Comparative metabolism of cellulose, sophorose and glucose in Trichoderma reesei using high-throughput genomic and proteomic analyses

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• 作者：Lilian dos Santos Castro (1)
  Wellington Ramos Pedersoli (1)
  Amanda Cristina Campos Antoni锚to (1)
  Andrei Stecca Steindorff (2)
  Rafael Silva-Rocha (1)
  Nilce M Martinez-Rossi (3)
  Antonio Rossi (1)
  Neil Andrew Brown (4)
  Gustavo H Goldman (4)
  Vitor M Fa莽a (1)
  Gabriela F Persinoti (3)
  Roberto Nascimento Silva (1)
  
  1. Department of Biochemistry and Immunology ; Ribeir茫o Preto Medical School ; University of S茫o Paulo ; 14049-900 ; Ribeir茫o Preto ; SP ; Brazil
  2. Departamento de Biologia Celular ; Universidade de Bras铆lia ; Asa Norte ; 70910-900 ; Bras铆lia ; DF ; Brazil
  3. Department of Genetics ; Ribeir茫o Preto Medical School ; University of S茫o Paulo ; 14049-900 ; Ribeir茫o Preto ; SP ; Brazil
  4. Faculdade de Ci锚ncias Farmac锚uticas de Ribeir茫o Preto ; S茫o Paulo ; and Laborat贸rio Nacional de Ci锚ncia e Tecnologia do Bioetanol ; Universidade de S茫o Paulo ; Campinas ; Brazil
  
• 关键词：Trichoderma reesei ; RNA ; seq ; DIGE ; Cellulases ; Bioethanol
• 刊名：Biotechnology for Biofuels
• 出版年：2014
• 出版时间：December 2014
• 年：2014
• 卷：7
• 期：1
• 全文大小：1,203 KB
• 参考文献：1. Pessoa-Jr, A, Roberto, IC, Menossi, M, dos Santos, RR, Filho, SO, Penna, TC (2005) Perspectives on bioenergy and biotechnology in Brazil. Appl Biochem Biotechnol 121鈥?24: pp. 59-70 CrossRef
  2. Mosier, N, Wyman, C, Dale, B, Elander, R, Lee, YY, Holtzapple, M, Ladisch, M (2005) Features of promising technologies for pretreatment of lignocellulosic biomass. Bioresour Technol 96: pp. 673-686 CrossRef
  3. Ojeda, K, Kafarov, V (2009) Exergy analysis of enzymatic hydrolysis reactors for transformation of lignocellulosic biomass to bioethanol. Chem Eng J 154: pp. 390-395 CrossRef
  4. Soccol, CR, Vandenberghe, LPD, Medeiros, ABP, Karp, SG, Buckeridge, M, Ramos, LP, Pitarelo, AP, Ferreira-Leitao, V, Gottschalk, LMF, Ferrara, MA, Bon, EPD, de Moraes, LMP, Araujo, JD, Torres, FAG (2010) Bioethanol from lignocelluloses: Status and perspectives in Brazil. Bioresource Technology 101: pp. 4820-4825 CrossRef
  5. Kubicek, CP, Herrera-Estrella, A, Seidl-Seiboth, V, Martinez, DA, Druzhinina, IS, Thon, M, Zeilinger, S, Casas-Flores, S, Horwitz, BA, Mukherjee, PK, Mukherjee, M, Kredics, L, Alcaraz, LD, Aerts, A, Antal, Z, Atanasova, L, Cervantes-Badillo, MG, Challacombe, J, Chertkov, O, McCluskey, K, Coulpier, F, Deshpande, N, von Dohren, H, Ebbole, DJ, Esquivel-Naranjo, EU, Fekete, E, Flipphi, M, Glaser, F, Gomez-Rodriguez, EY, Gruber, S (2011) Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome biology 12: pp. R40 CrossRef
  6. Schuster, A, Schmoll, M (2010) Biology and biotechnology of Trichoderma. Appl Microbiol Biotechnol 87: pp. 787-799 CrossRef
  7. Martinez, D, Berka, RM, Henrissat, B, Saloheimo, M, Arvas, M, Baker, SE, Chapman, J, Chertkov, O, Coutinho, PM, Cullen, D, Danchin, EG, Grigoriev, IV, Harris, P, Jackson, M, Kubicek, CP, Han, CS, Ho, I, Larrondo, LF, de Leon, AL, Magnuson, JK, Merino, S, Misra, M, Nelson, B, Putnam, N, Robbertse, B, Salamov, AA, Schmoll, M, Terry, A, Thayer, N, Westerholm-Parvinen, A (2008) Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol 26: pp. 553-560 CrossRef
  8. Saloheimo, M, Nakari-Setala, T, Tenkanen, M, Penttila, M (1997) cDNA cloning of a Trichoderma reesei cellulase and demonstration of endoglucanase activity by expression in yeast. Eur J Biochem 249: pp. 584-591 CrossRef
