Exploring Fungi-Associated Lignocellulose Degradation: Secretomic and Proteomic Approaches

  • Akshay Shankar
  • Shruti Ahlawat
  • Krishna Kant SharmaEmail author


Filamentous fungi of phyla Basidiomycota and Ascomycota are the group of microorganisms that are capable of secreting a variety of proteins and other secondary metabolites depending on the environment and culture conditions. The protein constitutes the hydrolytic enzymes which cause the deconstruction of the plant cell wall and has applicability in several biotechnological processes including second-generation ethanol production. Secretomic and proteomic analysis of the fungi is an excellent tool to find out the biological mechanisms of lignocellulose degradation. Furthermore, it is also an important tool to search for novel enzymes or metabolites of the biotechnology field. Extracellular secretion of the protein from different fungal species has been studied using different high-throughput techniques such as 2-D PAGE, MALDI-ToF/ToF, LC-MS/MS, iTRAQ technique using LC-MS/MS, and Nano-LC-MS/MS protein mass spectrometry. Bioinformatics tools have equal importance in the prediction and profiling of the expressed proteins, according to the current database. For this reason, publications documenting the fungal secretome and proteome have increased significantly in the past few years. Herein, we have updated the development and evolution of the proteome/secretome technology and its application in the protein profiling and functional genomics of the economically important filamentous fungi.


Fungi Proteome Secretome Lignocelluloses Mass spectrometry Liquid chromatography 



The authors acknowledge Maharshi Dayanand University for the infrastructure facilities. FIST-DST grant to the Department of Microbiology is sincerely acknowledged.


  1. Abbas A, Koc H, Liu F, Tien M (2005) Fungal degradation of wood: initial proteomic analysis of extracellular proteins of Phanerochaete chrysosporium grown on oak substrate. Curr Genet 47:49–56PubMedCrossRefPubMedCentralGoogle Scholar
  2. Abdallah C, Dumas-Gaudot E, Renaut J, Sergeant K (2012) Gel-based and gel-free quantitative proteomics approaches at a glance. Int J Plant Genom 2012:494572Google Scholar
  3. Adav SS, Li AA, Manavalan A, Punt P, Sze SK (2010) Quantitative iTRAQ secretome analysis of Aspergillus niger reveals novel hydrolytic enzymes. J Proteome Res 9(8):3932–3940PubMedCrossRefPubMedCentralGoogle Scholar
  4. Adav SS, Ravindran A, Chao LT, Tan L, Singh S, Sze SK (2011) Proteomic analysis of pH and strains dependent protein secretion of Trichoderma reesei. J Proteome Res 10:4579–4596PubMedCrossRefPubMedCentralGoogle Scholar
  5. Adav SS, Ravindran A, Cheow ES, Sze SK (2012a) Quantitative proteomic analysis of secretome of microbial consortium during saw dust utilization. J Proteome 75(18):5590–5603CrossRefGoogle Scholar
  6. Adav SS, Ravindran A, Sze SK (2012b) Quantitative proteomic analysis of lignocellulolytic enzymes by Phanerochaete chrysosporium on different lignocellulosic biomass. J Proteome 75(5):1493–1504CrossRefGoogle Scholar
  7. Adav SS, Ravindran A, Sze SK (2014) Study of Phanerochaete chrysosporium secretome revealed protein glycosylation as a substrate-dependent post-translational modification. J Proteome Res 13(10):4272–4280PubMedCrossRefPubMedCentralGoogle Scholar
  8. Adav SS, Ravindran A, Sze SK (2015) Quantitative proteomic study of Aspergillus fumigatus secretome revealed deamidation of secretory enzymes. J Proteome 119:154–168CrossRefGoogle Scholar
  9. Adsul MG, Bastawde KB, Varma AJ, Gokhale DV (2007) Strain improvement of Penicillium janthinellum NCIM 1171 for increased cellulase production. Bioresour Technol 98(7):1467–1473PubMedCrossRefPubMedCentralGoogle Scholar
  10. Alfaro M, Oguiza JA, Ramirez L, Pisabarro AG (2014) Comparative analysis of secretomes in basidiomycete fungi. J Proteome 102:28–43CrossRefGoogle Scholar
  11. Bantscheff M, Schirle M, Sweetman G, Rick J, Kuster B (2007) Quantitative mass spectrometry in proteomics: a critical review. Anal Bioanal Chem 389(4):1017–1031PubMedCrossRefPubMedCentralGoogle Scholar
