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Sporotrichum thermophile Xylanases and Their Biotechnological Applications

  • Ayesha Sadaf
  • Syeda Warisul Fatima
  • Sunil K. KhareEmail author
Chapter

Abstract

Thermophilic fungi are very useful resources for bio-industries and bioprocesses due to the inherent stability of their enzymes. These enzymes enable industrial biocatalysis at high temperatures, with low risk of contamination and high reaction rates. Sporotrichum thermophile is a well-known thermophilic ascomycete producing an array of interesting enzymes. Keeping in mind the industrial potential of S. thermophile, this chapter addresses the relevance of this thermophilic mould as well as the different types of enzymes produced by it with a special reference for its xylanase. The S. thermophile xylanase exhibits many interesting biochemical properties like broad pH and heat stability along with the ability to utilise a large number of xylan substrates. The genome analysis of S. thermophile revealed the presence of several carbohydrate hydrolases making it potentially useful in biomass utilisation. Recently the S. thermophile xylanase has also been shown to be remarkably stable and catalytically active in as high as 50% (v/v) concentration of most commonly used ionic liquids, the green solvents used for pretreating and solubilising the lignocellulosic biomass. This property has been successfully exploited for one-pot in situ IL pretreatment and saccharification of wheat straw. Further, the proteomic and transcriptomic analysis supported the upregulated lignocellulolytic enzymes like xylanases, cellulases, glucosidases and pectinases. Lately the genome editing of S. thermophile by CRISPR-Cas system has been attempted using targeted mutations for its cellulase enzyme system which has eventually led to enhanced production levels. Thus, the future research on S. thermophile will help in developing a robust and potential strain for cost-effective biofuel generation.

Keywords

Thermophilic fungi Thermostable xylanase Lignocellulosic biomass Biofuels Saccharification 

References

  1. Arazoe T, Miyoshi K, Yamato T, Ogawa T, Ohsato S, Arie T, Kuwata S (2015) Tailor-made CRISPR/Cas system for highly efficient targeted gene replacement in the rice blast fungus. Biotechnol Bioeng 112:2543–2549PubMedCrossRefGoogle Scholar
  2. Badgujar KC, Bhanage BM (2015) Factors governing dissolution process of lignocellulosic biomass in ionic liquid: current status, overview and challenges. Bioresour Technol 178:2–18PubMedCrossRefGoogle Scholar
  3. Badhan AK, Chadha BS, Sonia KG, Saini HS, Bhat MK (2004) Functionally diverse multiple xylanases of thermophilic fungus Myceliophthora sp. IMI 387099. Enzym Microb Technol 35:460–466CrossRefGoogle Scholar
  4. Badhan A, Chadha B, Kaur J, Saini H, Bhat M (2007) Production of multiple xylanolytic and cellulolytic enzymes by thermophilic fungus Myceliophthora sp. IMI 387099. Bioresour Technol 98:504–510PubMedCrossRefGoogle Scholar
  5. Bai W, Xue Y, Zhou C, Ma Y (2015a) Cloning, expression, and characterization of a novel alkali-tolerant xylanase from alkaliphilic Bacillus sp. SN5. Biotechnol Appl Biochem 62:208–217PubMedCrossRefGoogle Scholar
  6. Bai W, Zhou C, Zhao Y, Wang Q, Ma Y (2015b) Structural insight into and mutational analysis of family 11 xylanases: implications for mechanisms of higher pH catalytic adaptation. PLoS One 10:e0132834PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bajaj BK, Sharma M, Rao RS (2014) Agricultural residues for production of cellulase from Sporotrichum thermophile LAR5 and its application for saccharification of rice straw. J Mater Environ Sci 5:1454–1460Google Scholar
