Methodologies and perspectives of proteomics applied to filamentous fungi: From sample preparation to secretome analysis

International Journal of Molecular Sciences

Volumn 16, Issue 3, 2015, Pages 5803-5829

  Bianco, Linda ^a   Perrotta, Gaetano ^a  

^a Trisaia Research Center   (Italy)

Author keywords

Filamentous fungi; Fungal degradation; Fungal proteomics; Lignocellulose bioconversion; Secretome

Indexed keywords

CELL MEMBRANE PROTEIN; LACCASE; LIGNOCELLULOSE; PEROXIDASE; PROTEIN; TRICHLOROACETIC ACID; ENZYME; LIGNIN;

ANALYTIC METHOD; ASPERGILLUS NIGER; BIOMASS CONVERSION; BIOMICS; BIOREMEDIATION; CELL DISRUPTION; DEGLYCOSYLATION; FUNGUS; GEL BASED SEPARATION TECHNIQUES; GEL ELECTROPHORESIS; HYPOCREA LIXII; MASS SPECTROMETRY; MULTIDIMENSIONAL PROTEIN IDENTIFICATION TECHNOLOGY; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; NEUROSPORA CRASSA; NONHUMAN; PENICILLIUM CHRYSOGENUM; PENICILLIUM PURPUROGENUM; PHANEROCHAETE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN ANALYSIS; PROTEIN DENATURATION; PROTEOMICS; REVIEW; SECRETOMICS; SEPARATION TECHNIQUE; TALAROMYCES FUNICULOSUS; TERMITOMYCES; USTILAGO MAYDIS; METABOLISM;

FUNGI;

ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYMES; FUNGI; LIGNIN; PROTEOMICS;

EID: 84925864887     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms16035803     Document Type: Review

References (139)

1. Camarero, S.; Jesús, M.M.; Martínez, A.T. Understanding lignin biodegradation for the improved utilization of plant biomass in modern biorefineries. Biofuels Bioprod. Biorefin. 2014, 8, 615–625.
2. Sanchez, C. Lignocellulosic residues: Biodegradation and bioconversion by fungi. Biotechnol. Adv. 2009, 27, 185–197.
3. Kubicek, C.P. Fungi and Lignocellulosic Biomass; John Wiley & Sons: New York, NY, USA, 2012; pp. 29–44.
4. Kubicek, C.P.; Mikus, M.; Schuster, A.; Schmoll, M.; Seiboth, B. Metabolic engineering strategies for the improvement of cellulase production by Hypocrea jecorina. Biotechnol. Biofuels 2009, 2, 19–33.
5. Dashtban, M.; Schraf, T.H.; Syed, T.A.; Qin, W. Fungal biodegradation and enzymatic modification of lignin. Int. J. Biochem. Mol. Biol. 2010, 1, 36–50.
6. Guerra, A.; Mendonca, R.; Ferraz, A.; Lu, F.; Ralph, J. Structural characterization of lignin during Pinus taeda wood treatment with Ceriporiopsis subvermispora. Appl. Environ. Microbiol. 2004, 70, 4073–4078.
7. Arora, D.S.; Sharma, R.K. Enhancement in in vitro digestibility of wheat straw obtained from different geographical regions during solid state fermentation by white rot fungi. BioResource 2009, 4, 909–920.
8. Fackler, K.; Gradinger, C.; Hinterstoisser, B.; Messner, K.; Schwanninger, M. Lignin degradation by white rot fungi on spruce wood shavings during short-time solid-state fermentations monitored by near infrared spectroscopy. Enzym. Microb. Technol. 2006, 39, 1476–1483.
9. Hilden, K.; Hakala, T.K.; Maijala, P.; Lundell, T.K.; Hatakka, A. Novel thermotolerant laccases produced by the white-rot fungus Physisporinus rivulosus. Appl. Microbiol. Biotechnol. 2007, 77, 301–309.
10. Tanaka, H.; Itakura, S.; Enoki, A. Hydroxyl radical generation by an extracellular low-molecular-weight substance and phenol oxidase activity during wood degradation by the white-rot basidiomycete Trametes versicolor. J. Biotechnol. 1999, 75, 57–70.
11. Xu, C.; Ma, F.; Zhang, X. Lignocellulose degradation and enzyme production by Irpex lacteus CD2 during solid-state fermentation of corn stover. J. Biosci. Bioeng. 2009, 108, 372–375.
12. Anderson, W.F.; Akin, D.E. Structural and chemical properties of grass lignocelluloses related to conversion for biofuels. J. Ind. Microbiol. Biotechnol. 2008, 35, 355–366.