  12. Bianco L, Perrotta G (2016) Fruit development and ripening: proteomic as an approach to study Olea Europaea and other non-model organisms. Agric Proteomics 1:53–65CrossRefGoogle Scholar
  13. Bouws H, Wattenberg A, Zorn H (2008) Fungal secretomes-nature’s toolbox for white biotechnology. Appl Microbiol Biotechnol 80(3):381PubMedCrossRefPubMedCentralGoogle Scholar
  14. Cai Y, Gong Y, Liu W, Hu Y, Chen L, Yan L, Zhou Y, Bian Y (2017) Comparative secretomic analysis of lignocelluloses degradation by Lentinula edodes grown on microcrystalline cellulose, lignosulfonate and glucose. J Proteome 163:92–101CrossRefGoogle Scholar
  15. Carvalho W, Canilha L, Ferraz A, Milagres AM (2009) An overview of wood structure, composition and biodegradation. Nova Chem 32(8):1–5Google Scholar
  16. Chen S, Xu J, Liu C, Zhu Y, Nelson DR, Zhou S, Li C, Wang L, Guo X, Sun Y, Luo H (2012) Genome sequence of the model medicinal mushroom Ganoderma lucidum. Nat Commun 3:913PubMedPubMedCentralCrossRefGoogle Scholar
  17. Chutani P, Sharma KK (2015) Biochemical evaluation of xylanases from various filamentous fungi and their application for the deinking of ozone treated newspaper pulp. Carbohydr Polym 127:54–63PubMedCrossRefPubMedCentralGoogle Scholar
  18. Chutani P, Sharma KK (2016) Concomitant production of xylanases and cellulases from Trichoderma longibrachiatum MDU-6 selected for the deinking of paper waste. Bioprocess Biosyst Eng 39(5):747–758PubMedCrossRefPubMedCentralGoogle Scholar
  19. Claus H (2004) Laccases: structure, reactions, distribution. Micron 35(1-2):93–96PubMedCrossRefPubMedCentralGoogle Scholar
  20. Coleman JJ, Rounsley SD, Rodriguez-Carres M, Kuo A, Wasmann CC, Grimwood J, Schmutz J, Taga M, White GJ, Zhou S, Schwartz DC (2009) The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genet 5(8):e1000618PubMedPubMedCentralCrossRefGoogle Scholar
  21. Collier TS, Hawkridge AM, Georgianna DR, Payne GA, Muddiman DC (2008) Top-down identification and quantification of stable isotope labeled proteins from Aspergillus flavus using online nano-flow reversed-phase liquid chromatography coupled to a LTQ-FTICR mass spectrometer. Anal Chem 80(13):4994–5001PubMedPubMedCentralCrossRefGoogle Scholar
  22. Couturier M, Navarro D, Favel A, Haon M, Lechat C, Lesage-Meessen L, Chevret D, Lombard V, Henrissat B, Berrin JG (2016) Fungal secretomics of ascomycete fungi for biotechnological applications. Mycosphere J 7(10):1546–1553CrossRefGoogle Scholar
  23. Craig R, Beavis RC (2004) TANDEM: matching proteins with tandem mass spectra. Bioinformatics 20(9):1466–1467PubMedPubMedCentralCrossRefGoogle Scholar
  24. de Gouvea PF, Bernardi AV, Gerolamo LE, de Souza SE, Riano-Pachon DM, Uyemura SA, Dinamarco TM (2018) Transcriptome and secretome analysis of Aspergillus fumigatus in the presence of sugarcane bagasse. BMC Genomics 19(1):232PubMedPubMedCentralCrossRefGoogle Scholar
  25. de Oliveira JM, van Passel MW, Schaap PJ, de Graaff LH (2011) Proteomic analysis of the secretory response of Aspergillus niger to D-maltose and D-xylose. PLoS One 6(6):e20865PubMedCrossRefPubMedCentralGoogle Scholar
  26. de Souza WR, de Gouvea PF, Savoldi M, Malavazi I, de Souza Bernardes LA, Goldman MHS, Goldman GH (2011) Transcriptome analysis of Aspergillus niger grown on sugarcane bagasse. Biotechnol Biofuels 4(1):40PubMedPubMedCentralCrossRefGoogle Scholar
  27. Dix NJ, Webster J (1995) Colonization and decay of wood. In: Fungal ecology. Springer, Dordrecht, pp 145–171CrossRefGoogle Scholar
  28. Doyle S (2011) Fungal proteomics: from identification to function. FEMS Microbiol Lett 321(1):1–9PubMedCrossRefPubMedCentralGoogle Scholar
  29. Eastwood DC, Floudas D, Binder M, Majcherczyk A, Schneider P, Aerts A, Asiegbu FO, Baker SE, Barry K, Bendiksby M, Blumentritt M (2011) The plant cell wall–decomposing machinery underlies the functional diversity of forest fungi. Science 333(6043):762–765PubMedPubMedCentralCrossRefGoogle Scholar