  8. Bala A, Singh B (2016) Cost-effective production of biotechnologically important hydrolytic enzymes by Sporotrichum thermophile. Bioprocess Biosyst Eng 39:181–191PubMedCrossRefGoogle Scholar
  9. Bala A, Singh B (2017) Concomitant production of cellulase and xylanase by thermophilic mould Sporotrichum thermophile in solid state fermentation and their applicability in bread making. World J Microbiol Biotechnol 33:1–10CrossRefGoogle Scholar
  10. Bala A, Singh B (2018) Cellulolytic and xylanolytic enzymes of thermophiles for the production of renewable biofuels. Renew Energy.  https://doi.org/10.1016/j.renene.2018.09.100CrossRefGoogle Scholar
  11. Basit A, Liu J, Miao T, Zheng F, Rahim K, Lou H, Jiang W (2018) Characterization of two endo-β-1, 4-xylanases from Myceliophthora thermophila and their saccharification efficiencies, synergistic with commercial cellulase. Front Microbiol 9:1–11CrossRefGoogle Scholar
  12. Beeson WT, Iavarone AT, Hausmann CD, Cate JHD, Marletta MA (2011) Extracellular Aldonolactonase from Myceliophthora thermophila. Appl Environ Microbiol 77:650–656PubMedCrossRefGoogle Scholar
  13. Bergquist PL, Morgan HW, Saul D (2014) Selected enzymes from extreme thermophiles with applications in biotechnology. Curr Biotechnol 3:45–59CrossRefGoogle Scholar
  14. Berka RM, Grigoriev IV, Otillar R, Salamov A, Grimwood J, Reid I, Ishmael N, John T, Darmond C, Moisan M-C (2011) Comparative genomic analysis of the thermophilic biomass-degrading fungi Myceliophthora thermophila and Thielavia terrestris. Nat Biotechnol 29:922–927PubMedPubMedCentralCrossRefGoogle Scholar
  15. Boonrung S, Katekaew S, Mongkolthanaruk W, Aimi T, Boonlue S (2016) Purification and characterization of low molecular weight extreme alkaline xylanase from the thermophilic fungus Myceliophthora thermophila BF1-7. Mycoscience 57:408–416CrossRefGoogle Scholar
  16. Bouacem K, Bouanane-Darenfed A, Boucherba N, Joseph M, Gagaoua M, Hania WB, Kecha M, Benallaoua S, Hacene H, Ollivier B (2014) Partial characterization of xylanase produced by Caldicoprobacter algeriensis, a new thermophilic anaerobic bacterium isolated from an Algerian hot spring. Appl Biochem Biotechnol 174:1969–1981PubMedCrossRefPubMedCentralGoogle Scholar
  17. Butt MS, Tahir-Nadeem M, Ahmad Z, Sultan MT (2008) Xylanases and their applications in baking industry. Food Technol Biotechnol 46:22–31Google Scholar
  18. Chanwicha N, Katekaew S, Aimi T, Boonlue S (2015) Purification and characterization of alkaline xylanase from Thermoascus aurantiacus var. levisporus KKU-PN-I2-1 cultivated by solid-state fermentation. Mycoscience 56:309–318CrossRefGoogle Scholar
  19. Chawachart N, Anbarasan S, Turunen S, Li H, Khanongnuch C, Hummel M, Sixta H, Granström T, Lumyong S, Turunen O (2014) Thermal behaviour and tolerance to ionic liquid [emim] OAc in GH10 xylanase from Thermoascus aurantiacus SL16W. Extremophiles 18:1023–1034PubMedCrossRefGoogle Scholar
  20. Cheng YS, Chen CC, Huang CH, Ko TP, Luo W, Huang JW, Liu JR, Guo RT (2014) Structural analysis of a glycoside hydrolase family 11 xylanase from Neocallimastix patriciarum: insights into the molecular basis of a thermophilic enzyme. J Biol Chem 289:11020–11028PubMedPubMedCentralCrossRefGoogle Scholar
  21. Cherubini F (2010) The biorefinery concept: using biomass instead of oil for producing energy and chemicals. Energy Convers Manag 51:1412–1421CrossRefGoogle Scholar
  22. Collins T, Gerday C, Feller G (2005) Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiol Rev 29:3–23PubMedCrossRefGoogle Scholar
