Insights into high-efficiency lignocellulolytic enzyme production by Penicillium oxalicum GZ-2 induced by a complex substrate

Biotechnology for Biofuels

Volumn 7, Issue 1, 2014, Pages

  Liao, Hanpeng ^a   Li, Shuixian ^a   Wei, Zhong ^a   Shen, Qirong ^a   Xu, Yangchun ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

Cellulose and xylan; Gene expression; Lignocellulolytic enzyme; Penicillium oxalicum; Secretome

Indexed keywords

AGRICULTURAL WASTES; BIOMASS; CELLULOSE; GENE EXPRESSION; SUBSTRATES;

CELLOBIOHYDROLASES; CELLULASE PRODUCTION; CELLULOLYTIC ENZYME; COMPLEX SUBSTRATES; LIGNOCELLULOLYTIC ENZYMES; PENICILLIUM OXALICUM; SECRETOME; SYNERGISTIC EFFECT;

ENZYME ACTIVITY;

BIOMASS; CELLULOSE; ENZYME ACTIVITY; FUNGUS; GENE EXPRESSION; PROTEIN;

CELLULOSE; GENETIC ENGINEERING; PROTEINS; XYLANS;

HYPOCREA JECORINA; PENICILLIUM OXALICUM;

EID: 84988893709     PISSN: 17546834     EISSN: None     Source Type: Journal    
DOI: 10.1186/s13068-014-0162-2     Document Type: Article

References (62)