  30. Efstathiou G, Antonakis AN, Pavlopoulos GA, Theodosiou T, Divanach P, Trudgian DC, Thomas B, Papanikolaou N, Aivaliotis M, Acuto O, Iliopoulos I (2017) ProteoSign: an end-user online differential proteomics statistical analysis platform. Nucleic Acids Res 45(W1):W300–W306PubMedPubMedCentralCrossRefGoogle Scholar
  31. Erden E, Ucar MC, Gezer T, Pazarlioglu NK (2009) Screening for ligninolytic enzymes from autochthonous fungi and applications for decolorization of Remazole Marine Blue. Braz J Microbiol 40(2):346–353PubMedPubMedCentralCrossRefGoogle Scholar
  32. Fernandez-Fueyo E, Ruiz-Duenas FJ, Ferreira P, Floudas D, Hibbett DS, Canessa P (2012) Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis. Proc Natl Acad Sci U S A 109:5458–5463PubMedPubMedCentralCrossRefGoogle Scholar
  33. Fernandez-Fueyo E, Ruiz-Duenas FJ, Lopez-Lucendo MF, Perez-Boada M, Rencoret J, Gutierrez A, Pisabarro AG, Ramirez L, Martinez AT (2016) A secretomic view of woody and nonwoody lignocellulose degradation by Pleurotus ostreatus. Biotechnol Biofuels 9(1):49PubMedPubMedCentralCrossRefGoogle Scholar
  34. Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martínez AT, Otillar R, Spatafora JW, Yadav JS, Aerts A (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336(6089):1715–1719PubMedPubMedCentralCrossRefGoogle Scholar
  35. Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, FitzHugh W, Ma LJ, Smirnov S, Purcell S, Rehman B, Elkins T, Engels R, Wang S, Nielsen CB, Butler J, Endrizzi M, Qui D, Ianakiev P, Bell-Pedersen D, Nelson MA, Werner-Washburne M, Selitrennikoff CP, Kinsey JA, Braun EL, Zelter A, Chulte U, Kothe GO, Jedd G, Mewes W, Staben C, Marcotte E, Greenberg D, Roy A, Foley K, Naylor J, Stange-Thomann N, Barrett R, Gnerre S, Kamal M, Kamvysselis M, Mauceli E, Bielke C, Rudd S, Frishman D, Krystofova S, Rasmussen C, Metzenberg RL, Perkins DD, Kroken S, Cogoni C, Macino G, Catcheside D, Li W, Pratt RJ, Osmani SA, DeSouza CP, Glass L, Orbach MJ, Berglund JA, Voelker R, Yarden O, Plamann M, Seiler S, Dunlap J, Radford A, Aramayo R, Natvig DO, Alex LA, Mannhaupt G, Ebbole DJ, Freitag M, Paulsen I, Sachs MS, Lander ES, Nusbaum C, Birren B (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422(6934):859–868CrossRefGoogle Scholar
  36. Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, Batzoglou S, Lee SI, Başturkmen M, Spevak CC, Clutterbuck J, Kapitonov V, Jurka J, Scazzocchio C, Farman M, Butler J, Purcell S, Harris S, Braus GH, Draht O, Busch S, D'Enfert C, Bouchier C, Goldman GH, Bell-Pedersen D, Griffiths-Jones S, Doonan JH, Yu J, Vienken K, Pain A, Freitag M, Selker EU, Archer DB, Penalva MA, Oakley BR, Momany M, Tanaka T, Kumagai T, Asai K, Machida M, Nierman WC, Denning DW, Caddick M, Hynes M, Paoletti M, Fischer R, Miller B, Dyer P, Sachs MS, Osmani SA, Birren BW (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438(7071):1105–1115PubMedCrossRefPubMedCentralGoogle Scholar
  37. Glenn JK, Morgan MA, Mayfield MB, Kuwahara M, Gold MH (1983) An extracellular H2O2-requiring enzyme preparation involved in lignin biodegradation by the white rot basidiomycete Phanerochaete chrysosporium. Biochem Biophys Res Commun 114(3):1077–1083PubMedCrossRefGoogle Scholar
  38. Graham C, McMullan G, Graham RL (2011) Proteomics in the microbial sciences. Bioeng Bugs 2(1):17–30PubMedCrossRefPubMedCentralGoogle Scholar
  39. Gygi SP, Rist B, Gerber SA, Turecek F, Gelb MH, Aebersold R (1999) Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat Biotechnol 10:994CrossRefGoogle Scholar
  40. Hagglund P, Bunkenborg J, Maeda K, Svensson B (2008) Identification of thioredoxin disulfide targets using a quantitative proteomics approach based on isotope-coded affinity tags. J Proteome Res 7(12):5270–5276PubMedCrossRefPubMedCentralGoogle Scholar
  41. Hakkinen M, Arvas M, Oja M, Aro N, Penttilä 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 Factories 11(1):134CrossRefGoogle Scholar
  42. Han X, Aslanian A, Yates JR III (2008) Mass spectrometry for proteomics. Curr Opin Chem Biol 12(5):483–490PubMedPubMedCentralCrossRefGoogle Scholar