  23. da Costa Lopes AM, Bogel-Lukasik R (2015) Acidic ionic liquids as sustainable approach of cellulose and lignocellulosic biomass conversion without additional catalysts. ChemSusChem 8:947–965CrossRefGoogle Scholar
  24. Dalmaso GZL, Ferreira D, Vermelho AB (2015) Marine extremophiles: a source of hydrolases for biotechnological applications. Mar Drugs 13:1925–1965PubMedPubMedCentralCrossRefGoogle Scholar
  25. de Souza AR, de Araujo GC, Zanphorlin LM, Ruller R, Franco FC, Torres FA, Mertens JA, Bowman MJ, Gomes E, Da Silva R (2016) Engineering increased thermostability in the GH-10 endo-1, 4-β-xylanase from Thermoascus aurantiacus CBMAI 756. Int J Biol Macomol 93:20–26CrossRefGoogle Scholar
  26. Dhiman SS, Sharma J, Battan B (2008) Industrial applications and future prospects of microbial xylanases: a review. Bioresources 3:1377–1402Google Scholar
  27. Dien BS, Jung H-JG, Vogel KP, Casler MD, Lamb JF, Iten L, Mitchell RB, Sarath G (2006) Chemical composition and response to dilute-acid pretreatment and enzymatic saccharification of alfalfa, reed canarygrass, and switchgrass. Biomass Bioenergy 30:880–891CrossRefGoogle Scholar
  28. Dimarogona M, Topakas E, Olsson L, Christakopoulos P (2012) Lignin boosts the cellulase performance of a GH-61 enzyme from Sporotrichum thermophile. Bioresour Technol 110:480–487PubMedCrossRefGoogle Scholar
  29. Dotsenko GS, Semenova MV, Sinitsyna OA, Hinz SWA, Wery J, Zorov IN, Kondratieva EG, Sinitsyn AP (2012) Cloning, purification, and characterization of galactomannan-degrading enzymes from Myceliophthora thermophila. Biochem Mosc 77:1303–1311CrossRefGoogle Scholar
  30. Ebringerova A, Heinze T (2000) Xylan and xylan derivatives–biopolymers with valuable properties, 1. Naturally occurring xylans structures, isolation procedures and properties. Macromol Rapid Commun 21:542–556CrossRefGoogle Scholar
  31. Fan G, Yang S, Yan Q, Guo Y, Li Y, Jiang Z (2014) Characterization of a highly thermostable glycoside hydrolase family 10 xylanase from Malbranchea cinnamomea. Int J Biol Macomol l70:482–489CrossRefGoogle Scholar
  32. Fawzi E (2011) Highly thermostable xylanase purified from Rhizomucor miehei NRL 3169. Acta Biol Hung 62:85–94PubMedCrossRefGoogle Scholar
  33. Garcia-Huante Y, Cayetano-Cruz M, Santiago-Hernandez A, Cano-Ramirez C, Marsch-Moreno R, Campos JE, Aguilar-Osorio G, Benitez-Cardoza CG, Trejo-Estrada S, Hidalgo-Lara ME (2017) The thermophilic biomass-degrading fungus Thielavia terrestris Co3Bag1 produces a hyperthermophilic and thermostable β-1, 4-xylanase with exo-and endo-activity. Extremophiles 21:175–186PubMedCrossRefGoogle Scholar
  34. Ghimire PS, Jin C (2017) Genetics, molecular, and proteomics advances in filamentous fungi. Curr Microbiol 74:1226–1236CrossRefGoogle Scholar
  35. Goncalves GA, Takasugi Y, Jia L, Mori Y, Noda S, Tanaka T, Ichinose H, Kamiya N (2015) Synergistic effect and application of xylanases as accessory enzymes to enhance the hydrolysis of pretreated bagasse. Enzym Microb Technol 72:16–24CrossRefGoogle Scholar
  36. Gopalan N, Rodriguez-Duran L, Saucedo-Castaneda G, Nampoothiri KM (2015) Review on technological and scientific aspects of feruloyl esterases: a versatile enzyme for biorefining of biomass. Bioresour Technol 193:534–544PubMedCrossRefGoogle Scholar
  37. Gupta A, Verma JP (2015) Sustainable bio-ethanol production from agro-residues: a review. Renew Sust Energ Rev 41:550–567CrossRefGoogle Scholar
  38. Gusakov AV, Salanovich TN, Antonov AI, Ustinov BB, Okunev ON, Burlingame R, Emalfarb M, Baez M, Sinitsyn AP (2007) Design of highly efficient cellulase mixtures for enzymatic hydrolysis of cellulose. Biotechnol Bioeng 97:1028–1038PubMedCrossRefGoogle Scholar
