Comparative Analysis of Secretome Profiles of Manganese(II)-Oxidizing Ascomycete Fungi

Zeiner, Carolyn A.; Purvine, Samuel O.; Zink, Erika M.; Paša-Tolić, Ljiljana; Chaput, Dominique L.; Haridas, Sajeet; Wu, Si; LaButti, Kurt; Grigoriev, Igor V.; Henrissat, Bernard; Santelli, Cara M.; Hansel, Colleen M.; Pöggeler, Stefanie

doi:10.1371/journal.pone.0157844

Title: Comparative Analysis of Secretome Profiles of Manganese(II)-Oxidizing Ascomycete Fungi

Journal Article · 18 July 2016 · PLoS ONE

DOI: https://doi.org/10.1371/journal.pone.0157844 · OSTI ID:1342335

Zeiner, Carolyn A. ^[1]; Purvine, Samuel O. ^[2]; Zink, Erika M. ^[2]; Paša-Tolić, Ljiljana ^[2]; Chaput, Dominique L. ^[3]; Haridas, Sajeet ^[4]; Wu, Si ^[5]; LaButti, Kurt ^[4]; Grigoriev, Igor V. ^[4]; Henrissat, Bernard ^[6]; Santelli, Cara M. ^[7]; Hansel, Colleen M. ^[8]; Pöggeler, Stefanie ^[9]

Boston Univ., MA (United States); Harvard Univ., Cambridge, MA (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Smithsonian Inst., Washington, DC (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Univ. of Oklahoma, Norman, OK (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Centre National de la Recherche Scientifique and Aix-Marseille Univ., Marseille Cedex (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
Univ. of Minnesota, Minneapolis, MN (United States)
Woods Hole Oceanographic Institution, Woods Hole, MA (United States)
Georg-August-Univ. of Göttingen Inst. of Microbiology & Genetics (Germany)

Fungal secretomes contain a wide range of hydrolytic and oxidative enzymes, including cellulases, hemicellulases, pectinases, and lignin-degrading accessory enzymes, that synergistically drive litter decomposition in the environment. While secretome studies of model organisms such as Phanerochaete chrysosporium and Aspergillus species have greatly expanded our knowledge of these enzymes, few have extended secretome characterization to environmental isolates or conducted side-by-side comparisons of diverse species. Thus, the mechanisms of carbon degradation by many ubiquitous soil fungi remain poorly understood. Here we use a combination of LC-MS/MS, genomic, and bioinformatic analyses to characterize and compare the protein composition of the secretomes of four recently isolated, cosmopolitan, Mn(II)-oxidizing Ascomycetes (Alternaria alternata SRC1lrK2f, Stagonospora sp. SRC1lsM3a, Pyrenochaeta sp. DS3sAY3a, and Paraconiothyrium sporulosum AP3s5-JAC2a). We demonstrate that the organisms produce a rich yet functionally similar suite of extracellular enzymes, with species-specific differences in secretome composition arising from unique amino acid sequences rather than overall protein function. Furthermore, we identify not only a wide range of carbohydrate-active enzymes that can directly oxidize recalcitrant carbon, but also an impressive suite of redox-active accessory enzymes that suggests a role for Fenton-based hydroxyl radical formation in indirect, non-specific lignocellulose attack. Furthermore, our findings highlight the diverse oxidative capacity of these environmental isolates and enhance our understanding of the role of filamentous Ascomycetes in carbon turnover in the environment.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Pacific Northwest National Lab. (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); National Science Foundation; USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Scientific User Facilities Division

Grant/Contract Number:: AC05-76RL01830; AC02-05CH11231

OSTI ID:: 1342335

Alternate ID(s):: OSTI ID: 1346607

Report Number(s):: PNNL-SA--121069; 48100; KP1704020

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 7 Vol. 11; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (105)