  43. Henriksson G, Johansson G, Pettersson G (2000a) A critical review of cellobiose dehydrogenases. J Biotechnol 78(2):93–113PubMedCrossRefGoogle Scholar
  44. Henriksson G, Zhang L, Li J, Ljungquist P, Reitberger T, Pettersson G, Johansson G (2000b) Is cellobiose dehydrogenase from Phanerochaete chrysosporium a lignin degrading enzyme? Biochim Biophys Acta Protein Struct Mol Enzymol 1480(1–2):83–91CrossRefGoogle Scholar
  45. Henzel WJ, Billeci TM, Stults JT, Wong SC, Grimley C, Watanabe C (1993) Identifying proteins from two-dimensional gels by molecular mass searching of peptide fragments in protein sequence databases. Proc Natl Acad Sci 90(11):5011–5015PubMedCrossRefGoogle Scholar
  46. Hibbett DS, Donoghue MJ (2001) Analysis of character correlations among wood decay mechanisms, mating systems, and substrate ranges in homobasidiomycetes. Syst Biol 50(2):215–242PubMedCrossRefPubMedCentralGoogle Scholar
  47. Hoegger PJ, Kilaru S, James TY, Thacker JR, Kües U (2006) Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS J 273(10):2308–2326PubMedCrossRefGoogle Scholar
  48. Hoegger P, Majcherczyk A, Dwivedi R, Svobodova K, Kilaru S, Kües U (2007) Enzymes in wood degradation. In: Kües U (ed) Wood prod. Wood technol. Biotechnol. Impacts. Universitätsverlag Göttingen, Göttingen, pp 383–432Google Scholar
  49. Hofrichter M (2002) Lignin conversion by manganese peroxidase (MnP). Enzym Microb Technol 30(4):454–466CrossRefGoogle Scholar
  50. Hori C, Igarashi K, Katayama A, Samejima M (2011) Effects of xylan and starch on secretome of the basidiomycete Phanerochaete chrysosporium grown on cellulose. FEMS Microbiol Lett 321(1):14–23PubMedCrossRefGoogle Scholar
  51. Hori C, Gaskell J, Igarashi K, Samejima M, Hibbett D, Henrissat B, Cullen D (2013) Genome wide analysis of polysaccharides degrading enzymes in 11 white-and brown-rot Polyporales provides insight into mechanisms of wood decay. Mycologia 105(6):1412–1427PubMedCrossRefPubMedCentralGoogle Scholar
  52. Hori C, Gaskell J, Igarashi K, Kersten P, Mozuch M, Samejima M, Cullen D (2014) Temporal alterations in secretome of selective ligninolytic fungi Ceriporiopsis subvermispora during growth on aspen wood reveal its strategy of degrading lignocellulose. Appl Environ Microbiol 17:AEM-03652Google Scholar
  53. Horth P, Miller CA, Preckel T, Wenz C (2006) Efficient fractionation and improved protein identification by peptide OFFGEL electrophoresis. Mol Cell Proteomics 5(10):1968–1974PubMedCrossRefGoogle Scholar
  54. Jain KK, Kumar A, Shankar A, Pandey D, Chaudhary B, Sharma KK (2019) De novo transcriptome assembly and protein profiling of copper-induced lignocellulolytic fungus Ganoderma lucidum MDU-7 reveals genes involved in lignocellulose degradation and terpenoid biosynthetic pathways. Genomics.
  55. Ji XL, Zhang WT, Gai YP, Lu BY, Yuan CZ, Liu QX, Mu ZM (2012) Patterns of lignocellulose degradation and secretome analysis of Trametes trogii MT. Int Biodeterior Biodegradation 75:55–62CrossRefGoogle Scholar
  56. Juhasz T, Szengyel Z, Reczey K, Siika-Aho M, Viikari L (2005) Characterization of cellulases and hemicellulases produced by Trichoderma reesei on various carbon sources. Process Biochem 40(11):3519–3525CrossRefGoogle Scholar
  57. Jungblut PR, Holzhütter HG, Apweiler R, Schlüter H (2008) The speciation of the proteome. Chem Cent J 2(1):16PubMedPubMedCentralCrossRefGoogle Scholar
  58. Kellner H, Vandenbol M (2010) Fungi unearthed: transcripts encoding lignocellulolytic and chitinolytic enzymes in forest soil. PLoS One 5(6):e10971PubMedPubMedCentralCrossRefGoogle Scholar
  59. Kersten P, Cullen D (2007) Extracellular oxidative systems of the lignin-degrading Basidiomycete Phanerochaete chrysosporium. Fungal Genet Biol 44(2):77–87PubMedCrossRefPubMedCentralGoogle Scholar
  60. Kim Y, Nandakumar MP, Marten MR (2007) Proteomics of filamentous fungi. Trends Biotechnol 25(9):395–400PubMedCrossRefPubMedCentralGoogle Scholar
  61. Knezević A, Milovanović I, Stajić M, Vukojević J (2013) Potential of Trametes species to degrade lignin. Int Biodeterior Biodegradation 85:52–56CrossRefGoogle Scholar