  39. Hakulinen N, Turunen O, Janis J, Leisola M, Rouvinen J (2003) Three-dimensional structures of thermophilic β-1, 4-xylanases from Chaetomium thermophilum and Nonomuraea flexuosa: comparison of twelve xylanases in relation to their thermal stability. Eur J Biochem 270:1399–1412PubMedCrossRefGoogle Scholar
  40. Harris AD, Ramalingam C (2010) Xylanases and its application in food industry: a review. J Exp Sci 1:1–11Google Scholar
  41. Harris PV, Welner D, McFarland K, Re E, Navarro Poulsen JC, Brown K, Salbo R, Ding H, Vlasenko E, Merino S (2010) Stimulation of lignocellulosic biomass hydrolysis by proteins of glycoside hydrolase family 61: structure and function of a large, enigmatic family. Biochemistry 49:3305–3316PubMedPubMedCentralCrossRefGoogle Scholar
  42. Henrissat B, Davies G (1997) Structural and sequence-based classification of glycoside hydrolases. Curr Opin Struct Biol 7:637–644PubMedCrossRefGoogle Scholar
  43. Huang X, Lin J, Ye X, Wang G (2015) Molecular characterization of a thermophilic and salt-and alkaline-tolerant xylanase from Planococcus sp. SL4, a strain isolated from the sediment of a soda lake. J Microbiol Biotechnol 25:662–671PubMedCrossRefGoogle Scholar
  44. Hutchinson MI, Powell AJ, Tsang A, O’Toole N, Berka RM, Barry K, Grigoriev IV, Natvig DO (2016) Genetics of mating in members of the Chaetomiaceae as revealed by experimental and genomic characterization of reproduction in Myceliophthora heterothallica. Fungal Genet Biol 86:9–19PubMedCrossRefGoogle Scholar
  45. Karnaouri A, Topakas E, Antonopoulou I, Christakopoulos P (2014a) Genomic insights into the fungal lignocellulolytic system of Myceliophthora thermophila. Front Microbiol 5:1–22CrossRefGoogle Scholar
  46. Karnaouri AC, Topakas E, Christakopoulos P (2014b) Cloning, expression, and characterization of a thermostable GH7 endoglucanase from Myceliophthora thermophila capable of high-consistency enzymatic liquefaction. Appl Microbiol Biotechnol 98:231–242PubMedPubMedCentralCrossRefGoogle Scholar
  47. Karnaouri A, Matsakas L, Topakas E, Rova U, Christakopoulos P (2016) Development of thermophilic tailor-made enzyme mixtures for the bioconversion of agricultural and forest residues. Front Microbiol 7:1–14CrossRefGoogle Scholar
  48. Katapodis P, Vrsanska M, Kekos D, Nerinckx W, Biely P, Claeyssens M, Macris BJ, Christakopoulos P (2003) Biochemical and catalytic properties of an endoxylanase purified from the culture filtrate of Sporotrichum thermophile. Carbohydr Res 338:1881–1890PubMedCrossRefGoogle Scholar
  49. Katapodis P, Christakopoulou V, Christakopoulos P (2006) Optimization of xylanase production by Sporotrichum thermophile using corn cobs and response surface methodology. Eng Life Sci 6:410–415CrossRefGoogle Scholar
  50. Katayama T, Tanaka Y, Okabe T, Nakamura H, Fujii W, Kitamoto K, Maruyama J-I (2016) Development of a genome editing technique using the CRISPR/Cas9 system in the industrial filamentous fungus Aspergillus oryzae. Biotechnol Lett 38:637–642PubMedCrossRefGoogle Scholar
  51. Kaur G, Satyanarayana T (2004) Production of extracellular pectinolytic, cellulolytic and xylanolytic enzymes by thermophilic mould Sporotrichum thermophile Apinis in solid state fermentation. Indian J Biotechnol 3:552–557Google Scholar
  52. Kaur G, Kumar S, Satyanarayana T (2004) Production, characterization and application of a thermostable polygalacturonase of a thermophilic mould Sporotrichum thermophile. Apinis. Bioresour Technol 94:239–243PubMedCrossRefGoogle Scholar