13. Mai, C.; Kues, U.; Militz, H. Biotechnology in the wood industry. Appl. Microbiol. Biotechnol. 2004, 63, 477–494.
14. Abdel-Hamid, A.M.; Solbiati, J.O.; Cann, I.K. Insights into lignin degradation and its potential industrial applications. Adv. Appl. Microbiol. 2013, 82, 1–28.
15. Scherba, V.V.; Babitskaya, V.G. Polysaccharides of xylotrophic basidiomycetes. Appl. Biochem. Microbiol. 2008, 44, 78–83.
16. Rashid, M.H.; Siddiqui, K.S. The stability of extracellular beta-glucosidase from Aspergillus niger is significantly enhanced by non-covalently attached polysaccharides. Folia Microbiol. 1996, 41, 341–346.
17. Asgher, M.; Bhatti, H.N.; Ashraf, M.; Legge, R.L. Recent developments in biodegradation of industrial pollutants by white rot fungi and their enzyme system. Biodegradation 2008, 19, 771–783.
18. Pointing, S.B. Feasibility of bioremediation by white rot fungi. Appl. Microbiol. Biotechnol. 2001, 57, 20–33.
19. Maciel, M.J.; Silva, A.C.; Ribeiro, H.C.T. Industrial and biotechnological applications of ligninolytic enzymes of the basidiomycota: A review. Electron. J. Biotechnol. 2010, 13, 14–15.
20. Gygi, S.P.; Rist, B.; Gerber, S.A.; Turecek, F; Gelb, M.H.; Aebersold, R. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol. 1999, 17, 994–999.
21. González-Fernandez, R.; Jorrin-Novo, J.V. Proteomic protocols for the study of filamentous fungi. In Laboratory Protocols in Fungal Biology: Current Methods in Fungal Biology; Gupta, V.K., Ed.; Springer: New York, NY, USA, 2013; pp. 299–308.
22. Bowman, S.M.; Free, S.J. The structure and synthesis of the fungal cell wall. Bioessays 2006, 28, 799–808.
23. Barreiro, C.; García-Estrada, C.; Martín, J.F. Proteomics methodology applied to the analysis of filamentous fungi-new trends for an impressive diverse group of organisms. In Tandem Mass Spectrometry—Applications and Principles; Prasain, J., Ed.; InTech: Rijeka, Croatia, 2012; pp. 127–160.
24. Grinyer, J.; Kautto, L.; Traini, M.; Willows, R.D.; Te’o, J.; Bergquist, P. Proteome mapping of the Trichoderma reesei 20S proteasome. Curr. Genet. 2007, 51, 79–88.
25. Grinyer, J.; McKay, M.; Nevalainen, H.; Herbert, B.R. Fungal proteomics: Initial mapping of biological control strain Trichoderma harzianum. Curr. Genet. 2004, 45, 163–169.
26. Lim, D.; Hains, P.; Walsh, B.; Bergquist, P.; Nevalainen, H. Proteins associated with the cell envelope of Trichoderma reesei: A proteomic approach. Proteomics 2001, 1, 899–909.
27. Nandakumar, M.P.; Marten, M.R. Comparison of lysis methods and preparation protocols for one- and two-dimensional electrophoresis of Aspergillus oryzae intracellular proteins. Electrophoresis 2002, 23, 2216–2222.
28. Grinyer, J.; Hunt, S.; McKay, M.; Herbert, B.R.; Nevalainen, H. Proteomic response of the biological control fungus Trichoderma atroviride to growth on the cell walls of Rhizoctonia solani. Curr. Genet. 2005, 47, 381–388.
29. Taylor, R.D; Saparno, A.; Blackwell, B.; Anoop, V.; Gleddie, S.; Tinker, N.A. Proteomic analyses of Fusarium graminearum grown under mycotoxininducing conditions. Proteomics 2008, 8, 2256–2265.
30. Fernandez-Acero, F.J.; Colby, T.; Harzen, A.; Cantoral, J.M.; Schmidt, J. Proteomic analysis of the phytopathogenic fungus Botrytis cinerea during cellulose degradation. Proteomics 2009, 9, 2892–2902.
31. Kim, S.T.; Yu, S.; Kim, S.G.; Kim, H.J.; Kang, S.Y.; Hwang, D.H.; Jang, Y.S.; Kang, K.Y. Proteome analysis of rice blast fungus (Magnaporthe grisea) proteome during appressorium formation. Proteomics 2004, 4, 3579–3587.
32. Bhadauria, V.; Zhao, W.S.; Wang, L.X.; Zhang, Y.; Liu, J.H.; Yang, J.; Kong, L.A.; Peng, Y.L. Advances in fungal proteomics. Microbiol. Res. 2007, 162, 193–200.