  62. Krijger JJ, Thon MR, Deising HB, Wirsel SG (2014) Compositions of fungal secretomes indicate a greater impact of phylogenetic history than lifestyle adaptation. BMC Genomics 15(1):722PubMedPubMedCentralCrossRefGoogle Scholar
  63. Kumar A, Sharma KK, Kumar P, Ramchiary N (2015) Laccase isozymes from Ganoderma lucidum MDU-7: isolation, characterization, catalytic properties and differential role during oxidative stress. J Mol Catal B Enzym 113:68–75CrossRefGoogle Scholar
  64. Kumar A, Singh D, Sharma KK, Arora S, Singh AK, Gill SS, Singhal B (2017) Gel-based purification and biochemical study of laccase isozymes from Ganoderma sp. and its role in enhanced cotton callogenesis. Front Microbiol 8:674PubMedPubMedCentralCrossRefGoogle Scholar
  65. Lamer S, Jungblut PR (2001) Matrix-assisted laser desorption-ionization mass spectrometry peptide mass fingerprinting for proteome analysis: identification efficiency after on-blot or in-gel digestion with and without desalting procedures. J Chromatogr B Biomed Sci Appl 752(2):311–322PubMedCrossRefPubMedCentralGoogle Scholar
  66. Le Marquer M, Clemente HS, Roux C, Savelli B, dit Frey NF (2019) Identification of new signalling peptides through a genome-wide survey of 250 fungal secretomes. BMC Genomics 20(1):64. Scholar
  67. Lebrun JD, Demont-Caulet N, Cheviron N, Laval K, Trinsoutrot-Gattin I, Mougin C (2011) Secretion profiles of fungi as potential tools for metal ecotoxicity assessment: a study of enzymatic system in Trametes versicolor. Chemosphere 82(3):340–345PubMedCrossRefPubMedCentralGoogle Scholar
  68. Link AJ, Eng J, Schieltz DM, Carmack E, Mize GJ, Morris DR, Garvik BM, Yates JR (1999) Direct analysis of protein complexes using mass spectrometry. Nat Biotechnol 17(7):676PubMedCrossRefPubMedCentralGoogle Scholar
  69. Liu D, Li J, Zhao S, Zhang R, Wang M, Miao Y, Shen Y, Shen Q (2013) Secretome diversity and quantitative analysis of cellulolytic Aspergillus fumigatus Z5 in the presence of different carbon sources. Biotechnology for Biofuels 6(1):149PubMedPubMedCentralCrossRefGoogle Scholar
  70. Lu X, Sun J, Nimtz M, Wissing J, Zeng AP, Rinas U (2010) The intra-and extracellular proteome of Aspergillus niger growing on defined medium with xylose or maltose as carbon substrate. Microb Cell Factories 9(1):23CrossRefGoogle Scholar
  71. Machida M, Asai K, Sano M, Tanaka T, Kumagai T, Terai G, Kusumoto KI, Arima T, Akita O, Kashiwagi Y, Abe K (2005) Genome sequencing and analysis of Aspergillus oryzae. Nature 438(7071):1157PubMedCrossRefGoogle Scholar
  72. Maciel MJ, Ribeiro HC (2010) Industrial and biotechnological applications of ligninolytic enzymes of the basidiomycota: a review. Electron J Biotechnol 13(6):14–15Google Scholar
  73. Manavalan A, Adav SS, Sze SK (2011) iTRAQ-based quantitative secretome analysis of Phanerochaete chrysosporium. J Proteome 75(2):642–654CrossRefGoogle Scholar
  74. Manavalan T, Manavalan A, Thangavelu KP, Heese K (2012) Secretome analysis of Ganoderma lucidum cultivated in sugarcane bagasse. J Proteom 77:298–309CrossRefGoogle Scholar
  75. Martinez D, Larrondo LF, Putnam N, Gelpke MD, Huang K, Chapman J, Helfenbein KG, Ramaiya P, Detter JC, Larimer F, Coutinho PM (2004) Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol 22(6):695PubMedCrossRefPubMedCentralGoogle Scholar
  76. Martinez D, Berka RM, Henrissat B, Saloheimo M, Arvas M, Baker SE, Danchin EG (2008) Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nature Biotechnol 26(5):553CrossRefGoogle Scholar
  77. Martínez D, Challacombe J, Morgenstern I, Hibbett DS, Schmoll M, Kubicek CP, Ferreira P, Ruiz-Duenas FJ, Martinez AT, Kersten P, Hammel KE, Vanden-Wymelenberg A, Gaskell J, Lindquist E, Sabat G, Bondurant SS, Larrondo LF, Canessa P, Vicuna R, Yadav J, Doddapaneni H, Subramanian V, Pisabarro AG, Lavin JL, Oguiza JA, Master E, Henrissat B, Coutinho PM, Harris P, Magnuson JK, Baker SE, Bruno K, Kenealy W, Hoegger PJ, Kues U, Ramaiya P, Lucas S, Salamov A, Shapiro H, Tu H, Chee CL, Misra M, Xie G, Teter S, Yaver D, James T, Mokrejs M, Pospisek M, Grigoriev IV, Brettin T, Rokhsar D, Berka R, Cullen D (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci U S A 106:1954–1959PubMedPubMedCentralCrossRefGoogle Scholar
