Fungal Glycoside Hydrolases of White-Rot Fungi for Cellulosic Biofuels Production: A Review

Sunardi1,2,*,, Wiwin Tyas Istikowati3, Futoshi Ishiguri4 and Shinso Yokota4

1Department of Chemistry, Faculty of Mathematics and Natural Sciences, Lambung Mangkurat University, Banjarbaru 70714, Indonesia

2Wetland-Based Materials Research Center, Lambung Mangkurat University, Banjarbaru 70714, Indonesia

3Faculty of Forestry, Lambung Mangkurat University, Banjarbaru 70714 Indonesia

4Faculty of Agriculture, Utsunomiya University, Utsunomiya, Tochigi 321-8505, Japan

*Corresponding author: E-mail:;


The second generation bioethanol production from lignocellulose materials through environmental friendly methods is one of the biggest challenges on industrial application. Enzymatic hydrolysis of cellulose has more benefits compared with the acid hydrolysis. This method has the good specificity, low consumption of energy and chemicals and is more environmental friendly. However, the utilization of lignocellulose for bioethanol production through enzymatic methods is still confronting several difficulties for commercialization. Cellulose hydrolysis step has been reported to be the bottleneck of bioethanol production by enzymatic process, and the major barrier of this process is high price of enzymes, which making the process less economically feasible. For this reason, many developments are still needed in cellulase production from various organisms for cellulose saccharification. White-rot fungi have received much consideration for their valuable enzyme systems which can effective degrade lignocellulose biomass. These fungi could secrete extracellular oxidative and hydrolytic enzymes that degrade lignin, hemicellulose, and cellulose. This review provides a complete overview of the glycoside hydrolases enzymes production by white-rot fungus, such as endoglucanase, exoglucanase, β-glucosidase, cellobiose dehydrogenase and lytic polysaccharide monooxygenase. The use of white-rot fungus for low cost glycoside hydrolases enzymes production might be fascinating for second generation bioethanol production.


White-rot fungi, Biofuels, Glycoside hydrolases, Enzymatic hydrolysis, Enzymes.

Reference (119)

1.M.E. Himmel, S.Y. Ding, D.K. Johnson, W.S. Adney, M.R. Nimlos, J.W. Brady and T.D. Foust, Science, 315, 804 (2007);

2.M.D. Sweeney and F. Xu, Catalysts, 2, 244 (2012);

3.X.F. Tian, Z. Fang and F. Guo, Biofuels Bioprod. Biorefin., 6, 335 (2012);

4.M. Galbe and G. Zacchi, ed.: L. Olsson, Pretreatment of Lignocellulosic Materials for Efficient Bioethanol Production, In: Biofuels, Springer-Verlag, New York, pp. 41-65 (2007).

5.M. Taha, M. Foda, E. Shahsavari, A. Aburto-Medina, E. Adetutu and A. Ball, Curr. Opin. Biotechnol., 38, 190 (2016);

6.S.B.A. Hamid, M.M. Islam and R. Das, Cellulose, 22, 2157 (2015);

7.J. Zhuang, M.A. Marchant, S.E. Nokes and H.J. Strobel, Appl. Eng. Agric., 23, 679 (2007);

8.C.M. Phillips, I.V.W.T. Beeson IV, J.H. Cate and M.A. Marletta, ACS Chem. Biol., 6, 1399 (2011);

9.L. Viikari, J. Vehmaanperä and A. Koivula, Biomass Bioenergy, 46, 13 (2012);

10.V. Elisashvili, E. Kachlishvili, N. Tsiklauri, E. Metreveli, T. Khardziani and S.N. Agathos, World J. Microb. Biot., 25, 331 (2009);

11.T. Manavalan, A. Manavalan and K. Heese, Curr. Microbiol., 70, 485 (2015);

12.A. Manavalan, S.S. Adav and S.K. Sze, J. Proteomics, 75, 642 (2011);

13.S. Haghighi Mood, A. Hossein Golfeshan, M. Tabatabaei, G.S. Jouzani, G.H. Najafi, M. Gholami and M. Ardjmand, Renew. Sustain. Energy Rev., 27, 77 (2013);

14.A. Sørensen, M. Lübeck, P.S. Lübeck and B.K. Ahring, Biomolecules, 3, 612 (2013);

15.V. Menon and M. Rao, Pror. Energy Combust. Sci., 38, 522 (2012);

16.A. Eisentraut, International Energy Agency, Paris, pp. 217 (2010).