Manganese(II) oxidation by manganese peroxidase from the basidiomycete Phanerochaete chrysosporium. Kinetic mechanism and role of chelators. Wariishi, H.; Valli, K.; Gold, M. H. Journal of Biological Chemistry, Vol. 267, Issue 33 https://doi.org/10.1016/S0021-9258(18)35893-9	journal	November 1992
Pathways for Extracellular Fenton Chemistry in the Brown Rot Basidiomycete Gloeophyllum trabeum Jensen, K. A.; Houtman, C. J.; Ryan, Z. C. Applied and Environmental Microbiology, Vol. 67, Issue 6 https://doi.org/10.1128/AEM.67.6.2705-2711.2001	journal	June 2001
Diversity of the exoproteome of Fusarium graminearum grown on plant cell wall Phalip, Vincent; Delalande, François; Carapito, Christine Current Genetics, Vol. 48, Issue 6 https://doi.org/10.1007/s00294-005-0040-3	journal	November 2005
MycoCosm portal: gearing up for 1000 fungal genomes Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1183	journal	December 2013
Chemically Etched Open Tubular and Monolithic Emitters for Nanoelectrospray Ionization Mass Spectrometry Kelly, Ryan T.; Page, Jason S.; Luo, Quanzhou Analytical Chemistry, Vol. 78, Issue 22, p. 7796-7801 https://doi.org/10.1021/ac061133r	journal	November 2006
Compositions of fungal secretomes indicate a greater impact of phylogenetic history than lifestyle adaptation Krijger, Jorrit-Jan; Thon, Michael R.; Deising, Holger B. BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-722	journal	January 2014
The carbon starvation response of Aspergillus niger during submerged cultivation: Insights from the transcriptome and secretome Nitsche, Benjamin M.; Jørgensen, Thomas R.; Akeroyd, Michiel BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-380	journal	January 2012
Genome-scale model reconstruction of the methylotrophic yeast Ogataea polymorpha Liebal, Ulf Winfried; Fabry, Brigida A.; Ravikrishnan, Aarthi RWTH Aachen University https://doi.org/10.18154/rwth-2021-02761	text	January 2021
Abbau und Umsetzung von lignifiziertem Pflanzenmaterial durch mikroskopische Bodenpilze Haider, K.; Domsch, K. H. Archiv f�r Mikrobiologie, Vol. 64, Issue 4 https://doi.org/10.1007/bf00417015	journal	January 1969
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen Krogh, Anders; Larsson, Björn; von Heijne, Gunnar Journal of Molecular Biology, Vol. 305, Issue 3 https://doi.org/10.1006/jmbi.2000.4315	journal	January 2001
Predicting Subcellular Localization of Proteins Based on their N-terminal Amino Acid Sequence Emanuelsson, Olof; Nielsen, Henrik; Brunak, Søren Journal of Molecular Biology, Vol. 300, Issue 4 https://doi.org/10.1006/jmbi.2000.3903	journal	July 2000
Promotion of Mn(II) Oxidation and Remediation of Coal Mine Drainage in Passive Treatment Systems by Diverse Fungal and Bacterial Communities Santelli, C. M.; Pfister, D. H.; Lazarus, D. Applied and Environmental Microbiology, Vol. 76, Issue 14 https://doi.org/10.1128/aem.03029-09	journal	May 2010
Mn(II) oxidation is the principal function of the extracellular Mn-peroxidase from Phanerochaete chrysosporium Glenn, Jeffrey K.; Akileswaran, Lakshmi; Gold, Michael H. Archives of Biochemistry and Biophysics, Vol. 251, Issue 2, p. 688-696 https://doi.org/10.1016/0003-9861(86)90378-4	journal	December 1986
Subtilases: The superfamily of subtilisin-like serine proteases Siezen, Roland J.; Leunissen, Jack A. M. Protein Science, Vol. 6, Issue 3 https://doi.org/10.1002/pro.5560060301	journal	March 1997
Microbial degradation of lignin: how a bulky recalcitrant polymer is efficiently recycled in nature and how we can take advantage of this Ruiz-Dueñas, Francisco J.; Martínez, Ángel T. Microbial Biotechnology, Vol. 2, Issue 2 https://doi.org/10.1111/j.1751-7915.2008.00078.x	journal	March 2009
Alternaria as a major allergen for asthma in children raised in a desert environment. Halonen, M.; Stern, D. A.; Wright, A. L. American Journal of Respiratory and Critical Care Medicine, Vol. 155, Issue 4 https://doi.org/10.1164/ajrccm.155.4.9105079	journal	April 1997