  9. Hakkinen, M, Arvas, M, Oja, M, Aro, N, Penttila, M, Saloheimo, M, Pakula, TM (2012) Re-annotation of the CAZy genes of Trichoderma reesei and transcription in the presence of lignocellulosic substrates. Microb Cell Fact 11: pp. 134 CrossRef
  10. Verbeke, J, Coutinho, P, Mathis, H, Quenot, A, Record, E, Asther, M, Heiss-Blanquet, S (2009) Transcriptional profiling of cellulase and expansin-related genes in a hypercellulolytic Trichoderma reesei. Biotechnol Lett 31: pp. 1399-1405 30-5" target="_blank" title="It opens in new window">CrossRef
  11. Mandels, M, Parrish, FW, Reese, ET (1962) Sophorose as an inducer of cellulase in Trichoderma viride. J Bacteriol 83: pp. 400-408
  12. Kubicek, CP, Messner, R, Gruber, F, Mach, RL, Kubicek-Pranz, EM (1993) The Trichoderma cellulase regulatory puzzle: from the interior life of a secretory fungus. Enzyme Microb Technol 15: pp. 90-99 30-6" target="_blank" title="It opens in new window">CrossRef
  13. Seiboth, B, Hakola, S, Mach, RL, Suominen, PL, Kubicek, CP (1997) Role of four major cellulases in triggering of cellulase gene expression by cellulose in Trichoderma reesei. J Bacteriol 179: pp. 5318-5320
  14. Foreman, PK, Brown, D, Dankmeyer, L, Dean, R, Diener, S, Dunn-Coleman, NS, Goedegebuur, F, Houfek, TD, England, GJ, Kelley, AS, Meerman, HJ, Mitchell, T, Mitchinson, C, Olivares, HA, Teunissen, PJ, Yao, J, Ward, M (2003) Transcriptional regulation of biomass-degrading enzymes in the filamentous fungus Trichoderma reesei. The Journal of biological chemistry 278: pp. 31988-31997 304750200" target="_blank" title="It opens in new window">CrossRef
  15. Schmoll, M, Kubicek, CP (2003) Regulation of trichoderma cellulase formation: lessons in molecular biology from an industrial fungus.A review. Acta Microbiol Immunol Hung 50: pp. 125-145 CrossRef
  16. El-Gogary, S, Leite, A, Crivellaro, O, Eveleigh, DE, El-Dorry, H (1989) Mechanism by which cellulose triggers cellobiohydrolase I gene expression in Trichoderma reesei. Proc Natl Acad Sci USA 86: pp. 6138-6141 CrossRef
  17. Nogawa, M, Goto, M, Okada, H, Morikawa, Y (2001) L-Sorbose induces cellulase gene transcription in the cellulolytic fungus Trichoderma reesei. Curr Genet 38: pp. 329-334 CrossRef
  18. Chambergo, FS, Bonaccorsi, ED, Ferreira, AJ, Ramos, AS, Ferreira Junior, JR, Abrahao-Neto, J, Farah, JP, Farah, JP, El-Dorry, H (2002) Elucidation of the metabolic fate of glucose in the filamentous fungus Trichoderma reesei using expressed sequence tag (EST) analysis and cDNA microarrays. J Biol Chem 277: pp. 13983-13988 CrossRef
  19. Kubicek, CP (2013) Systems biological approaches towards understanding cellulase production by Trichoderma reesei. J Biotechnol 163: pp. 133-142 CrossRef
  20. Kubicek, CP, Mikus, M, Schuster, A, Schmoll, M, Seiboth, B (2009) Metabolic engineering strategies for the improvement of cellulase production by Hypocrea jecorina. Biotechnol Biofuels 2: pp. 19 CrossRef
  21. Castro, LD, Antonieto, AC, Pedersoli, WR, Silva-Rocha, R, Persinoti, GF, Silva, RN (2014) Expression pattern of cellulolytic and xylanolytic genes regulated by transcriptional factors XYR1 and CRE1 are affected by carbon source in Trichoderma reesei. Gene Expr Patterns 14: pp. 88-95 CrossRef
  22. Bischof, R, Fourtis, L, Limbeck, A, Gamauf, C, Seiboth, B, Kubicek, CP (2013) Comparative analysis of the Trichoderma reesei transcriptome during growth on the cellulase inducing substrates wheat straw and lactose. Biotechnol Biofuels 6: pp. 127 CrossRef
  23. Pao, SS, Paulsen, IT, Saier, MH (1998) Major facilitator superfamily. Microbiol Mol Biol R 62: pp. 1-34