33. Bhadauria, V.; Peng, Y.L. Optimization of a protein extraction technique for fungal proteomics Indian J. Microbiol. 2010, 50, 127–131.
34. Shimizu, M.; Wariishi, H. Development of a sample preparation method for fungal proteomics FEMS Microbiol. Lett. 2005, 247, 17–22.
35. Vödisch, M.; Scherlach, K.; Winkler, R.; Hertweck, C.; Braun, H.P.; Roth, M.; Haas, H.; Werner, E.R.; Brakhage, A.A.; Kniemeyer, O. Analysis of the Aspergillus fumigatus proteome reveals metabolic changes and the activation of the pseurotin a biosynthesis gene cluster in response to hypoxia. J. Proteome Res. 2011, 10, 2508–2524.
36. Nandakumar, M.P.; Shen, J.; Raman, B.; Marten, M.R. Solubilization of trichloroacetic acid (TCA) precipitated microbial proteins via NaOH for one and two dimensional electrophoresis. J. Proteome Res. 2003, 2, 89–93.
37. Rabilloud, T. Use of thiourea to increase the solubility of membrane proteins in two-dimensional electrophoresis. Electrophoresis 1998, 19, 758–760.
38. Everberg, H.; Gustavasson, N.; Tjerned, F. Enrichment of membrane proteins by partitioning in detergent/polymer aqueous two-phase systems. Methods Mol. Biol. 2008, 424, 403–412.
39. Rabilloud, T.; Adessi, C.; Giraudel, A.; Lunardi, J. Improvement of the solubilization of proteins in twodimensional electrophoresis with immobilized pH gradients. Electrophoresis 1997, 18, 307–316.
40. Herbert, B.R.; Grinyer, J.; McCarthy, J.T.; Isaacs, M.; Harry, E.J.; Nevalainen, H.; Traini, M.D.; Hunt, S.; Schulz, B.; Laver, M, et al. Improved 2-DE of microorganisms after acidic extraction. Electrophoresis 2006, 27, 1630–1640.
41. Bennett, J.W. The molds of Katrina. Update. N. Y. Acad. Sci. 2006, 126, 6–9.
42. Kim, Y.; Nandakumar, M.P.; Marten, M.R. Proteomics of filamentous fungi. Trends Biotechnol. 2007, 25, 395–400.
43. Fragner, D.; Zomorrodi, M.; Kues, U.; Majcherczyk, A. Optimized protocol for the 2-DE of extracellular proteins from higher basidiomycetes inhabiting lignocellulose. Electrophoresis 2009, 30, 2431–2441.
44. Kao, S.H.; Wong, H.K.; Chiang, C.Y.; Chen, H.M. Evaluating the compatibility of three colorimetric protein assays for two-dimensional electrophoresis experiments. Proteomics 2008, 8, 2178–2184.
45. Medina, M.L.; Francisco, WA. Isolation and enrichment of secreted proteins from filamentous fungi. In 2D PAGE: Sample Preparation and Fractionation; Humana Press: New York, NY, USA, 2008; pp. 275–285.
46. Adav, S.S.; Li, A.A.; Manavalan, A.; Punt, P.; Sze, S.K. Quantitative iTRAQ secretome analysis of aspergillus niger reveals novel hydrolytic enzymes. J. Proteome Res. 2010, 9, 3932–3940.
47. Adav, S.S.; Chao, L.T.; Sze, S.K. Quantitative secretomic analysis of Trichoderma reesei strains reveals enzymatic composition for lignocellulosic biomass degradation. Mol. Cell Proteomics 2012, 11, doi:10.1074/mcp.M111.012419.
48. Salvachúa, D.; Martínez, A.T.; Tien, M.; López-Lucendo, M.F.; García, F.: de los Ríos V.; Martínez, M.J.; Prieto, A. Differential proteomic analysis of the secretome of Irpex lacteus and other white-rot fungi during wheat straw pretreatment. Biotechnol. Biofuels 2013, 6, 115–129.
49. Gonzalez-Vogel, A.; Eyzaguirre, J.; Oleas, G.; Callegari, E.; Navarrete, M. Proteomic analysis in non-denaturing condition of the secretome reveals the presence of multienzyme complexes in Penicillium purpurogenum. Appl. Microbiol. Biotechnol. 2011, 89, 145–155.
50. Silva, A.J.D.; Gómez-Mendoza, D.P.; Junqueira, M.; Domont, G.B.; Ferreira Filho, X.; de Sousa, M.V.; Ricart, C.A.O. Blue native-PAGE analysis of Trichoderma harzianum secretome reveals cellulases and hemicellulases working as multienzymatic complexes. Proteomics 2012, 12, 2729–2738.
51. De Oliveira, J.M.P.F.; de Graaff, L.H. Proteomics of industrial fungi: Trends and insights for biotechnology. Appl. Microbiol. Biotechnol. 2011, 89, 225–237.