  53. Kocabas DS, Güder S, Ozben N (2015) Purification strategies and properties of a low-molecular weight xylanase and its application in agricultural waste biomass hydrolysis. J Mol Catal B Enzym 115:66–75CrossRefGoogle Scholar
  54. Kolbusz MA, Di Falco M, Ishmael N, Marqueteau S, Moisan M-C, Baptista CDS, Powlowski J, Tsang A (2014) Transcriptome and exoproteome analysis of utilization of plant-derived biomass by Myceliophthora thermophila. Fungal Genet Biol 72:10–20PubMedCrossRefGoogle Scholar
  55. Kshirsagar SD, Saratale GD, Saratale RG, Govindwar SP, Oh MK (2016) An isolated Amycolatopsis sp. GDS for cellulase and xylanase production using agricultural waste biomass. J Appl Microbiol 120:112–125PubMedCrossRefGoogle Scholar
  56. Kumar V, Marin-Navarro J, Shukla P (2016) Thermostable microbial xylanases for pulp and paper industries: trends, applications and further perspectives. World J Microbiol Biotechnol 32:1–10CrossRefGoogle Scholar
  57. Kumari A, Satyanarayana T, Singh B (2016) Mixed substrate fermentation for enhanced phytase production by thermophilic mould Sporotrichum thermophile and its application in beneficiation of poultry feed. Appl Biochem Biotechnol 178:197–210PubMedCrossRefGoogle Scholar
  58. Kunamneni A, Ghazi I, Camarero S, Ballesteros A, Plou FJ, Alcalde M (2008) Decolorization of synthetic dyes by laccase immobilized on epoxy-activated carriers. Process Biochem 43:169–178CrossRefGoogle Scholar
  59. Lin XQ, Han S, Zhang N, Hu H, Zheng SP, Ye YR, Lin Y (2013) Bleach boosting effect of xylanase A from Bacillus halodurans C-125 in ECF bleaching of wheat straw pulp. Enzym Microb Technol 52:91–98CrossRefGoogle Scholar
  60. Liu R, Chen L, Jiang Y, Zhou Z, Zou G (2015) Efficient genome editing in filamentous fungus Trichoderma reesei using the CRISPR/Cas9 system. Cell Discov 1:1–11CrossRefGoogle Scholar
  61. Liu Q, Gao R, Li J, Lin L, Zhao J, Sun W, Tian C (2017) Development of a genome-editing CRISPR/Cas9 system in thermophilic fungal Myceliophthora species and its application to hyper-cellulase production strain engineering. Biotechnol Biofuels 10:1–14PubMedPubMedCentralCrossRefGoogle Scholar
  62. Mahmood H, Moniruzzaman M, Yusup S, Akil HM (2016) Pretreatment of oil palm biomass with ionic liquids: a new approach for fabrication of green composite board. J Clean Prod 126:677–685CrossRefGoogle Scholar
  63. Manju S, Singh Chadha B (2011) Production of hemicellulolytic enzymes for hydrolysis of lignocellulosic biomass. In: Pandey A, Larroche C, Ricke SC, Dussap CG, Gnansounou E (eds) Biofuels-alternative feedstocks and conversion processes. Academic Press, Amsterdam, pp 203–228Google Scholar
  64. Margaritis A, Merchant RF, Yaguchi M (1986) Thermostable cellulases from thermophilic microorganisms. Crit Rev Biotechnol 4:327–367CrossRefGoogle Scholar
  65. Marsh K, Boxall J, Lichtenthaler R (2004) Room temperature ionic liquids and their mixtures—a review. Fluid Phase Equilib 219:93–98CrossRefGoogle Scholar
  66. McPhillips K, Waters DM, Parlet C, Walsh DJ, Arendt EK, Murray PG (2014) Purification and characterisation of a β-1, 4-xylanase from Remersonia thermophila CBS 540.69 and its application in bread making. Appl Biochem Biotechnol 172:1747–1762PubMedCrossRefGoogle Scholar
  67. Menon V, Rao M (2012) Trends in bioconversion of lignocellulose: biofuels, platform chemicals & biorefinery concept. Prog Energy Combust Sci 38:522–550CrossRefGoogle Scholar
  68. Mitra S, Mukhopadhyay BC, Mandal AR, Arukha AP, Chakrabarty K, Das GK, Chakrabartty PK, Biswas SR (2015) Cloning, overexpression, and characterization of a novel alkali-thermostable xylanase from Geobacillus sp. WBI J Basic Microbiol 55:527–537PubMedCrossRefGoogle Scholar