  24. Boyce, KJ, Andrianopoulos, A (2013) Morphogenetic circuitry regulating growth and development in the dimorphic pathogen Penicillium marneffei. Eukaryot Cell 12: pp. 154-160 CrossRef
  25. Yao, J, Bajjalieh, SM (2009) SVOP is a nucleotide binding protein. PLoS One 4: pp. e5315 CrossRef
  26. Wieczorke, R, Krampe, S, Weierstall, T, Freidel, K, Hollenberg, CP, Boles, E (1999) Concurrent knock-out of at least 20 transporter genes is required to block uptake of hexoses in Saccharomyces cerevisiae. FEBS Lett 464: pp. 123-128 CrossRef
  27. Zhang, W, Kou, Y, Xu, J, Cao, Y, Zhao, G, Shao, J, Wang, H, Wang, Z, Bao, X, Chen, G, Liu, W (2013) Two major facilitator superfamily sugar transporters from trichoderma reesei and their roles in induction of cellulase biosynthesis. J Biol Chem 288: pp. 32861-32872 CrossRef
  28. Ries, L, Pullan, ST, Delmas, S, Malla, S, Blythe, MJ, Archer, DB (2013) Genome-wide transcriptional response of Trichoderma reesei to lignocellulose using RNA sequencing and comparison with Aspergillus niger. BMC Genomics 14: pp. 541 CrossRef
  29. Ivanova, C, Baath, JA, Seiboth, B, Kubicek, CP (2013) Systems analysis of lactose metabolism in Trichoderma reesei identifies a lactose permease that is essential for cellulase induction. PLoS One 8: pp. e62631 CrossRef
  30. Du, J, Li, S, Zhao, H (2010) Discovery and characterization of novel d-xylose-specific transporters from Neurospora crassa and Pichia stipitis. Mol Biosyst 6: pp. 2150-2156 CrossRef
  31. Sun, J, Tian, C, Diamond, S, Glass, NL (2012) Deciphering transcriptional regulatory mechanisms associated with hemicellulose degradation in Neurospora crassa. Eukaryot Cell 11: pp. 482-493 CrossRef
  32. Glass, NL, Palma-Guerrero, J, Jonkers, W, Leeder, A, Hall, C, Kowbel, D, Taylor, JW, Brem, R (2013) Revealing fungal communication modules by genomics, population genomics, and genome wide association studies in Neurospora crassa. Phytopathology 103: pp. 186-187
  33. Mukherjee, PK, Horwitz, BA, Herrera-Estrella, A, Schmoll, M, Kenerley, CM (2013) Trichoderma research in the genome era. Annu Rev Phytopathol 51: pp. 105-129 CrossRef
  34. Furukawa, T, Shida, Y, Kitagami, N, Mori, K, Kato, M, Kobayashi, T, Okada, H, Ogasawara, W, Morikawa, Y (2009) Identification of specific binding sites for XYR1, a transcriptional activator of cellulolytic and xylanolytic genes in Trichoderma reesei. Fungal Genet Biol 46: pp. 564-574 CrossRef
  35. Strauss, J, Mach, RL, Zeilinger, S, Hartler, G, Stoffler, G, Wolschek, M, Kubicek, CP (1995) Cre1, the carbon catabolite repressor protein from Trichoderma reesei. FEBS Lett 376: pp. 103-107 CrossRef
  36. Portnoy, T, Margeot, A, Seidl-Seiboth, V, Le Crom, S, Ben Chaabane, F, Linke, R, Seiboth, B, Kubicek, CP (2011) Differential regulation of the cellulase transcription factors XYR1, ACE2, and ACE1 in Trichoderma reesei strains producing high and low levels of cellulase. Eukaryot Cell 10: pp. 262-271 CrossRef
  37. Nitta, M, Furukawa, T, Shida, Y, Mori, K, Kuhara, S, Morikawa, Y, Ogasawara, W (2012) A new Zn(II)(2)Cys(6)-type transcription factor BglR regulates beta-glucosidase expression in Trichoderma reesei. Fungal Genet Biol 49: pp. 388-397 CrossRef
  38. Martinez-Antonio, A, Collado-Vides, J (2003) Identifying global regulators in transcriptional regulatory networks in bacteria. Curr Opin Microbiol 6: pp. 482-489 CrossRef
  39. Seiboth, B, Karimi, RA, Phatale, PA, Linke, R, Hartl, L, Sauer, DG, Smith, KM, Baker, SE, Freitag, M, Kubicek, CP (2012) The putative protein methyltransferase LAE1 controls cellulase gene expression in Trichoderma reesei. Mol Microbiol 84: pp. 1150-1164 CrossRef