52. Hernandez-Macedo, M.L.; Ferraz, A.; Rodriguez, J.; Ottoboni, L.M.; de Mello, M.P. Iron-regulated proteins in Phanerochaete chrysosporium and Lentinula edodes: Differential analysis by sodium dodecyl sulfate polyacrylamide gel electrophoresis and two-dimensional polyacrylamide gel electrophoresis profiles. Electrophoresis 2002, 23, 655–661.
53. Schmitt, S.; Prokisch, H.; Schlunck, T.; Camp, D.G.; Ahting, U.; Waizenegger, T.; Scharfe, C.; Meitinger, T.; Imhof, A.; Neupert, W, et al. Proteome analysis of mitochondrial outer membrane from Neurospora crassa. Proteomics 2006, 6, 72–80.
54. Gao, B.B.; Stuart, L.; Feener, E.P. Label-free quantitative analysis of one-dimensional PAGE LC/MS/MS proteome: Application on angiotensin II-stimulated smooth muscle cells secretome. Mol. Cell Proteomics 2008, 7, 2399–2409.
55. Piersma, S.R.; Warmoes, M.O.; de Witm M.; de Reus, I., Knol, J.C.; Jiménez, C.R. Whole gel processing procedure for GeLC-MS/MS based proteomics. Proteome Sci. 2013, 11, 17–25.
56. Guais, O.; Borderies, G.; Pichereaux, C.; Maestracci, M.; Neugnot, V.; Rossignol, M.; François, J.M. Proteomics analysis of “Rovabiot Excel”, a secreted protein cocktail from the filamentous fungus Penicillium funiculosum grown under industrial process fermentation. J. Ind. Microbiol. Biotechnol. 2008, 35, 1659–1668.
57. Braaksma, M.; Martens-Uzunova, E.S.; Punt, P.J.; Schaap, P.J. An inventory of the Aspergillus niger secretome by combining in silico predictions with shotgun proteomics data. BMC Genomics 2010, 11, 584–595.
58. De Oliveira, J.M.P.F.; van Passel, M.W.; Schaap, P.J.; de Graaff, L.H. Shotgun proteomics of Aspergillus niger microsomes upon D-xylose induction. Appl. Environ. Microbiol. 2010, 76, 4421–4429.
59. Couturier, M.; Navarro, D.; Olivé, C.; Chevret, D.; Haon, M.; Favel, A.; Lesage-Meessen, L.; Henrissat, B.; Coutinho, P.M.; Berrin, J.G. Post-genomic analyses of fungal lignocellulosic biomass degradation reveal the unexpected potential of the plant pathogen Ustilago maydis. BMC Genomics 2012, 13, 57–71.
60. Wittig, I.; Braun, H.P.; Schägger, H. Blue native PAGE. Nat. Protoc. 2006, 1, 418–428.
61. Jami, M.S.; Barreiro, C.; García-Estrada, C.; Martín, J.F. Proteome analysis of the penicillin producer Penicillium chrysogenum: Characterization of protein changes during the industrial strain improvement. Mol. Cell Proteomics 2010, 9, 1182–1198.
62. Jami, M.S.; García-Estrada, C.; Barreiro, C.; Cuadrado, A.A; Salehi-Najafabadi, Z.; Martín, J.F. The Penicillium chrysogenum extracellular proteome. Conversionfrom a food-rotting strain to a versatile cell factory for white biotechnology. Mol. Cell Proteomics 2010, 9, 2729–2744.
63. Ozcan, S.; Yildirim, V.; Kaya, L.; Albrecht, D.; Becher, D.; Hecker, M.; Ozcengiz, G. Phanerochaete chrysosporium soluble proteome as a prelude for the analysis of heavy metal stress response. Proteomics 2007, 7, 1249–1260.
64. Ravalason, H.; Jan, G.; Mollé, D.; Pasco, M.; Coutinho, P.M.; Lapierre, C.; Pollet, B.; Bertaud, F.; Petit-Conil, M.; Grisel, S, et al. Secretome analysis of Phanerochaete chrysosporium strain CIRM-BRFM41 grown on softwood. Appl. Microbiol. Biotechnol. 2008, 80, 719–33.
65. Lu, X.; Sun, J.; Nimtz, M.; Wissing, J.; Zeng, A.P.; Rinas, U. The intra- and extracellular proteome of Aspergillus niger growing on defined medium with xylose or maltose as carbon substrate. Microb. Cell Fact. 2010, 20, 23–36.