1. Martinez D, Berka RM, Henrissat B, Saloheimo M, Arvas M, Baker SE, Chapman J, Chertkov O, Coutinho PM, Cullen D: Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol 2008, 26:553-560.
2. Merino ST, Cherry J: Progress and challenges in enzyme development for biomass utilization. In Biofuels. Edited by Lisbeth O. Springer Berlin Heidelberg: Springer; 2007:95-120.
3. Marjamaa K, Toth K, Bromann PA, Szakacs G, Kruus K: Novel Penicillium cellulases for total hydrolysis of lignocellulosics. Enzyme Microb Technol 2013, 52:358-369.
4. Liming X, Xueliang S: High-yield cellulase production by Trichoderma reesei ZU-02 on corn cob residue. Bioresour Technol 2004, 91:259-262.
5. Fang X, Yano S, Inoue H, Sawayama S: Lactose enhances cellulase production by the filamentous fungus Acremonium cellulolyticus. J Biosci Bioeng 2008, 106:115-120.
6. Mandels M, Reese ET: Induction of cellulase in fungi by cellobiose. J Bacteriol 1960, 79:816.
7. Sternberg D, Mandels GR: Induction of cellulolytic enzymes in Trichoderma reesei by sophorose. J Bacteriol 1979, 139:761-769.
8. Morikawa Y, Ohashi T, Mantani O, Okada H: Cellulase induction by lactose in Trichoderma reesei PC-3-7. Appl Microbiol Biotechnol 1995, 44:106-111.
9. Karaffa L, Fekete E, Gamauf C, Szentirmai A, Kubicek CP, Seiboth B: D-Galactose induces cellulase gene expression in Hypocrea jecorina at low growth rates. Microbiology 2006, 152:1507-1514.
10. Do Vale LH, Gómez-Mendoza DP, Kim MS, Pandey A, Ricart CA, Edivaldo Filho XF, Sousa MV: Secretome analysis of the fungus Trichoderma harzianum grown on cellulose. Proteomics 2012, 12:2716-2728.
11. Royer JC, Nakas J: Interrelationship of xylanase induction and cellulase induction of Trichoderma longibrachiatum. Appl Environ Microbiol 1990, 56:2535-2539.
12. Liao H, Xu C, Tan S, Wei Z, Ling N, Yu G, Raza W, Zhang R, Shen Q, Xu Y: Production and characterization of acidophilic xylanolytic enzymes from Penicillium oxalicum GZ-2. Bioresour Technol 2012, 123:117-124.
13. Fujii T, Fang X, Inoue H, Murakami K, Sawayama S: Enzymatic hydrolyzing performance of Acremonium cellulolyticus and Trichoderma reesei against three lignocellulosic materials. Biotechnol Biofuels 2009, 2:1-8.
14. Rana V, Eckard AD, Teller P, Ahring BK: On-site enzymes produced from Trichoderma reesei RUT-C30 and Aspergillus saccharolyticus for hydrolysis of wet exploded corn stover and loblolly pine. Bioresour Technol 2014, 154:282-289.
15. Juhasz T, Szengyel Z, Reczey K, Siika-Aho M, Viikari L: Characterization of cellulases and hemicellulases produced by Trichoderma reesei on various carbon sources. Process Biochem 2005, 40:3519-3525.
16. Alriksson B, Rose SH, van Zyl WH, Sjöde A, Nilvebrant N-O, Jönsson LJ: Cellulase production from spent lignocellulose hydrolysates by recombinant Aspergillus niger. Appl Environ Microbiol 2009, 75:2366-2374.
17. Li J, Lin L, Li H, Tian C, Ma Y: Transcriptional comparison of the filamentous fungus Neurospora crassa growing on three major monosaccharides D-glucose, D-xylose and L-arabinose. Biotechnol Biofuels 2014, 7:1-15.
18. Jourdier E, Cohen C, Poughon L, Larroche C, Monot F, Chaabane FB: Cellulase activity mapping of Trichoderma reesei cultivated in sugar mixtures under fed-batch conditions. Biotechnol Biofuels 2013, 6:79-91.
19. Andersen MR, Vongsangnak W, Panagiotou G, Salazar MP, Lehmann L, Nielsen J: A trispecies Aspergillus microarray: comparative transcriptomics of three Aspergillus species. Proc Natl Acad Sci U S A 2008, 105:4387-4392.
20. Delmas S, Pullan ST, Gaddipati S, Kokolski M, Malla S, Blythe MJ, Ibbett R, Campbell M, Liddell S, Aboobaker A: Uncovering the genome-wide transcriptional responses of the filamentous fungus Aspergillus niger to lignocellulose using RNA sequencing. PLoS Genet 2012, 8:e1002875.
21. Munster JMv, Daly P, Delmas S, Pullan ST, Blythe MJ, Malla S, Kokolski M, Noltorp E, Wennberg K, Fetherston R: The role of carbon starvation in the induction of enzymes that degrade plant-derived carbohydrates in Aspergillus niger. Fungal Genet Biol 2014.