17.P. Lozano, B. Bernal, A.G. Jara and M.P. Belleville, Bioresour. Technol., 151, 159 (2014);

18.L. Rosgaard, S. Pedersen, J. Langston, D. Akerhielm, J.R. Cherry and A.S. Meyer, Biotechnol. Prog., 23, 1270 (2007);

19.C. Lehmann, F. Sibilla, Z. Maugeri, W.R. Streit, P. Domínguez de María, R. Martinez and U. Schwaneberg, Green Chem., 14, 2719 (2012);

20.J. Pérez, J. Muñoz-Dorado, T. de la Rubia and J. Martínez, Int. Microbiol., 5, 53 (2002);

21.S. Prasad, A. Singh and H.C. Joshi, Resour. Conserv. Recycl., 50, 1 (2007);

22.A.C. O’Sullivan, Cellulose, 4, 173 (1997);

23.D.N.S. Hon, Cellulose, 1, 1 (1994);

24.R.F.H. Dekker, ed.: T. Higuchi, Biodegradation of Hemicelluloses, In:  Biosynthesis and Biodegradation of Wood Components, Academic Press, New York, pp. 505-533 (1985).

25.T. Watanabe, J. Ohnishi, Y. Yamasaki, S. Kaizu and T. Koshijima, Agric. Biol. Chem., 53, 2233 (1989).

26.E. Sjöström, Wood Chemistry: Fundamentals and Applications, Academic Press: New York, edn 2, pp. 293 (1993).

27.A. Hatakka and K.E. Hammel, ed.: M. Hofrichter, Fungal Biodegra-dation of Lignocelluloses, In: The Mycota X. Industrial Applications, Springer-Verlag: Heidelberg, edn 2, pp. 319-340 (2010).

28.C. Alvarez, F.M. Reyes-Sosa and B. Díez, Microb. Biotechnol., 9, 149 (2016);

29.L. Otjen and R.A. Blanchette, Can. J. Bot., 64, 905 (1986);

30.A. Abbas, H. Koc, F. Liu and M. Tien, Curr. Genet., 47, 49 (2005);

31.S. Watkinson, D. Bebber, P. Darrah, M. Fricker, M. Tlalka and L. Boddy, ed.: G.M. Gadd, The Role of Wood Decay Fungi in the Carbon and Nitrogen Dynamics of the Forest Floor, In: Fungi in Biogeochemical Cycles, Cambridge University Press, Cambridge, pp. 151-181 (2006).

32.S. Malherbe and T.E. Cloete, Rev. Environ. Sci. Bio., 1, 105 (2002);

33.M. Dashtban, H. Schraft and W. Qin, Int. J. Biol. Sci., 5, 578 (2009);

34.I. Kamei, Y. Hirota and S. Meguro, Bioresour. Technol., 126, 137 (2012);

35.R.A. Blanchette, Can. J. Bot., 73(S1), 999 (1995);

36.K.E. Eriksson and B. Pettersson, Eur. J. Biochem., 51, 213 (1975);

37.L. Otjen, R. Blanchette, M. Effland and G. Leatham, Holzforschung, 41, 343 (1987);

38.A. Machuca and A. Ferraz, Enzyme Microb. Technol., 29, 386 (2001);

39.H. Tanaka, K. Koike, S. Itakura and A. Enoki, Enzyme Microb. Technol., 45, 384 (2009);

40.T.K. Kirk, Holzforschung, 29, 99 (1975);

41.A.T. Martínez, M. Speranza, F.J. Ruiz-Dueñas, P. Ferreira, S. Camarero, F. Guillén, M.J. Martínez, A. Gutiérrez and J.C. del Río, Int. Microbiol., 8, 195 (2005).