66. Shimizu, M.; Yuda, N.; Nakamura, T.; Tanaka, H.; Wariishi, H. Metabolic regulation at the tricarboxylic acid and glyoxylate cycles of the lignin-degrading basidiomycete Phanerochaete chrysosporium against exogenous addition of vanillin. Proteomics 2005, 5, 3919–3931.
67. Marouga, R.; David, S.; Hawkins, E. The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal. Bioanal. Chem. 2005, 382, 669–678.
68. Dos Santos Castro, L.; Pedersoli, W.R.; Antoniêto, A.C.C.; Steindorff, A.S.; Silva-Rocha, R.; Martinez-Rossi, N.M.; Brown, N.A.; Goldman, G.H.; Faça, V.M.; Persinoti, G.F, et al. Comparative metabolism of cellulose, sophorose and glucose in Trichoderma reesei using high-throughput genomic and proteomic analyses. Biotechnol. Biofuels 2014, 7, 1–18.
69. Rahmad, N.; Al-Obaidi, J.R.; Rashid, N.M.N.; Zean, N B.; Yusoff, M.H.Y.M.; Shaharuddin, N.S.; Mohd, J.N.A.; Saleh, N.M. Comparative proteomic analysis of different developmental stages of the edible mushroom Termitomyces heimii. Biol. Res. 2014, 47, 30–38.
70. Yates, J.R., III; Ruse, C.I.; Nakorchevsky, A. Proteomics by mass spectrometry: Approaches, advances, and applications. Annu. Rev. Biomed. Eng. 2009, 11, 49–79.
71. Walther, T.C.; Mann, M. Mass spectrometry-based proteomics in cell biology. J. Cell Biol. 2010, 190, 491–500.
72. Bantscheff, M.; Lemeer, S.; Savitski, M.M.; Kuster, B. Quantitative mass spectrometry in proteomics: Critical review update from 2007 to the present. Anal. Bioanal. Chem. 2012, 404, 939–965.
73. Washburn, M.P.; Wolters, D.; Yates, J.R., III. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 2001, 19, 242–247.
74. Cooper, B.; Neelam, A.; Campbell, K.B.; Lee, J.; Liu, G.; Garrett, W.M.; Scheffler, B.; Tucker, M.L. Protein accumulation in the germinating Uromyces appendiculatus uredospore. Mol. Plant Microbe Interact. 2007, 20, 857–866.
75. Tian, C.; Beeson, W.T.; Iavarone, A.T.; Sun, J.; Marletta, M.A.; Cate, J.H.; Glass, N.L. Systems analysis of plant cell wall degradation by the model filamentous fungus Neurospora crassa. Proc. Natl. Acad. Sci. USA 2009, 106, 22157–22162.
76. Scully, E.D.; Hoover, K.; Carlson, J.; Tien, M.; Geib, S.M. Proteomic analysis of Fusarium solani isolated from the asian longhorned beetle, Anoplophora glabripennis. PLoS One 2012, 7, e32990.
77. De Godoy, L.M.; Olsen, J.V.; Cox, J.; Nielsen, M.L.; Hubner, N.C.; Fröhlich, F.; Walther, T.C.; Mann, M. Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 2008, 455, 1251–1254.
78. Nagaraj, N.; Kulak, N.A.; Cox, J.; Neuhauser, N.; Mayr, K.; Hoerning, O.; Vorm, O.; Mann, M. System-wide perturbation analysis with nearly complete coverage of the yeast proteome by single-shot ultra HPLC runs on a bench top Orbitrap. Mol. Cell Proteomics 2012, 11, doi:10.1074/mcp.M111.013722.
79. Picotti, P.; Clément-Ziza, M.; Lam, H.; Campbell, D.S.; Schmidt, A.; Deutsch, E.W.; Röst, H.; Sun, Z.; Rinner, O.; Reiter, L.; et al. A complete mass-spectrometric map of the yeast proteome applied to quantitative trait analysis. Nature 2013, 494, 266–270.
80. Webb, K.J.; Xu, T.; Park, S.K.; Yates, J.R., III. Modified MuDPIT separation identified 4488 proteins in a system-wide analysis of quiescence in yeast. J. Proteome Res. 2013, 12, 2177–2184.
81. Picotti, P.; Bodenmiller, B.; Mueller, L.N.; Domon, B.; Aebersold, R. Full dynamic range proteome analysis of S. cerevisiae by targeted proteomics. Cell 2009, 138, 795–806.
82. Thakur, S.S.; Geiger, T.; Chatterjee, B.; Bandilla, P.; Fröhlich, F.; Cox, J.; Mann, M. Deep and highly sensitive proteome coverage by LC-MS/MS without prefractionation. Mol. Cell Proteomics 2011, doi:10.1074/mcp.M110.003699.