Proteomic analysis of rutin-induced secreted proteins from Aspergillus flavus Medina, Martha L.; Kiernan, Urban A.; Francisco, Wilson A. Fungal Genetics and Biology, Vol. 41, Issue 3 https://doi.org/10.1016/j.fgb.2003.11.014	journal	March 2004
Secretome diversity and quantitative analysis of cellulolytic Aspergillus fumigatus Z5 in the presence of different carbon sources Liu, Dongyang; Li, Juan; Zhao, Shuang Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-149	journal	January 2013
Copper radical oxidases and related extracellular oxidoreductases of wood-decay Agaricomycetes Kersten, Phil; Cullen, Dan Fungal Genetics and Biology, Vol. 72 https://doi.org/10.1016/j.fgb.2014.05.011	journal	November 2014
Microbial Communities Promoting Mn(II) Oxidation in Ashumet Pond, a Historically Polluted Freshwater Pond Undergoing Remediation Santelli, Cara M.; Chaput, Dominique L.; Hansel, Colleen M. Taylor & Francis https://doi.org/10.6084/m9.figshare.978003	text	January 2014
Comparative Transcriptome and Secretome Analysis of Wood Decay Fungi Postia placenta and Phanerochaete chrysosporium Vanden Wymelenberg, A.; Gaskell, J.; Mozuch, M. Applied and Environmental Microbiology, Vol. 76, Issue 11 https://doi.org/10.1128/aem.00058-10	journal	April 2010
Predicting Subcellular Localization of Proteins Based on their N-terminal Amino Acid Sequence Emanuelsson, Olof; Nielsen, Henrik; Brunak, Søren Journal of Molecular Biology, Vol. 300, Issue 4 https://doi.org/10.1006/jmbi.2000.3903	journal	July 2000
MEROPS : the database of proteolytic enzymes, their substrates and inhibitors Rawlings, Neil D.; Waller, Matthew; Barrett, Alan J. Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt953	journal	October 2013
Promotion of Mn(II) Oxidation and Remediation of Coal Mine Drainage in Passive Treatment Systems by Diverse Fungal and Bacterial Communities Santelli, C. M.; Pfister, D. H.; Lazarus, D. Applied and Environmental Microbiology, Vol. 76, Issue 14 https://doi.org/10.1128/Aem.03029-09	journal	May 2010
Comparative Transcriptome and Secretome Analysis of Wood Decay Fungi Postia placenta and Phanerochaete chrysosporium Vanden Wymelenberg, A.; Gaskell, J.; Mozuch, M. Applied and Environmental Microbiology, Vol. 76, Issue 11 https://doi.org/10.1128/AEM.00058-10	journal	April 2010
Copper radical oxidases and related extracellular oxidoreductases of wood-decay Agaricomycetes Kersten, Phil; Cullen, Dan Fungal Genetics and Biology, Vol. 72 https://doi.org/10.1016/j.fgb.2014.05.011	journal	November 2014
Fungi associated with necrotic apical parts of Fraxinus excelsior shoots Przybyl, K. Forest Pathology, Vol. 32, Issue 6 https://doi.org/10.1046/j.1439-0329.2002.00301.x	journal	December 2002
Chemically Etched Open Tubular and Monolithic Emitters for Nanoelectrospray Ionization Mass Spectrometry Kelly, Ryan T.; Page, Jason S.; Luo, Quanzhou Analytical Chemistry, Vol. 78, Issue 22, p. 7796-7801 https://doi.org/10.1021/ac061133r	journal	November 2006
Pathways for Extracellular Fenton Chemistry in the Brown Rot Basidiomycete Gloeophyllum trabeum Jensen, K. A.; Houtman, C. J.; Ryan, Z. C. Applied and Environmental Microbiology, Vol. 67, Issue 6 https://doi.org/10.1128/aem.67.6.2705-2711.2001	journal	June 2001
Stagonospora nodorum: cause of stagonospora nodorum blotch of wheat Solomon, Peter S.; Lowe, Rohan G. T.; Tan, Kar-Chun Molecular Plant Pathology, Vol. 7, Issue 3 https://doi.org/10.1111/j.1364-3703.2006.00326.x	journal	May 2006
The Ecology of Fungi on Plant Remains Above the soil Hudson, H. J. New Phytologist, Vol. 67, Issue 4 https://doi.org/10.1111/j.1469-8137.1968.tb06399.x	journal	October 1968