  40. Karimi-Aghcheh, R, Bok, JW, Phatale, PA, Smith, KM, Baker, SE, Lichius, A, Omann, M, Zeilinger, S, Seiboth, B, Rhee, C, Keller, NP, Freitag, M, Kubicek, CP (2013) Functional analyses of Trichoderma reesei LAE1 reveal conserved and contrasting roles of this regulator. G3 (Bethesda) 3: pp. 369-378 CrossRef
  41. Rossi, A, Cruz, AH, Santos, RS, Silva, PM, Silva, EM, Mendes, NS, Martinez-Rossi, NM (2013) Ambient pH sensing in filamentous fungi: pitfalls in elucidating regulatory hierarchical signaling networks. IUBMB Life 65: pp. 930-935 CrossRef
  42. Li, C, Yang, Z, He Can Zhang, R, Zhang, D, Chen, S, MA, L (2013) Effect of pH on cellulase production and morphology of Trichoderma reesei and the application in cellulosic material hydrolysis. J Biotechnol 168: pp. 470-477 CrossRef
  43. Mach, RL, Zeilinger, S (2003) Regulation of gene expression in industrial fungi: Trichoderma. Appl Microbiol Biotechnol 60: pp. 515-522 CrossRef
  44. Gasch, AP, Spellman, PT, Kao, CM, Carmel-Harel, O, Eisen, MB, Storz, G, Botstein, D, Brown, PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: pp. 4241-4257 CrossRef
  45. Herpoel-Gimbert, I, Margeot, A, Dolla, A, Jan, G, Molle, D, Lignon, S, Mathis, H, Sigoillot, JC, Monot, F, Asther, M (2008) Comparative secretome analyses of two Trichoderma reesei RUT-C30 and CL847 hypersecretory strains. Biotechnol Biofuels 1: pp. 18 CrossRef
  46. Jun, H, Kieselbach, T, Jonsson, LJ (2011) Enzyme production by filamentous fungi: analysis of the secretome of Trichoderma reesei grown on unconventional carbon source. Microb Cell Fact 10: pp. 68 CrossRef
  47. Adav, SS, Chao, LT, Sze, SK (2012) Quantitative secretomic analysis of Trichoderma reesei strains reveals enzymatic composition for lignocellulosic biomass degradation. Mol Cell Proteomics 11: pp. M111 012419 CrossRef
  48. Tisch, D, Kubicek, CP, Schmoll, M (2011) New insights into the mechanism of light modulated signaling by heterotrimeric G-proteins: ENVOY acts on gna1 and gna3 and adjusts cAMP levels in Trichoderma reesei (Hypocrea jecorina). Fungal Genet Biol 48: pp. 631-640 CrossRef
  49. Druzhinina, IS, Shelest, E, Kubicek, CP (2012) Novel traits of Trichoderma predicted through the analysis of its secretome. FEMS Microbiol Lett 337: pp. 1-9 CrossRef
  50. Zhou, QX, Xu, JT, Kou, YB, Lv, XX, Zhang, X, Zhao, GL, Zhang, WX, Chen, GJ, Liu, WF (2012) Differential involvement of beta-glucosidases from hypocrea jecorina in rapid induction of cellulase genes by cellulose and cellobiose. Eukaryot Cell 11: pp. 1371-1381 CrossRef
  51. Znameroski, EA, Coradetti, ST, Roche, CM, Tsai, JC, Iavarone, AT, Cate, JHD, Glass, NL (2012) Induction of lignocellulose-degrading enzymes in Neurospora crassa by cellodextrins. Proc Natl Acad Sci USA 109: pp. 6012-6017 CrossRef
  52. Gielkens, MM, Dekkers, E, Visser, J, de Graaff, LH (1999) Two cellobiohydrolase-encoding genes from Aspergillus niger require D-xylose and the xylanolytic transcriptional activator XlnR for their expression. Appl Environ Microbiol 65: pp. 4340-4345
  53. Schmoll, M, Schuster, A, Silva Rdo, N, Kubicek, CP (2009) The G-alpha protein GNA3 of Hypocrea jecorina (Anamorph Trichoderma reesei) regulates cellulase gene expression in the presence of light. Eukaryot Cell 8: pp. 410-420 CrossRef
  54. Li, H, Durbin, R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: pp. 1754-1760 CrossRef
  55. Li, H, Handsaker, B, Wysoker, A, Fennell, T, Ruan, J, Homer, N, Marth, G, Abecasis, G, Durbin, R, Proc, GPD (2009) The sequence alignment/Map format and SAMtools. Bioinformatics 25: pp. 2078-2079 CrossRef