83. Kelstrup, C.D.; Jersie-Christensen, R.R.; Batth, T.S.; Arrey, T.N.; Kuehn, A.; Kellmann, M.; Olsen, J.V. Rapid and deep proteomes by faster sequencing on a benchtop quadrupole ultra-high-field orbitrap mass spectrometer. J. Proteome Res. 2014, 13, 6187–6195.
84. Scheltema, R.A.; Hauschild, J.P.; Lange, O.; Hornburg, D.; Denisov, E.; Damoc, E.; Kuehn, A.; Makarov, A.; Mann, M. The Q exactive HF, a benchtop mass spectrometer with a pre-filter, high-performance quadrupole and an ultra-high-field orbitrap analyzer. Mol. Cell Proteomics 2014, 13, 3698–3708.
85. Stewart, I.I.; Thomson, T.; Figeys, D. 18O labeling: A tool for proteomics. Rapid Commun. Mass Spectrom. 2001, 15, 2456–2465.
86. Ross, P.L.; Huang, Y.N.; Marchese, J.N.; Williamson, B.; Parker, K.; Hattan, S.; Khainovski, N.S.; Dey, S.; Daniels, S.; Purkayastha, S, et al. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell Proteomics 2004, 3, 1154–1169.
87. Thompson, A.; Schäfer, J.; Kuhn, K.; Kienle, S.; Schwarz, J.; Schmidt, G.; Neumann, T.; Johnstone, R.; Mohammed, A.K.; Hamon, C. Tandem mass tags: A novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal. Chem. 2003, 75, 1895–1904.
88. Cagas, S.E.; Jain, M.R.; Li, H.; Perlin, D.S. The proteomic signature of Aspergillus fumigatus during early development. Mol. Cell Proteomics 2011, 10, doi:10.1074/mcp.M111.010108.
89. Cagas, S.E.; Jain, M.R.; Li, H.; Perlin, D.S. Profiling the Aspergillus fumigatus proteome in response to caspofungin. Antimicrob. Agents Chemother. 2011, 55, 146–154.
90. 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, 149–165.
91. Manavalan, A.; Adav, S.S.; Sze, S.K. TRAQ-based quantitative secretome analysis of Phanerochaete chrysosporium. J. Proteomics 2011, 75, 642–654.
92. Adav, S.S.; Ravindran, A.; Sze, S.K. Quantitative proteomic analysis of lignocellulolytic enzymes by Phanerochaete chrysosporium on different lignocellulosic biomass. J. Proteomics 2012, 75, 1493–1504.
93. Adav, S.S.; Chao, L.T.; Sze, S.K. Protein abundance in multiplexed samples (PAMUS) for quantitation of Trichoderma reesei secretome. J. Proteomics 2013, 83, 180–196.
94. Zhang, J.; Wang, Y.; Li, S. Deuterium isobaric amine-reactive tags for quantitative proteomics. Anal. Chem. 2010, 82, 7588–7595.
95. Ramsubramaniam, N.; Tao, F.; Li, S.; Marten, M.R. Novel and cost-effective 6-plex isobaric tagging reagent, DiART, is effective for identification and relative quantification of complex protein mixtures using PQD fragmentation. J. Mass Spectrom. 2013, 48, 1032–1041.
96. Mann, M. Functional and quantitative proteomics using SILAC. Nat. Rev. Mol. Cell Biol. 2006, 7, 952–958.
97. Oda, Y.; Huang, K.; Cross, F.R.; Cowburn, D.; Chait, B.T. Accurate quantitation of protein expression and site-specific phosphorylation. Proc. Natl. Acad. Sci. USA 1999, 96, 6591–6596.
98. De Godoy, L.M. SILAC yeast: From labeling to comprehensive proteome quantification. In Shotgun Proteomics; Martins-de-Souza, D., Ed.; Springer: New York, NY, USA, 2014; pp. 81–109.
99. Phillips, C.M.; Iavarone, A.T.; Marletta, M.A. Quantitative proteomic approach for cellulose degradation by Neurospora crassa. J. Proteome Res. 2011, 10, 4177–4185.
100. Wasinger, V.C.; Zeng, M.; Yau, Y. Current status and advances in quantitative proteomic mass spectrometry. Int. J. Proteomics 2013, doi:10.1155/2013/180605.
101. Liu, H.; Sadygov, R.G.; Yates, J.R., III. A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal. Chem. 2004, 76, 4193–4201.
102. Zybailov, B.; Coleman, M.K.; Florens, L.; Washburn, M.P. Correlation of relative abundance ratios derived from peptide ion chromatograms and spectrum counting for quantitative proteomic analysis using stable isotope labeling. Anal. Chem. 2005, 77, 6218–6224.
103. Zybailov, B.; Mosley, A.L.; Sardiu, M.E.; Coleman, M.K.; Florens, L.; Washburn, M.P. Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. J. Proteome Res. 2006, 5, 2339–2347.