Novel enzymatic oxidation of Mn ²⁺ to Mn ³⁺ catalyzed by a fungal laccase Höfer, Christine; Schlosser, Dietmar FEBS Letters, Vol. 451, Issue 2 https://doi.org/10.1016/S0014-5793(99)00566-9	journal	May 1999
Fungi associated with necrotic apical parts of Fraxinus excelsior shoots Przybyl, K. Forest Pathology, Vol. 32, Issue 6 https://doi.org/10.1046/j.1439-0329.2002.00301.x	journal	December 2002
Alternaria as a major allergen for asthma in children raised in a desert environment. Halonen, M.; Stern, D. A.; Wright, A. L. American Journal of Respiratory and Critical Care Medicine, Vol. 155, Issue 4 https://doi.org/10.1164/ajrccm.155.4.9105079	journal	April 1997
New Pyrenochaeta Species Causing Keratitis Ferrer, C.; Perez-Santonja, J. J.; Rodriguez, A. E. Journal of Clinical Microbiology, Vol. 47, Issue 5 https://doi.org/10.1128/JCM.01912-08	journal	March 2009
Association of Mutations in a Lysosomal Protein with Classical Late-Infantile Neuronal Ceroid Lipofuscinosis Sleat, D. E. Science, Vol. 277, Issue 5333 https://doi.org/10.1126/science.277.5333.1802	journal	September 1997
Locating proteins in the cell using TargetP, SignalP and related tools Emanuelsson, Olof; Brunak, Søren; von Heijne, Gunnar Nature Protocols, Vol. 2, Issue 4 https://doi.org/10.1038/nprot.2007.131	journal	April 2007
Locating proteins in the cell using TargetP, SignalP and related tools Emanuelsson, Olof; Brunak, Søren; von Heijne, Gunnar Nature Protocols, Vol. 2, Issue 4 https://doi.org/10.1038/nprot.2007.131	journal	April 2007
Secretomes: The fungal strike force Girard, Vincent; Dieryckx, Cindy; Job, Claudette PROTEOMICS, Vol. 13, Issue 3-4 https://doi.org/10.1002/pmic.201200282	journal	January 2013
OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes Li, L. Genome Research, Vol. 13, Issue 9 https://doi.org/10.1101/gr.1224503	journal	September 2003
MS-GF+ makes progress towards a universal database search tool for proteomics Kim, Sangtae; Pevzner, Pavel A. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6277	journal	October 2014
The intra- and extracellular proteome of Aspergillus niger growing on defined medium with xylose or maltose as carbon substrate Lu, Xin; Sun, Jibin; Nimtz, Manfred Microbial Cell Factories, Vol. 9, Issue 1 https://doi.org/10.1186/1475-2859-9-23	journal	January 2010
Microbial Communities Promoting Mn(II) Oxidation in Ashumet Pond, a Historically Polluted Freshwater Pond Undergoing Remediation Santelli, Cara M.; Chaput, Dominique L.; Hansel, Colleen M. Figshare https://doi.org/10.6084/m9.figshare.c.1944170.v1	collection	January 2015
Purification and characterization of a 1,2,4-trihydroxybenzene 1,2-dioxygenase from the basidiomycete Phanerochaete chrysosporium. Rieble, S.; Joshi, D. K.; Gold, M. H. Journal of Bacteriology, Vol. 176, Issue 16 https://doi.org/10.1128/jb.176.16.4838-4844.1994	journal	August 1994
A time course analysis of the extracellular proteome of Aspergillus nidulans growing on sorghum stover Saykhedkar, Sayali; Ray, Anamika; Ayoubi-Canaan, Patricia Biotechnology for Biofuels, Vol. 5, Issue 1 https://doi.org/10.1186/1754-6834-5-52	journal	January 2012
Biological Control of Sclerotinia pseudotuberosa and Other Fungi During Moist Storage of Quercus robur Seeds Finch-Savage, W. E.; Clay, H. A.; Budge, S. P. European Journal of Plant Pathology, Vol. 109, Issue 6, p. 615-624 https://doi.org/10.1023/A:1024784831972	journal	January 2003
A time course analysis of the extracellular proteome of Aspergillus nidulans growing on sorghum stover Saykhedkar, Sayali; Ray, Anamika; Ayoubi-Canaan, Patricia Biotechnology for Biofuels, Vol. 5, Issue 1 https://doi.org/10.1186/1754-6834-5-52	journal	January 2012
SignalP 4.0: discriminating signal peptides from transmembrane regions Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar Nature Methods, Vol. 8, Issue 10 https://doi.org/10.1038/nmeth.1701	journal	September 2011