  69. Moreira L (2016) Insights into the mechanism of enzymatic hydrolysis of xylan. Appl Microbiol Biotechnol 100:5205–5214PubMedCrossRefGoogle Scholar
  70. Neto YA, de Oliveira LC, de Oliveira AH, Rosa JC, Juliano MA, Juliano L, Rodrigues A, Cabral H (2015) Determination of specificity and biochemical characteristics of neutral protease isolated from Myceliophthora thermophila. Protein Pept Lett 22:972–982PubMedCrossRefGoogle Scholar
  71. Nodvig CS, Nielsen JB, Kogle ME, Mortensen UH (2015) A CRISPR-Cas9 system for genetic engineering of filamentous fungi. PLoS One 10:e0133085PubMedPubMedCentralCrossRefGoogle Scholar
  72. Pahkala K, Kontturi M, Kallioinen A, Myllymaki O, Uusitalo J, Siika-Aho M, von Weymarn N (2007) Production of bio-ethanol from barley straw and reed canary grass: a raw material study. Paper presented at the 15th European biomass conference and exhibition, Berlin, Germany, 7–11 MayGoogle Scholar
  73. Patel SJ, Savanth VD (2015) Review on fungal xylanases and their applications. Int J Adv Res 3:311–315Google Scholar
  74. Ping L, Wang M, Yuan X, Cui F, Huang D, Sun W, Zou B, Huo S, Wang H (2017) Production and characterization of a novel acidophilic and thermostable xylanase from Thermoascus aurantiacus. Int J Biol Macomol 109:1270–1279CrossRefGoogle Scholar
  75. Plecha S, Hall D, Tiquia-Arashiro SM (2013) Screening and characterization of soil microbes capable of degrading cellulose from switchgrass (Panicum virgatum L.). Environ Technol 34:1895–1904PubMedPubMedCentralCrossRefGoogle Scholar
  76. Pohl C, Kiel J, Driessen A, Bovenberg R, Nygard Y (2016) CRISPR/Cas9 based genome editing of Penicillium chrysogenum. ACS Synth Biol 5:754–764PubMedCrossRefGoogle Scholar
  77. Polizeli M, Rizzatti A, Monti R, Terenzi H, Jorge JA, Amorim D (2005) Xylanases from fungi: properties and industrial applications. Appl Microbiol Biotechnol 67:577–591PubMedCrossRefPubMedCentralGoogle Scholar
  78. Ravindran R, Jaiswal AK (2016) A comprehensive review on pre-treatment strategy for lignocellulosic food industry waste: challenges and opportunities. Bioresour Technol 199:92–102PubMedCrossRefGoogle Scholar
  79. Sadaf A, Khare SK (2014) Production of Sporotrichum thermophile xylanase by solid state fermentation utilizing deoiled Jatropha curcas seed cake and its application in xylooligosachharide synthesis. Bioresour Technol 153:126–130PubMedCrossRefGoogle Scholar
  80. Sadaf A, Morya VK, Khare S (2016) Applicability of Sporotrichum thermophile xylanase in the in situ saccharification of wheat straw pre-treated with ionic liquids. Process Biochem 51:2090–2096CrossRefGoogle Scholar
  81. Sadaf A, Grewal J, Khare SK (2018) Ionic liquid stable cellulases and hemicellulases: application in biobased production of biofuels. In: Bhaskar T, Pandey A, Mohan SV, Lee DJ, Khanal SK (eds) Waste Biorefinery. Elsevier, Amsterdam, pp 505–532CrossRefGoogle Scholar
  82. Saksono B, Sukmarini L (2010) Structural analysis of xylanase from marine thermophilic Geobacillus stearothermophilus in Tanjung Api, Poso, Indonesia. Hayati J Biosci 17:189–195CrossRefGoogle Scholar
  83. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289PubMedCrossRefGoogle Scholar
  84. Sharma A, Parashar D, Satyanarayana T (2016) Acidophilic microbes: biology and applications. In: Rampelotto P (ed) Biotechnology of extremophiles: grand challenges in biology and biotechnology, vol 1. Springer, Cham, pp 215–241CrossRefGoogle Scholar
  85. Singh B (2016) Myceliophthora thermophila syn. Sporotrichum thermophile: a thermophilic mould of biotechnological potential. Crit Rev Biotechnol 36:59–69PubMedCrossRefGoogle Scholar