  78. Mathieu Y, Piumi F, Valli R, Aramburu JC, Ferreira P, Faulds C, Record E (2016) Secreted aryl alcohol quinone oxidoreductases from Pycnoporus cinnabarinus provides new activities and insights into fungal degradation of plant biomass. Appl Environ Microbiol 12:AEM-03761Google Scholar
  79. Mattow J, Schaible UE, Schmidt F, Hagens K, Siejak F, Brestrich G, Haeselbarth G, Müller EC, Jungblut PR, Kaufmann SH (2003) Comparative proteome analysis of culture supernatant proteins from virulent Mycobacterium tuberculosis H37Rv and attenuated M. bovis BCG Copenhagen. Electrophoresis 24(19-20):3405–3420PubMedCrossRefPubMedCentralGoogle Scholar
  80. Mayer AM, Staples RC (2002) Laccase: new functions for an old enzyme. Phytochemistry 60(6):551–565PubMedCrossRefPubMedCentralGoogle Scholar
  81. Minden J (2007) Comparative proteomics and difference gel electrophoresis. Biotechniques 43(6):739–745PubMedCrossRefPubMedCentralGoogle Scholar
  82. Minussi RC, Miranda MA, Silva JA, Ferreira CV, Aoyama H, Marangoni S, Rotilio D, Pastore GM, Durán N (2007) Purification, characterization and application of laccase from Trametes versicolor for colour and phenolic removal of olive mill wastewater in the presence of 1-hydroxybenzotriazole. Afr J Biotechnol 6(2):1–10Google Scholar
  83. Miura N, Ueda M (2018) Evaluation of unconventional protein secretion by Saccharomyces cerevisiae and other fungi. Cell 7(9):128CrossRefGoogle Scholar
  84. Mukherjee P, Mani S (2013) Methodologies to decipher the cell secretome. Biochim Biophys Acta Protein Proteomics 1834(11):2226–2232CrossRefGoogle Scholar
  85. Nagele E, Vollmer M, Hörth P (2003) Two-dimensional nano-liquid chromatography-mass spectrometry system for applications in proteomics. J Chromatogr A 1009(1-2):197–205PubMedCrossRefPubMedCentralGoogle Scholar
  86. Nitsche BM, Jørgensen TR, Akeroyd M, Meyer V, Ram AF (2012) The carbon starvation response of Aspergillus niger during submerged cultivation: insights from the transcriptome and secretome. BMC Genomics 13(1):380PubMedPubMedCentralCrossRefGoogle Scholar
  87. O’Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250(10):4007–4021PubMedPubMedCentralGoogle Scholar
  88. Pellegrin C, Morin E, Martin FM, Veneault-Fourrey C (2015) Comparative analysis of secretomes from ectomycorrhizal fungi with an emphasis on small-secreted proteins. Front Microbiol 18(6):1278Google Scholar
  89. Phalip V, Delalande F, Carapito C, Goubet F, Hatsch D, Leize-Wagner E, Dupree P, Van Dorsselaer A, Jeltsch JM (2005) Diversity of the exoproteome of Fusarium graminearum grown on plant cell wall. Curr Genet 48(6):366–379PubMedCrossRefPubMedCentralGoogle Scholar
  90. Phillips CM, Iavarone AT, Marletta MA (2011) Quantitative proteomic approach for cellulose degradation by Neurospora crassa. J Proteome Res 10(9):4177–4185PubMedCrossRefPubMedCentralGoogle Scholar
  91. Piontek K, Smith AT, Blodig W (2001) Lignin peroxidase structure and function. Biochem Soc Trans 29:111–116PubMedCrossRefPubMedCentralGoogle Scholar
  92. Poland J, Cahill MA, Sinha P (2003) Isoelectric focusing in long immobilized pH gradient gels to improve protein separation in proteomic analysis. Electrophoresis 24(7–8):1271–1275PubMedCrossRefPubMedCentralGoogle Scholar
  93. Ravalason H, Jan G, Molle D, Pasco M, Coutinho PM, Lapierre C, Pollet B, Bertaud F, Petit-Conil M, Grisel S, Sigoillot JC (2008) Secretome analysis of Phanerochaete chrysosporium strain CIRM-BRFM41 grown on softwood. Appl Microbiol Biotechnol 80(4):719–733PubMedCrossRefPubMedCentralGoogle Scholar
  94. Rohr CO, Levin LN, Mentaberry AN, Wirth SA (2013) A first insight into Pycnoporus sanguineus BAFC 2126 transcriptome. PLoS One 8(12):e81033PubMedPubMedCentralCrossRefGoogle Scholar