104. Lu, P.; Vogel, C.; Wang, R.; Yao, X.; Marcotte, E.M. Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat. Biotechnol. 2006, 25, 117–124.
105. Ishihama, Y.; Oda, Y.; Tabata, T.; Sato, T.; Nagasu, T.; Rappsilber, J.; Mann, M. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol. Cell Proteomics 2005, 4, 1265–1272.
106. Adav, S.S.; Cheow, E.S.H.; Ravindran, A.; Dutta, B.; Sze, S.K. Label free quantitative proteomic analysis of secretome by Thermobifida fusca on different lignocellulosic biomass. J. Proteomics 2012, 75, 3694–3706.
107. Arike, L.; Peil, L. Spectral counting label-free proteomics. In Shotgun Proteomics; Martins-de-Souza, D., Ed.; Springer: New York, NY, USA, 2014; pp. 213–222.
108. Tjalsma, H.; Bolhuis, A.; Jongbloed, J.D.H.; Bron, S.; van Dijl, J.M. Signal peptidedependent protein transport in Bacillus subtilis: A genome-based survey of the secretome. Microb. Mol. Biol. Rev. 2000, 64, 515–547.
109. Alfaro, M.; Oguiza, J.A.; Ramírez, L.; Pisabarro, A.G. Comparative analysis of secretomes in basidiomycete fungi. J. Proteomics 2014, 102, 28–43.
110. Nickel, W.; Seedorf, M. Unconventional mechanisms of protein transport to the cell surface of eukaryotic cells. Annu. Rev. Cell Dev. Biol. 2008, 24, 287–308.
111. Bouws, H.; Wattenberg, A.; Zorn, H. Fungal secretomes—Nature’s toolbox for white biotechnology. Appl. Microbiol. Biotechnol. 2008, 80, 381–388.
112. Adav, S.S.; Sze, S.K. Fungal secretome for biorefinery: Recent advances in proteomic technology. Mass Spectrom. Lett. 2013, 4, 1–9.
113. Kubicek, C.P. Systems biological approaches towards understanding cellulase production by Trichoderma reesei. J. Biotechnol. 2013, 163, 133–142.
114. Martinez, D.; Berka, R.; Henrissat, B.; Saloheimo, M.; Arvas, M.; Baker, S.E.; Chapman, J.; Chertkov, O.; Coutinho, P.M.; Cullen, D, et al. Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat. Biotechnol. 2008, 26, 553–560.
115. Cherry, J.R.; Fidantsef, A.L. Directed evolution of industrial enzymes: An update. Curr. Opin. Biotechnol. 2003, 14, 438–443.
116. Adav, S.S.; Ravindran, A.; Sze, S.K. Proteomic analysis of temperature dependent extracellular proteins from Aspergillus fumigatus grown under solid-state culture condition. J. Proteome Res. 2013, 12, 2715–2731.
117. Chundawat, S.P.; Lipton, M.S.; Purvine, S.O.; Uppugundla, N.; Gao, D.; Balan, V.; Dale, B.E. Proteomics-based compositional analysis of complex cellulase-hemicellulase mixture. J. Proteome Res. 2011, 10, 4365–4372.
118. Ohtsuki, T.; Yazaki, S.; Ui, S.; Mimura, A. Production of large multienzyme complex by aerobic thermophilic fungus Chaetomium sp. nov. MS-017 grown on palm oil mill fibre. Lett. Appl. Microbiol. 2005, 40, 111–116.
119. Callegari, E.; Navarrete, N. The use of mass spectrometry for characterization of fungal secretomes. In Tandem Mass Spectrometry—Applications and Principles; Prasain, K.J., Ed.; InTech: Rijeka, Croatia, 2012; doi:10.5772/30908.
120. Langston, J.A.; Shaghasi, T.; Abbate, E.; Xu, F.; Vlasenko, E.; Sweeney, M.D. Oxidoreductive cellulose depolymerization by the enzymes cellobiose dehydrogenase and glycoside hydrolase 61. Appl. Environ. Microbiol. 2011, 77, 7007–7015.
121. Chang, K.L.; Thitikorn-amorn, J.; Hsieh, J.F.; Ou, B.M.; Chen, S.H.; Ratanakhanokchai, K.; Huang, P.J.; Chen, S.T. Enhanced enzymatic conversion with freeze pretreatment of rice straw. Biomass Bioenergy 2011, 35, 90–95.
122. Sun, Y.; Cheng, J.Y. Hydrolysis of lignocellulosic materials for ethanol production: A review. Bioresour. Technol. 2002, 83, 1–11.