  86. Singh B, Satyanarayana T (2009) Characterization of a HAP–phytase from a thermophilic mould Sporotrichum thermophile. Bioresour Technol 100:2046–2051PubMedCrossRefPubMedCentralGoogle Scholar
  87. Singh B, Pocas-Fonseca MJ, Johri B, Satyanarayana T (2016) Thermophilic molds: biology and applications. Crit Rev Microbiol 42:985–1006PubMedPubMedCentralCrossRefGoogle Scholar
  88. Tadesse H, Luque R (2011) Advances on biomass pretreatment using ionic liquids: an overview. Energy Environ Sci 4:3913–3929CrossRefGoogle Scholar
  89. Taibi Z, Saoudi B, Boudelaa M, Trigui H, Belghith H, Gargouri A, Ladjama A (2012) Purification and biochemical characterization of a highly thermostable xylanase from Actinomadura sp. strain Cpt20 isolated from poultry compost. Appl Biochem Biotechnol 166:663–679PubMedCrossRefPubMedCentralGoogle Scholar
  90. Takahashi Y, Kawabata H, Murakami S (2013) Analysis of functional xylanases in xylan degradation by Aspergillus niger E-1 and characterization of the GH family 10 xylanase XynVII. Springerplus 2:1–11CrossRefGoogle Scholar
  91. Thomas MF, Li LL, Handley-Pendleton JM, Van der Lelie D, Dunn JJ, Wishart JF (2011) Enzyme activity in dialkyl phosphate ionic liquids. Bioresour Technol 102:11200–11203PubMedCrossRefGoogle Scholar
  92. Thuy Pham TP, Cho CW, Yun YS (2010) Environmental fate and toxicity of ionic liquids: a review. Water Res 44:352–372CrossRefGoogle Scholar
  93. Tiquia-Arashiro SM, Mormile M (2013) Sustainable technologies: bioenergy and biofuel from biowaste and biomass. Environ Technol 34(13):1637–1805PubMedCrossRefGoogle Scholar
  94. Topakas E, Katapodis P, Kekos D, Macris BJ, Christakopoulos P (2003) Production and partial characterization of xylanase by Sporotrichum thermophile under solid-state fermentation. World J Microbiol Biotechnol 19:195–198CrossRefGoogle Scholar
  95. Topakas E, Stamatis H, Biely P, Christakopoulos P (2004) Purification and characterization of a type B feruloyl esterase (StFAE-A) from the thermophilic fungus Sporotrichum thermophile. Appl Microbiol Biotechnol 63:686–690PubMedCrossRefPubMedCentralGoogle Scholar
  96. Turner MB, Spear SK, Huddleston JG, Holbrey JD, Rogers RD (2003) Ionic liquid salt-induced inactivation and unfolding of cellulase from Trichoderma reesei. Green Chem 5:443–447CrossRefGoogle Scholar
  97. Vafiadi C, Christakopoulos P, Topakas E (2010) Purification, characterization and mass spectrometric identification of two thermophilic xylanases from Sporotrichum thermophile. Process Biochem 45:419–424CrossRefGoogle Scholar
  98. van den Brink J, van Muiswinkel GC, Theelen B, Hinz SW, de Vries RP (2012) Efficient plant biomass degradation by the thermophilic fungus Myceliophthora heterothallica. Appl Environ Microbiol 79:1316–1324PubMedCrossRefPubMedCentralGoogle Scholar
  99. Van Gool M, Van Muiswinkel G, Hinz S, Schols H, Sinitsyn A, Gruppen H (2012) Two GH10 endo-xylanases from Myceliophthora thermophila C1 with and without cellulose binding module act differently towards soluble and insoluble xylans. Bioresour Technol 119:123–132PubMedCrossRefPubMedCentralGoogle Scholar
  100. Van Gool MP, Van Muiswinkel GCJ, Hinz SWA, Schols HA, Sinitsyn AP, Gruppen H (2013) Two novel GH11 endo-xylanases from Myceliophthora thermophila C1 act differently toward soluble and insoluble xylans. Enzym Microb Technol 53:25–32CrossRefGoogle Scholar
  101. Vardakou M, Katapodis P, Samiotaki M, Kekos D, Panayotou G, Christakopoulos P (2003) Mode of action of family 10 and 11 endoxylanases on water-unextractable arabinoxylan. Int J Biol Macomol 33:129–134CrossRefGoogle Scholar