  95. Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, Hattan S, Khainovski N, Pillai S, Dey S, Daniels S, Purkayastha S (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 3(12):1154–1169PubMedCrossRefPubMedCentralGoogle Scholar
  96. Ruiz-Dueñas FJ, Martínez AT (2009) Microbial degradation of lignin: how a bulky recalcitrant polymer is efficiently recycled in nature and how we can take advantage of this. Microb Biotechnol 2(2):164–177PubMedPubMedCentralCrossRefGoogle Scholar
  97. Ruiz-Dueñas FJ, Pogni R, Morales M, Giansanti S, Mate MJ, Romero A, Martínez AT (2009) Protein radicals in fungal versatile peroxidase catalytic tryptophan radical in both compound I and compound II and studies on W164Y, W164H, and W164S variants. J Biol Chem 284(12):7986–7994PubMedPubMedCentralCrossRefGoogle Scholar
  98. San Ryu J, Shary S, Houtman CJ, Panisko EA, Korripally P, John FJ, Crooks C, Siika-aho M, Magnuson JK, Hammel KE (2011) Proteomic and functional analysis of the cellulase system expressed by Postia placenta during brown rot of solid wood. Appl Environ Microbiol 77:7933–7941CrossRefGoogle Scholar
  99. Sato S, Liu F, Koc H, Tien M (2007) Expression analysis of extracellular proteins from Phanerochaete chrysosporium grown on different liquid and solid substrates. Microbiology 153(9):3023–3033PubMedPubMedCentralCrossRefGoogle Scholar
  100. Saykhedkar S, Ray A, Ayoubi-Canaan P, Hartson SD, Prade R, Mort AJ (2012) A time course analysis of the extracellular proteome of Aspergillus nidulans growing on sorghum stover. Biotechnology for biofuels. 5(1):52PubMedPubMedCentralCrossRefGoogle Scholar
  101. Sharma KK (2016) Fungal genome sequencing: basic biology to biotechnology. Crit Rev Biotechnol 36(4):743–759PubMedPubMedCentralGoogle Scholar
  102. Sharma KK, Kuhad RC (2008) Laccase: enzyme revisited function redefined. Indian J Microbiol 48:309–316PubMedPubMedCentralCrossRefGoogle Scholar
  103. Sharma KK, Singh D, Singh B, Kuhad RC (2013) Ligninolytic enzymes in environmental management. In: Biotechnology for environmental management and resource recovery. Springer, India, pp 219–238CrossRefGoogle Scholar
  104. Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal Chem 68(5):850–858PubMedCrossRefPubMedCentralGoogle Scholar
  105. Sripuan T, Aoki K, Yamamoto K, Tongkao D, Kumagai H (2003) Purification and characterization of thermostable α-galactosidase from Ganoderma lucidum. Biosci Biotechnol Biochem 67(7):1485–1491PubMedCrossRefPubMedCentralGoogle Scholar
  106. Steffen W, Crutzen PJ, McNeill JR (2007) The Anthropocene: are humans now overwhelming the great forces of nature. AMBIO 36(8):614–621PubMedCrossRefPubMedCentralGoogle Scholar
  107. Stroher E, Dietz KJ (2006) Concepts and approaches towards understanding the cellular redox proteome. Plant Biol 8(4):407–418PubMedCrossRefPubMedCentralGoogle Scholar
  108. Tomsovsky M, Homolka L (2003) Laccase and other ligninolytic enzyme activities of selected strains of Trametes spp. from different localities and substrates. Folia Microbiol 48(3):413CrossRefGoogle Scholar
  109. Trejo-Hernandez MR, Lopez-Munguia A, Ramirez RQ (2001) Residual compost of Agaricus bisporus as a source of crude laccase for enzymic oxidation of phenolic compounds. Process Biochem 36(7):635–639CrossRefGoogle Scholar
  110. Vasina DV, Pavlov AR, Koroleva OV (2016) Extracellular proteins of Trametes hirsuta s t. 072 induced by copper ions and a lignocellulose substrate. BMC Microbiol 16(1):106PubMedPubMedCentralCrossRefGoogle Scholar
  111. Vincent D, Kohler A, Claverol S, Solier E, Joets J, Gibon J, Lebrun MH, Plomion C, Martin F (2011) Secretome of the free-living mycelium from the ectomycorrhizal basidiomycete Laccaria bicolor. J Proteome Res 11(1):157–171PubMedCrossRefPubMedCentralGoogle Scholar
  112. Vasina DV, Loginov DS, Koroleva OV (2013) Comparative proteomic study of the basidiomycete Trametes hirsuta grown on different substrates. Biochem Mosc 78(5):477–484CrossRefGoogle Scholar
  113. Waanders LF, Hanke S, Mann M (2007) Top-down quantitation and characterization of SILAC-labeled proteins. J Am Soc Mass Spectrom 18(11):2058–2064PubMedCrossRefPubMedCentralGoogle Scholar