123. Palmqvist, E.; Hahn-Hägerdal, B. Fermentation of lignocellulosic hydrolysates. II: Inhibitors and mechanisms of inhibition. Bioresour. Technol. 2000, 74, 25–33.
124. Martinez, D.; Larrondo, L.F.; Putnam, N.; Gelpke, M.D.S.; Huang, K.; Chapman, J.; Helfenbein, K.G.; Ramaiya, P.; Detter, J.C.; Larimer, F, et al. Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP 78. Nat. Biotechnol. 2004, 22, 695–700.
125. Wymelenberg, A.V.; Sabat, G.; Martinez, D.; Rajangam, A.S.; Teeri, T.T.; Gaskell, J.; Kersten, P.J.; Cullen, D. The Phanerochaete chrysosporium secretome: Database predictions and initial mass spectrometry peptide identifications in cellulose-grown medium. J. Biotechnol. 2005, 118, 17–34.
126. Wymelenberg, A.V.; Minges, P.; Sabat, G.; Martinez, D.; Aerts, A.; Salamov, A.; Grigoriev, I.; Shapiro, H.; Putnam, N.; Belinky, P, et al. Computational analysis of the Phanerochaete chrysosporium v2.0 genome database and mass spectrometry identification of peptides in ligninolytic cultures reveal complex mixtures of secreted proteins. Fungal Genet. Biol. 2006, 43, 343–356.
127. Sato, S.; Liu, F.; Koc, H.; Tien, M. Expression analysis of extracellular proteins from Phanerochaete chrysosporium grown on different liquid and solid substrates. Microbiology 2007, 153, 3023–3033.
128. Henriksson, G.; Zhang, L.; Li, J.; Ljungquist, P.; Reitberger, T.; Pettersson, G.; Johansson, G. Is cellobiose dehydrogenase from Phanerochaete chrysosporium a lignin degrading enzyme? Biochim. Biophys. Acta 2000, 1480, 83–91.
129. Ander, P.; Marzullo, L. Sugar oxidoreductases and veratryl alcohol oxidase as related to lignin degradation. J. Biotechnol. 1997, 53, 115–131.
130. Hori, C.; Gaskell, J.; Igarashi, K.; Kersten, P.; Mozuch, M.; Samejima, M.; Cullen, D. Temporal alterations in the secretome of the selective ligninolytic fungus Ceriporiopsis subvermispora during growth on aspen wood reveal this organism’s strategy for degrading lignocellulose. Appl. Environ. Microbiol. 2014, 80, 2062–2070.
131. Perrotta, G.; Bianco, L.; Carbone, F.; Daddiego, L.; Facella, P.; Lopez, L. Functional metagenomic and proteomic characterization of soil microbial community associated with decomposing reeds. New Biotechnol. 2014, 31, S170–S171.
132. Baldrian, P.; López-Mondéjar, R. Microbial genomics, transcriptomics and proteomics: New discoveries in decomposition research using complementary methods. Appl. Microbiol. Biotechnol. 2014, 98, 1531–1537.
133. Adav, S.S.; Ravindran, A.; Cheow, E.S.H.; Sze, S.K. Quantitative proteomic analysis of secretome of microbial consortium during saw dust utilization. J. Proteomics 2012, 75, 5590–5603.
134. Novotný, Č.; Svobodová, K.; Erbanová, P.; Cajthaml, T.; Kasinath, A.; Lang, E.; Šašek, V. Ligninolytic fungi in bioremediation: extracellular enzyme production and degradation rate. Soil Biol. Biochem. 2004, 36, 1545–1551.
135. More, T.T.; Yan, S.; Tyagi, R.D.; Surampalli, R.Y. Potential use of filamentous fungi for wastewater sludge treatment. Bioresour. Technol. 2010, 101, 7691–7700.
136. Gadd, G.M. Fungi in Bioremediation; Cambridge University Press: Cambridge, UK, 2001; p. 496.
137. Reina, R.; Kellner, H.; Jehmlich, N.; Ullrich, R.; García-Romera, I.; Aranda, E.; Liers, C. Differences in the secretion pattern of oxidoreductases from Bjerkandera adusta induced by a phenolic olive mill extract. Fungal Genet. Biol. 2014, 72, 99–105.
138. Korniłłowicz-Kowalska, T.; Rybczyńska, K. Anthraquinone dyes decolorization capacity of anamorphic Bjerkandera adusta CCBAS 930 strain and its HRP-like negative mutants. World J. Microbiol. Biotechnol. 2014, 30, 1725–1736.
139. Anastasi, A.; Spina, F.; Prigione, V.; Tigini, V.; Giansanti, P.; Varese, G.C. Scale-up of a bioprocess for textile wastewater treatment using Bjerkandera adusta. Bioresour. Technol. 2010, 101, 3067–3075.