42.C. Sánchez, Biotechnol. Adv., 27, 185 (2009);

43.L. Zifèáková and P. Baldrian, Fungal Ecol., 5, 481 (2012);

44.J. Rytioja, K. Hildén, A. Hatakka and M.R. Mäkelä, Fungal Genet. Biol., 72, 91 (2014);

45.D. Floudas, B.W. Held, R. Riley, L.G. Nagy, G. Koehler, A.S. Ransdell, H. Younus, J. Chow, J. Chiniquy, A. Lipzen, A. Tritt, H. Sun, S. Haridas, K. LaButti, R.A. Ohm, U. Kües, R.A. Blanchette, I.V. Grigoriev, R.E. Minto and D.S. Hibbett, Fungal Genet. Biol., 76, 78 (2015);

46.A.L. Demain, M. Newcomb and J.H.D. Wu, Microbiol. Mol. Biol. Rev., 69, 124 (2005);

47.S. Dutta and K.C.W. Wu, Green Chem., 16, 4615 (2014);

48.B. Henrissat, I. Callebaut, S. Fabrega, P. Lehn, J.P. Mornon and G. Davies, Proc. Natl. Acad. Sci. USA, 92, 7090 (1995);

49.B. Henrissat, Biochem. J., 280, 309 (1991);

50.V. Lombard, H. Golaconda Ramulu, E. Drula, P.M. Coutinho and B. Henrissat, Nucleic Acids Res., 42(D1), D490 (2014);

51.B. Henrissat and G. Davies, Curr. Opin. Struct. Biol., 7, 637 (1997);

52.L.R. Lynd, P.J. Weimer, W.H. van Zyl and I.S. Pretorius, Microbiol. Mol. Biol. Rev., 66, 506 (2002);

53.M. Sandgren, J. Ståhlberg and C. Mitchinson, Prog. Biophys. Mol. Biol., 89, 246 (2005);

54.C. Wan and Y. Li, Biotechnol. Adv., 30, 1447 (2012);

55.L. Levin, L. Villalba, V. Da Re, F. Forchiassin and L. Papinutti, Process Biochem., 42, 995 (2007);

56.P. Tomme, R.A.J. Warren and N.R. Gilkes, Adv. Microb. Physiol., 37, 1 (1995);

57.C.M. Payne, B.C. Knott, H.B. Mayes, H. Hansson, M.E. Himmel, M. Sandgren, J. Ståhlberg and G.T. Beckham, Chem. Rev., 115, 1308 (2015);

58.D.R. Schmidhalter and G. Canevascini, Arch. Biochem. Biophys., 300, 551 (1993);

59.P. Baldrian and V. Valášková, FEMS Microbiol. Rev., 32, 501 (2008);

60.I. Herpoël-Gimbert, A. Margeot, A. Dolla, G. Jan, D. Mollé, S. Lignon, H. Mathis, J.C. Sigoillot, F. Monot and M. Asther, Biotechnol. Biofuels, 1, 18 (2008);

61.B. Sipos, Z. Benkõ, D. Dienes, K. Réczey, L. Viikari and M. Siika-aho, Appl. Biochem. Biotechnol., 161, 347 (2010);

62.S.P.S. Chundawat, M.S. Lipton, S.O. Purvine, N. Uppugundla, D. Gao, V. Balan and B.E. Dale, J. Proteome Res., 10, 4365 (2011);

63.K.M. Bhat and R. Maheshwari, Appl. Environ. Microbiol., 53, 2175 (1987);

64.A.M.V. Garzillo, S.D. Paolo, M. Ruzzi and V. Buonocore, Appl. Microbiol. Biotechnol., 42, 476 (1994);

65.M. Jeya, Y.W. Zhang, I.W. Kim and J.K. Lee, Bioresour. Technol., 100, 5155 (2009);

66.A.A. Dias, G.S. Freitas, G.S.M. Marques, A. Sampaio, I.S. Fraga, M.A.M. Rodrigues, D.V. Evtuguin and R.M.F. Bezerra, Bioresour. Technol., 101, 6045 (2010);

67.F. Ma, J. Wang, Y. Zeng, H. Yu, Y. Yang and X. Zhang, Process Biochem., 46, 1767 (2011);