  114. Wang B, Cai P, Sun W, Li J, Tian C, Ma Y (2015) A transcriptomic analysis of Neurospora crassa using five major crop residues and the novel role of the sporulation regulator rca-1 in lignocellulase production. Biotechnology for Biofuels 8(1):21PubMedPubMedCentralCrossRefGoogle Scholar
  115. Washburn MP, Wolters D, Yates JR III (2001) Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol 19(3):242PubMedCrossRefPubMedCentralGoogle Scholar
  116. Wiese S, Reidegeld KA, Meyer HE, Warscheid B (2007) Protein labeling by iTRAQ: a new tool for quantitative mass spectrometry in proteome research. Proteomics 7(3):340–350PubMedCrossRefPubMedCentralGoogle Scholar
  117. Wymelenberg AV, Minges P, Sabat G, Martinez D, Aerts A, Salamov A, Grigoriev I, Shapiro H, Putnam N, Belinky P, Dosoretz C (2006) 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 43(5):343–356CrossRefGoogle Scholar
  118. Wymelenberg AV, Gaskell J, Mozuch M, Kersten P, Sabat G, Martinez D, Cullen D (2009) Transcriptome and secretome analyses of Phanerochaete chrysosporium reveal complex patterns of gene expression. Appl Environ Microbiol 75(12):4058–4068CrossRefGoogle Scholar
  119. Wymelenberg AV, Gaskell J, Mozuch M, Sabat G, Ralph J, Skyba O, Mansfield SD, Blanchette RA, Martinez D, Grigoriev I, Kersten PJ (2010) Comparative transcriptome and secretome analysis of wood decay fungi Postia placenta and Phanerochaete chrysosporium. Appl Environ Microbiol 76(11):3599–3610CrossRefGoogle Scholar
  120. Wymelenberg AV, Gaskell J, Mozuch M, BonDurant SS, Sabat G, Ralph J, Skyba O, Mansfield SD, Blanchette RA, Grigoriev IV, Kersten PJ (2011) Significant alteration of gene expression in wood decay fungi Postia placenta and Phanerochaete chrysosporium by plant species. Appl Environ Microbiol 77(13):4499–4507CrossRefGoogle Scholar
  121. Xie F, Liu T, Qian WJ, Petyuk VA, Smith RD (2011) Liquid chromatography-mass spectrometry-based quantitative proteomics. J Biol Chem 286:25443–25449PubMedPubMedCentralCrossRefGoogle Scholar
  122. Yu GJ, Yin YL, Yu WH, Liu W, Jin YX, Shrestha A, Yang Q, Ye XD, Sun H (2015) Proteome exploration to provide a resource for the investigation of Ganoderma lucidum. PLoS One 10(3):e0119439PubMedPubMedCentralCrossRefGoogle Scholar
  123. Zargar SM, Gupta N, Mir RA, Rai V (2016) Shift from gel based to gel free proteomics to unlock unknown regulatory network in plants: a comprehensive review. J Adv Res Biotechnol 1(1):19Google Scholar
  124. Zeiner CA, Purvine SO, Zink EM, Pasa-Tolic L, Chaput DL, Haridas S, Wu S, LaButti K, Grigoriev IV, Henrissat B, Santelli CM (2016) Comparative analysis of secretome profiles of manganese (II)-oxidizing Ascomycete fungi. PLoS One 11(7):e0157844PubMedPubMedCentralCrossRefGoogle Scholar
  125. Zhang Y, Fonslow BR, Shan B, Baek MC, Yates JR III (2013) Protein analysis by shotgun/bottom-up proteomics. Chem Rev 113(4):2343–2394PubMedPubMedCentralCrossRefGoogle Scholar
  126. Zhu N, Liu J, Yang J, Lin Y, Yang Y, Ji L, Li M, Yuan H (2016) Comparative analysis of the secretomes of Schizophyllum commune and other wood-decay basidiomycetes during solid-state fermentation reveals its unique lignocellulose-degrading enzyme system. Biotechnol Biofuels 9(1):42PubMedPubMedCentralCrossRefGoogle Scholar
  127. Znameroski EA, Coradetti ST, Roche CM, Tsai JC, Iavarone AT, Cate JH, Glass NL (2012) Induction of lignocellulose-degrading enzymes in Neurospora crassa by cellodextrins. Proc Natl Acad Sci 109(16):6012–6017PubMedCrossRefPubMedCentralGoogle Scholar
  128. Zorn H, Bouws H, Takenberg M, Nimtz M, Getzlaff R, Breithaupt DE, Berger RG (2005) An extracellular carboxylesterase from the basidiomycete Pleurotus sapidus hydrolyses xanthophyll esters. Biol Chem 386(5):435–440PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Akshay Shankar
    • 1
  • Shruti Ahlawat
    • 1
  • Krishna Kant Sharma
    • 1
    Email author
  1. 1.Department of MicrobiologyMaharshi Dayanand UniversityRohtakIndia

Personalised recommendations