailey MJ, Biely P, Poutanen K (1992) Interlaboratory testing of methods for assay of xylanase activity. J Biotechnol 23:257–270

    Article  CAS  Google Scholar 

  33. Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

    Article  CAS  Google Scholar 

  34. Elisashvili V, Penninckx M, Kachlishvili E, Tsiklauri N, Metreveli E, Kharziani T, Kvesitadze G (2008) Lentinus edodes and Pleurotus species lignocellulolytic enzymes activity in submerged and solid-state fermentation of lignocellulosic wastes of different composition. Bioresour Technol 99:457–462

    Article  CAS  Google Scholar 

  35. Sharma SK, Kalra KL, Grewal HS (2002) Enzymatic saccharification of pretreated sunflower stalks. Biomass Bioenergy 23:237–243

    Article  CAS  Google Scholar 

  36. Monlau F, Barakat A, Steyer JP, Carrere H (2012) Comparison of seven types of thermo-chemical pretreatments on the structural features and anaerobic digestion of sunflower stalks. Bioresour Technol 120:241–247

    Article  CAS  Google Scholar 

  37. Arriaga S, Revah S (2005) Improving hexane removal by enhancing fungal development in a microbial consortium biofilter. Biotechnol Bioeng 90:107–115

    Article  CAS  Google Scholar 

  38. Kausara H, Sariaha M, Sauda HM, Alam MZ, Ismail MR (2010) Development of compatible lignocellulolytic fungal consortium for rapid composting of rice straw. Int Biodeter Biodeg 64:594–600

    Article  Google Scholar 

  39. Dayanand K, Lee KM, Kim TS, Li J, Dhiman SS, Kang YC, Lee JK (2013) Microbial consortia for saccharification of woody biomass and ethanol fermentation. Fuel 107:815–822

    Article  Google Scholar 

  40. Ferreira S, Duarte AP, Ribeiro MH, Queiroz JA, Domingues FC (2009) Response surface optimization of enzymatic hydrolysis of Cistus ladanifer and Cytisus striatus for bioethanol production. Biochem Eng J 45:192–200

    Article  CAS  Google Scholar 

  41. Jagtap SS, Dhiman SS, Kim TS, Li J, Lee JK, Kang YC (2013) Enzymatic hydrolysis of aspen biomass into fermentable sugars by using lignocellulases from Armillaria gemina. Bioresour Technol 133:307–314

    Article  CAS  Google Scholar 

  42. Ruiz E, Romero I, Moya M, Cara C, Vidal JD, Castro E (2013) Dilute sulfuric acid pretreatment of sunflower stalks for sugar production. Bioresour Technol 140:292–298

    Article  CAS  Google Scholar 

  43. Jung CD, Yu JH, Eom IY, Hong KS (2013) Sugar yields from sunflower stalks treated by hydrothermolysis and subsequent enzymatic hydrolysis. Bioresour Technol 138:1–7

    Article  CAS  Google Scholar 

  44. Jagtap SS, Dhiman SS, Kim TS, Li J, Kim IW, Kang YC, Lee JK (2013) 2013b. Characterization of a β-1,4-glucosidase from a newly isolated strain of Pholiota adiposa and its application to the hydrolysis of biomass. Biomass Bioenergy 54:181–190

    Article  CAS  Google Scholar 

  45. Lee K, Cho H, Moon Y, Ban S, Kim J (2013) Cadmium and lead uptake capacity of energy crops and distribution of metals within the plant structures. KSCE J Civil Eng 17:44–50

    Article  Google Scholar 

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Acknowledgments

This work was supported by the Energy Efficiency and Resources Core Technology Program of the Korea Institute of Energy Technology Evaluation and Planning (KETEP), granted financial resource from the Ministry of Trade, Industry and Energy, Republic of Korea (201320200000420). This research was also supported by Korea Ministry of Environment as GAIA Project (G112-00055-0023-0) and KU Brain Pool of Konkuk University.

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Correspondence to Jung-Kul Lee.

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P. Ramachandran and T.-S. Kim equally contributed to this work.

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Ramachandran, P., Kim, TS., Dhiman, S.S. et al. Saccharification of sunflower stalks using lignocellulases from a fungal consortium comprising Pholiota adiposa and Armillaria gemina . Bioprocess Biosyst Eng 38, 1645–1653 (2015). https://doi.org/10.1007/s00449-015-1406-7

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