68.X.Q. Dong, J.S. Yang, N. Zhu, E.T. Wang and H.L. Yuan, Bioresour. Technol., 131, 443 (2013);

69.S.S. Jagtap, S.S. Dhiman, T.S. Kim, J. Li, J.K. Lee and Y.C. Kang, Bioresour. Technol., 133, 307 (2013);

70.Sunardi, J. Tanabe, F. Ishiguri, J. Ohshima, K. Iizuka and S. Yokota, Int. Biodeter. Biodegr., 110, 108 (2016);

71.Sunardi, A. Nakamura, F. Ishiguri and S. Yokota, Asian J. Chem., 30, 317 (2018);

72.D.B. Wilson, Ann. N. Y. Acad. Sci., 1125, 289 (2008);

73.Y. Li, D.C. Irwin and D.B. Wilson, Appl. Environ. Microbiol., 76, 2582 (2010);

74.S.J. Horn, G. Vaaje-Kolstad, B. Westereng and V.G.H. Eijsink, Biotechnol. Biofuels, 5, 45 (2012);

75.J. Fang, Y. Qu and P. Gao, Biotechnol. Tech., 11, 195 (1997);

76.E. Kachlishvili, M.J. Penninckx, N. Tsiklauri and V. Elisashvili, World J. Microbiol. Biotechnol., 22, 391 (2006);

77.M. Jeya, N.P.T. Nguyen, H.J. Moon, S.H. Kim and J.K. Lee, Bioresour. Technol., 101, 8742 (2010);

78.J. Eyzaguirre, M. Hidalgo and A. Leschot, Handbook of Carbohydrate Engineering. Taylor & Francis, New York, pp. 645-758 (2005).

79.B.E. Lechner and V.L. Papinutti, Process Biochem., 41, 594 (2006);

80.G. Henriksson, P. Ander, B. Pettersson and G. Pettersson, Appl. Microbiol. Biotechnol., 42, 790 (1995);

81.G. Henriksson, V. Sild, I.J. Szabó, G. Pettersson and G. Johansson, Biochim. Biophys. Acta, 1383, 48 (1998);

82.G. Henriksson, G. Johansson and G. Pettersson, J. Biotechnol., 78, 93 (2000);

83.M. Zamocky, R. Ludwig, C. Peterbauer, B.M. Hallberg, C. Divne, P. Nicholls and D. Haltrich, Curr. Protein Pept. Sci., 7, 255 (2006);

84.A. Hüttermann and A. Noelle, Holzforschung, 36, 283 (1982);

85.B.P. Roy, T. Dumonceaux, A.A. Koukoulas and F.S. Archibald, Appl. Environ. Microbiol., 62, 4417 (1996);

86.U. Temp and C. Eggert, Appl. Environ. Microbiol., 65, 389 (1999);

87.M. Yoshida, T. Ohira, K. Igarashi, H. Nagasawa and M. Samejima, FEMS Microbiol. Lett., 217, 225 (2002);

88.R. Ludwig, A. Salamon, J. Varga, M. Zámocky, C.K. Peterbauer, K.D. Kulbe and D. Haltrich, Appl. Microbiol. Biotechnol., 64, 213 (2004);

89.S. Nakagame, A. Furujyo and J. Sugiura, Biosci. Biotechnol. Biochem., 70, 1629 (2006);

90.M. Bey, J.G. Berrin, L. Poidevin and J.C. Sigoillot, Microb. Cell Fact., 10, 113 (2011);

91.J. Sulej, G. Janusz, A. Mazur, K. Zuber, A. Zebracka and J. Rogalski, Process Biochem., 48, 1715 (2013);

92.G. Vaaje-Kolstad, B. Westereng, S.J. Horn, Z. Liu, H. Zhai, M. Sørlie and V.G.H. Eijsink, Science, 330, 219 (2010);

93.J.A. Langston, T. Shaghasi, E. Abbate, F. Xu, E. Vlasenko and M.D. Sweeney, Appl. Environ. Microbiol., 77, 7007 (2011);