22. De Souza WR, Maitan-Alfenas GP, de Gouvêa PF, Brown NA, Savoldi M, Battaglia E, Goldman MHS, de Vries RP, Goldman GH: The influence of Aspergillus niger transcription factors AraR and XlnR in the gene expression during growth in D-xylose, L-arabinose and steam-exploded sugarcane bagasse. Fungal Genet Biol 2013, 60:29-45.
23. Liu D, Li J, Zhao S, Zhang R, Wang M, Miao Y, Shen Y, Shen Q: Secretome diversity and quantitative analysis of cellulolytic Aspergillus fumigatus Z5 in the presence of different carbon sources. Biotechnol Biofuels 2013, 6:149.
24. Saykhedkar S, Ray A, Ayoubi-Canaan P, Hartson SD, Prade R, Mort AJ: A time course analysis of the extracellular proteome of Aspergillus nidulans growing on sorghum stover. Biotechnol Biofuels 2012, 5:1-36.
25. Horta MAC, Vicentini R, da Silva DP, Laborda P, Crucello A, Freitas S, Kuroshu RM, Polikarpov I, da Cruz Pradella JG, Souza AP: Transcriptome profile of Trichoderma harzianum IOC-3844 induced by sugarcane bagasse. PLoS One 2014, 9:e88689.
26. De Souza WR, de Gouvea PF, Savoldi M, Malavazi I, de Souza Bernardes LA, Goldman MHS, de Vries RP, de Castro Oliveira JV, Goldman GH: Transcriptome analysis of Aspergillus niger grown on sugarcane bagasse. Biotechnol Biofuels 2011, 4:1-17.
27. Adav SS, Li AA, Manavalan A, Punt P, Sze SK: Quantitative iTRAQ secretome analysis of Aspergillus niger reveals novel hydrolytic enzymes. J Proteome Res 2010, 9:3932-3940.
28. Alvira P, Gyalai-Korpos M, Barta Z, Oliva JM, Réczey K, Ballesteros M: Production and hydrolytic efficiency of enzymes from Trichoderma reesei RUTC30 using steam pretreated wheat straw as carbon source. J Chem Technol Biotechnol 2013, 88:1150-1156.
29. Jorgensen H, Morkeberg A, Krogh KBR, Olsson L: Production of cellulases and hemicellulases by three Penicillium species: effect of substrate and evaluation of cellulase adsorption by capillary electrophoresis. Enzyme Microb Technol 2005, 36:42-48.
30. Wei X, Zheng K, Chen M, Liu G, Li J, Lei Y, Qin Y, Qu Y: Transcription analysis of lignocellulolytic enzymes of Penicillium decumbens 114-2 and its catabolite-repression-resistant mutant. C R Biol 2011, 334:806-811.
31. Mach-Aigner AR, Pucher ME, Steiger MG, Bauer GE, Preis SJ, Mach RL: Transcriptional regulation of xyr1, encoding the main regulator of the xylanolytic and cellulolytic enzyme system in Hypocrea jecorina. Appl Environ Microbiol 2008, 74:6554-6562.
32. Furukawa T, Shida Y, Kitagami N, Mori K, Kato M, Kobayashi T, Okada H, Ogasawara W, Morikawa Y: Identification of specific binding sites for XYR1, a transcriptional activator of cellulolytic and xylanolytic genes in Trichoderma reesei. Fungal Genet Biol 2009, 46:564-574.
33. Gielkens MM, Dekkers E, Visser J, de Graaff LH: Two cellobiohydrolase-encoding genes from Aspergillus niger require D-xylose and the xylanolytic transcriptional activator XlnR for their expression. Appl Environ Microbiol 1999, 65:4340-4345.
34. Van Peij NN, Gielkens MM, de Vries RP, Visser J, de Graaff LH: The transcriptional activator XlnR regulates both xylanolytic and endoglucanase gene expression in Aspergillus niger. Appl Environ Microbiol 1998, 64:3615-3619.
35. Stricker AR, Steiger MG, Mach RL: Xyr1 receives the lactose induction signal and regulates lactose metabolism in Hypocrea jecorina. FEBS Lett 2007, 581:3915-3920.
36. Mach-Aigner AR, Pucher ME, Mach RL: D-Xylose as a repressor or inducer of xylanase expression in Hypocrea jecorina (Trichoderma reesei). Appl Environ Microbiol 2010, 76(6):1770-1776.
37. Marui J, Tanaka A, Mimura S, de Graaff LH, Visser J, Kitamoto N, Kato M, Kobayashi T, Tsukagoshi N: A transcriptional activator, AoXlnR, controls the expression of genes encoding xylanolytic enzymes in Aspergillus oryzae. Fungal Genet Biol 2002, 35:157-169.
38. Kurasawa T, Yachi M, Suto M, Kamagata Y, Takao S, Tomita F: Induction of cellulase by gentiobiose and its sulfur-containing analog in Penicillium purpurogenum. Appl Environ Microbiol 1992, 58:106-110.