  56. Thorvaldsdottir, H, Robinson, JT, Mesirov, JP (2013) Integrative genomics viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14: pp. 178-192 CrossRef
  57. Atanasova, L, Jaklitsch, WM, Komon-Zelazowska, M, Kubicek, CP, Druzhinina, IS (2010) Clonal species Trichoderma parareesei sp. nov. likely resembles the ancestor of the cellulase producer Hypocrea jecorina/T. reesei. Appl Environ Microbiol 76: pp. 7259-7267 CrossRef
  58. Anders, S, Huber, W (2010) Differential expression analysis for sequence count data. Genome Biol 11: pp. R106 CrossRef
  59. Vencio, RZ, Koide, T, Gomes, SL, Pereira, CA (2006) BayGO: bayesian analysis of ontology term enrichment in microarray data. BMC Bioinformatics 7: pp. 86 CrossRef
  60. Shannon, P, Markiel, A, Ozier, O, Baliga, NS, Wang, JT, Ramage, D, Amin, N, Schwikowski, B, Ideker, T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: pp. 2498-2504 303" target="_blank" title="It opens in new window">CrossRef
  61. Steiger, MG, Mach, RL, Mach-Aigner, AR (2010) An accurate normalization strategy for RT-qPCR in Hypocrea jecorina (Trichoderma reesei). J Biotechnol 145: pp. 30-37 CrossRef
  62. Livak, KJ, Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25: pp. 402-408 CrossRef
  63. MacLean, B, Eng, JK, Beavis, RC, McIntosh, M (2006) General framework for developing and evaluating database scoring algorithms using the TANDEM search engine. Bioinformatics 22: pp. 2830-2832 CrossRef
  64. Keller, A, Nesvizhskii, AI, Kolker, E, Aebersold, R (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74: pp. 5383-5392 CrossRef
  65. Nesvizhskii, AI, Keller, A, Kolker, E, Aebersold, R (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75: pp. 4646-4658 CrossRef
  
• 刊物类别：Chemistry and Materials Science
• 刊物主题：Biotechnology
  Plant Breeding/Biotechnology
  Renewable and Green Energy
  Environmental Engineering/Biotechnology
  
• 出版者：BioMed Central
• ISSN：1754-6834

文摘

Background The filamentous fungus Trichoderma reesei is a major producer of lignocellulolytic enzymes utilized by bioethanol industries. However, to achieve low cost second generation bioethanol production on an industrial scale an efficient mix of hydrolytic enzymes is required for the deconstruction of plant biomass. In this study, we investigated the molecular basis for lignocellulose-degrading enzyme production T. reesei during growth in cellulose, sophorose, and glucose. Results We examined and compared the transcriptome and differential secretome (2D-DIGE) of T. reesei grown in cellulose, sophorose, or glucose as the sole carbon sources. By applying a stringent cut-off threshold 2,060 genes were identified as being differentially expressed in at least one of the respective carbon source comparisons. Hierarchical clustering of the differentially expressed genes identified three possible regulons, representing 123 genes controlled by cellulose, 154 genes controlled by sophorose and 402 genes controlled by glucose. Gene regulatory network analyses of the 692 genes differentially expressed between cellulose and sophorose, identified only 75 and 107 genes as being specific to growth in sophorose and cellulose, respectively. 2D-DIGE analyses identified 30 proteins exclusive to sophorose and 37 exclusive to cellulose. A correlation of 70.17% was obtained between transcription and secreted protein profiles. Conclusions Our data revealed new players in cellulose degradation such as accessory proteins with non-catalytic functions secreted in different carbon sources, transporters, transcription factors, and CAZymes, that specifically respond in response to either cellulose or sophorose.