94.C. Sygmund, D. Kracher, S. Scheiblbrandner, K. Zahma, A.K.G. Felice, W. Harreither, R. Kittl and R. Ludwig, Appl. Environ. Microbiol., 78, 6161 (2012);

95.R.J. Quinlan, M.D. Sweeney, L. Lo Leggio, H. Otten, J.-C.N. Poulsen, K.S. Johansen, K.B.R.M. Krogh, C.I. Jorgensen, M. Tovborg, A. Anthonsen, T. Tryfona, C.P. Walter, P. Dupree, F. Xu, G.J. Davies and P.H. Walton, Proc. Natl. Acad. Sci. USA, 108, 15079 (2011);

96.E.M. Turner, M. Wright, T. Ward, D.J. Osborne and R. Self, J. Gen. Microbiol., 91, 167 (1975);

97.J.Y. Lu and A.Y. Tang, J. Food Sci., 51, 668 (1986);

98.F.O. Heidorne, P.O. Magalhães, A.L. Ferraz and A.M.F. Milagres, Enzyme Microb. Technol., 38, 436 (2006);

99.P.O. Magalhães, A. Ferraz and A.F.M. Milagres, J. Appl. Microbiol., 101, 480 (2006);

100.M. Streamer, K.E. Eriksson and B. Pettersson, Eur. J. Biochem., 59, 607 (1975);

101.V. Deshpande, K.E. Eriksson and B. Pettersson, Eur. J. Biochem., 90, 191 (1978);

102.X. Rouau and E. Odier, Enzyme Microb. Technol., 8, 22 (1986);

103.J. Mallerman, L. Papinutti and L. Levin, J. Microbiol. Biotechnol., 25, 57 (2015);

104.T. Vìtrovský, P. Baldrian and J. Gabriel, Appl. Biochem. Biotechnol., 169, 100 (2013);

105.S. Sik and A. Ünyayar, Turk. J. Biol., 22, 287 (1998).

106.D.N.X. Salmon, M.R. Spier, C.R. Soccol, L.P. Vandenberghe, V. Weingartner Montibeller, M.C.J. Bier and V. Faraco, Fungal Biol., 118, 655 (2014);

107.R. Sasidhara and T. Thirunalasundari, Eur. J. Exp. Biol., 4, 375 (2014).

108.B. Hegarty, A. Steinfurth, W. Liese and O. Schmidt, Holzforschung, 41, 265 (1987);

109.T. Kanda, K. Wakabayashi and K. Nisizawa, J. Biochem., 79, 977 (1976);

110.E.S. Lymar, B. Li and V. Renganathan, Appl. Environ. Microbiol., 61, 2976 (1995);

111.K. Igarashi, M. Samejima and K.E.L. Eriksson, Eur. J. Biochem., 253, 101 (1998);

112.C. Sigoillot, A. Lomascolo, E. Record, J.L. Robert, M. Asther and J.C. Sigoillot, Enzyme Microb. Technol., 31, 876 (2002);

113.H. Morais, C. Ramos, N. Matos, E. Forgács, T. Cserháti, V. Almeida, J. Oliveira, Y. Darwish and Z. Illés, J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 770, 111 (2002);

114.A.C. Lo, J.R. Barbier and G.E. Willick, Eur. J. Biochem., 192, 175 (1990);

115.R. Maheshwari, G. Bharadwaj and M.K. Bhat, Microbiol. Mol. Biol. Rev., 64, 461 (2000);

116.I. Irbe, V. Elisashvili, M.D. Asatiani, A. Janberga, I. Andersone, B. Andersons, V. Biziks and J. Grinins, Inter. Biodeter. Biodegrad., 86, 71 (2014);

117.X. Li, J. Pei, G. Wu and W. Shao, Biotechnol. Lett., 27, 1369 (2005);

118.Y.J. Cai, S.J. Chapman, J.A. Buswell and S.T. Chang, Appl. Environ. Microbiol., 65, 553 (1999);

119.C. Liers, R. Ullrich, K.T. Steffen, A. Hatakka and M. Hofrichter, Appl. Microbiol. Biotechnol., 69, 573 (2006);

   View Article PDF File Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.