  102. Verma D, Kawarabayasi Y, Miyazaki K, Satyanarayana T (2013) Cloning, expression and characteristics of a novel alkalistable and thermostable xylanase encoding gene (Mxyl) retrieved from compost-soil metagenome. PLoS One 8:e52459PubMedPubMedCentralCrossRefGoogle Scholar
  103. Viikari L, Alapuranen M, Puranen T, Vehmaanpera J, Siika-Aho M (2007) Thermostable enzymes in lignocellulose hydrolysis. In: Olsson L (ed) Biofuels: advances in biochemical engineering/biotechnology, vol 108. Springer, Berlin, Heidelberg, pp 121–145CrossRefGoogle Scholar
  104. Wang Y, Fu Z, Huang H, Zhang H, Yao B, Xiong H, Turunen O (2012) Improved thermal performance of Thermomyces lanuginosus GH11 xylanase by engineering of an N-terminal disulfide bridge. Bioresour Technol 112:275–279PubMedCrossRefGoogle Scholar
  105. Wang J, Mai G, Liu G, Yu S (2013) Molecular cloning and heterologous expression of an acid-stable endoxylanase gene from Penicillium oxalicum in Trichoderma reesei. J Microbiol Biotechnol 23:251–259PubMedCrossRefPubMedCentralGoogle Scholar
  106. Wang G, Wu J, Yan R, Lin J, Ye X (2017) A novel multi-domain high molecular, salt-stable alkaline xylanase from Alkalibacterium sp. SL3. Front Microbiol 7:2120PubMedPubMedCentralGoogle Scholar
  107. Watanabe M, Fukada H, Ishikawa K (2016) Construction of thermophilic xylanase and its structural analysis. Biochemistry 55:4399–4409PubMedCrossRefPubMedCentralGoogle Scholar
  108. Weerachavangkul C, Laothanachareon T, Boonyapakron K, Wongwilaiwalin S, Nimchua T, Eurwilaichitr L, Pootanakit K, Igarashi Y, Champreda V (2012) Alkaliphilic endoxylanase from lignocellulolytic microbial consortium metagenome for biobleaching of eucalyptus pulp. J Microbiol Biotechnol 22:1636–1643PubMedCrossRefPubMedCentralGoogle Scholar
  109. Wojtczak G, Breuil C, Yamada J, Saddler J (1987) A comparison of the thermostability of cellulases from various thermophilic fungi. Appl Microbiol Biotechnol 27:82–87CrossRefGoogle Scholar
  110. Xu G, Li J, Liu Q, Sun W, Jiang M, Tian C (2018) Transcriptional analysis of Myceliophthora thermophila on soluble starch and role of regulator AmyR on polysaccharide degradation. Bioresour Technol 265:558–562PubMedCrossRefGoogle Scholar
  111. Ye Z, Zheng Y, Li B, Borrusch MS, Storms R, Walton JD (2014) Enhancement of synthetic Trichoderma-based enzyme mixtures for biomass conversion with an alternative family 5 glycosyl hydrolase from Sporotrichum thermophile. PLoS One 9:e109885PubMedPubMedCentralCrossRefGoogle Scholar
  112. Yegin S (2017) Single-step purification and characterization of an extreme halophilic, ethanol tolerant and acidophilic xylanase from Aureobasidium pullulans NRRL Y-2311-1 with application potential in the food industry. Food Chem 221:67–75PubMedCrossRefGoogle Scholar
  113. Zeldes BM, Keller MW, Loder AJ, Straub CT, Adams MW, Kelly RM (2015) Extremely thermophilic microorganisms as metabolic engineering platforms for production of fuels and industrial chemicals. Front Microbiol 6:1–17CrossRefGoogle Scholar
  114. Zhang Y, An J, Yang G, Zhang X, Xie Y, Chen L, Feng Y (2016) Structure features of GH10 xylanase from Caldicellulosiruptor bescii: implication for its thermophilic adaption and substrate binding preference. Acta Biochim Biophys Sin 48:948–957PubMedCrossRefGoogle Scholar
  115. Zhuo R, Yu H, Qin X, Ni H, Jiang Z, Ma F, Zhang X (2018) Heterologous expression and characterization of a xylanase and xylosidase from white rot fungi and their application in synergistic hydrolysis of lignocellulose. Chemosphere 212:24–33PubMedCrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of ChemistryIndian Institute of Technology DelhiHauz KhasIndia

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