39. Stricker AR, Grosstessner-Hain K, Würleitner E, Mach RL: Xyr1 (xylanase regulator 1) regulates both the hydrolytic enzyme system and D-xylose metabolism in Hypocrea jecorina. Eukaryot Cell 2006, 5:2128-2137.
40. Tani S, Kawaguchi T, Kobayashi T: Complex regulation of hydrolytic enzyme genes for cellulosic biomass degradation in filamentous fungi. Appl Microbiol Biotechnol 2014, 98:4829-4837.
41. Liu G, Zhang L, Wei X, Zou G, Qin Y, Ma L, Li J, Zheng H, Wang S, Wang C: Genomic and secretomic analyses reveal unique features of the lignocellulolytic enzyme system of Penicillium decumbens. PLoS One 2013, 8:e55185.
42. Ilmen M, Saloheimo A, Onnela M-L, Penttilä ME: Regulation of cellulase gene expression in the filamentous fungus Trichoderma reesei. Appl Environ Microbiol 1997, 63:1298-1306.
43. Vandooren J, Geurts N, Martens E, Van den Steen PE, Opdenakker G: Zymography methods for visualizing hydrolytic enzymes. Nat Meth 2013, 10:211-220.
44. Kim KH, Brown KM, Harris PV, Langston JA, Cherry JR: A proteomics strategy to discover β-glucosidases from Aspergillus fumigatus with two-dimensional page in-gel activity assay and tandem mass spectrometry. J Proteome Res 2007, 6:4749-4757.
45. Hori C, Igarashi K, Katayama A, Samejima M: Effects of xylan and starch on secretome of the basidiomycete Phanerochaete chrysosporium grown on cellulose. FEMS Microbiol Lett 2011, 321:14-23.
46. Liao H, Sun S, Wang P, Bi W, Tan S, Wei Z, Mei X, Liu D, Raza W, Shen Q: A new acidophilic endo-β-1,4-xylanase from Penicillium oxalicum: cloning, purification, and insights into the influence of metal ions on xylanase activity. J Ind Microbiol Biotechnol 2014, 41:1071-1083.
47. Gómez-Mendoza DP, Junqueira M, Do Vale LHF, Domont GB, Filho EXF, Sousa MVD, Ricart CAO: Secretomic survey of Trichoderma harzianum grown on plant biomass substrates. J Proteome Res 2014, 13(4):1810-1822.
48. Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, Kubicek CP, Ferreira P, Ruiz-Duenas FJ, Martinez AT, Kersten P: Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci U S A 2009, 106:1954-1959.
49. Bailey MJ, Buchert J, Viikari L: Effect of pH on production of xylanase by Trichoderma reesei on xylan- and cellulose-based media. Appl Biochem Biotechnol 1993, 40:224-229.
50. Chávez R, Bull P, Eyzaguirre J: The xylanolytic enzyme system from the genus Penicillium. J Biotechnol 2006, 123:413-433.
51. Ghose T: Measurement of cellulase activities. Pure Appl Chem 1987, 59:257-268.
52. Bailey MJ, Biely P, Poutanen K: Interlaboratory testing of methods for assay of xylanase activity. J Biotechnol 1992, 23:257-270.
53. Miller GL: Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 1959, 31:426-428.
54. Parry NJ, Beever DE, Owen E, Vandenberghe I, Van Beeumen J, Bhat MK: Biochemical characterization and mechanism of action of a thermostable beta-glucosidase purified from Thermoascus aurantiacus. Biochem J 2001, 353:117-127.
55. Ahamed A, Vermette P: Culture-based strategies to enhance cellulase enzyme production from Trichoderma reesei RUT-C30 in bioreactor culture conditions. Biochem Eng J 2008, 40:399-407.
56. Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
57. Peterson R, Grinyer J, Nevalainen H: Extracellular hydrolase profiles of fungi isolated from koala faeces invite biotechnological interest. Mycol Prog 2011, 10:207-218.
58. The National Center for Biotechnology Information. [https://www.ncbi.nlm.nih.gov]
59. Lee C, Lee S, Shin SG, Hwang S: Real-time PCR determination of rRNA gene copy number: absolute and relative quantification assays with Escherichia coli. Appl Microbiol Biotechnol 2008, 78:371-376.
60. Petersen TN, Brunak S, von Heijne G, Nielsen H: SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Meth 2011, 8:785-786.
61. Compute pI/Mw tool. [http://web.expasy.org/compute-pi/]
62. Katz E, Fon M, Eigenheer RA, Phinney BS, Fass JN, Lin D, Sadka A, Blumwald E: A label-free differential quantitative mass spectrometry method for the characterization and identification of protein changes during citrus fruit development. Proteome Sci 2010, 8:68.