Glyoxal Oxidase from Phanerochaete chrysosporium Is a New Radical-Copper Oxidase Whittaker, Mei M.; Kersten, Philip J.; Nakamura, Nobuhumi Journal of Biological Chemistry, Vol. 271, Issue 2 https://doi.org/10.1074/jbc.271.2.681	journal	January 1996
Reversed-phase chromatography with multiple fraction concatenation strategy for proteome profiling of human MCF10A cells Wang, Yuexi; Yang, Feng; Gritsenko, Marina A. PROTEOMICS, Vol. 11, Issue 10 https://doi.org/10.1002/pmic.201000722	journal	April 2011
The carbohydrate-active enzymes database (CAZy) in 2013 Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1178	journal	November 2013
Purification and characterization of a 1,2,4-trihydroxybenzene 1,2-dioxygenase from the basidiomycete Phanerochaete chrysosporium. Rieble, S.; Joshi, D. K.; Gold, M. H. Journal of Bacteriology, Vol. 176, Issue 16 https://doi.org/10.1128/jb.176.16.4838-4844.1994	journal	August 1994
Measurement of protein using bicinchoninic acid Smith, P. K.; Krohn, R. I.; Hermanson, G. T. Analytical Biochemistry, Vol. 150, Issue 1 https://doi.org/10.1016/0003-2697(85)90442-7	journal	October 1985
Target-Decoy Search Strategy for Mass Spectrometry-Based Proteomics Elias, Joshua E.; Gygi, Steven P. Methods in Molecular Biology https://doi.org/10.1007/978-1-60761-444-9_5	book	December 2009
Pleosporales Zhang, Ying; Crous, Pedro W.; Schoch, Conrad L. Fungal Diversity, Vol. 53, Issue 1 https://doi.org/10.1007/s13225-011-0117-x	journal	October 2011
Interrelating Different Types of Genomic Data, from Proteome to Secretome: 'Oming in on Function Greenbaum, Dov; Luscombe, Nicholas M.; Jansen, Ronald Genome Research, Vol. 11, Issue 9 https://doi.org/10.1101/gr.207401	journal	September 2001
Biotreatment of pulp mill bleachery effluents with the coelomycetous fungusStagonospora gigaspora Bergbauer, Matthias; Eggert, Claudia; Kalnowski, G�nther Biotechnology Letters, Vol. 14, Issue 4 https://doi.org/10.1007/BF01022331	journal	April 1992
SignalP 4.0: discriminating signal peptides from transmembrane regions Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar Nature Methods, Vol. 8, Issue 10 https://doi.org/10.1038/nmeth.1701	journal	September 2011
Biodegradation and biological treatments of cellulose, hemicellulose and lignin: an overview Pérez, J.; Muñoz-Dorado, J.; de la Rubia, T. International Microbiology, Vol. 5, Issue 2 https://doi.org/10.1007/s10123-002-0062-3	journal	April 2002
Structural and enzymatic properties of the sedolisin family of serine-carboxyl peptidases. Wlodawer, Alexander; Li, Mi; Gustchina, Alla Acta Biochimica Polonica, Vol. 50, Issue 1 https://doi.org/10.18388/abp.2003_3716	journal	March 2003
A critical review of cellobiose dehydrogenases Henriksson, Gunnar; Johansson, Gunnar; Pettersson, Göran Journal of Biotechnology, Vol. 78, Issue 2 https://doi.org/10.1016/S0168-1656(00)00206-6	journal	March 2000
Proteomic and transcriptional analyses of Arthrobotrys oligospora cell wall related proteins reveal complexity of fungal virulence against nematodes Liang, Lianming; Wu, Heng; Liu, Zhiheng Applied Microbiology and Biotechnology, Vol. 97, Issue 19 https://doi.org/10.1007/s00253-013-5178-1	journal	August 2013
Comparative Bacterial Proteomics: Analysis of the Core Genome Concept Callister, Stephen J.; McCue, Lee Ann; Turse, Joshua E. PLoS ONE, Vol. 3, Issue 2 https://doi.org/10.1371/journal.pone.0001542	journal	February 2008
A First Insight into Pycnoporus sanguineus BAFC 2126 Transcriptome Rohr, Cristian O.; Levin, Laura N.; Mentaberry, Alejandro N. PLoS ONE, Vol. 8, Issue 12 https://doi.org/10.1371/journal.pone.0081033	journal	December 2013
Secretome diversity and quantitative analysis of cellulolytic Aspergillus fumigatus Z5 in the presence of different carbon sources Liu, Dongyang; Li, Juan; Zhao, Shuang Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-149	journal	January 2013
Promotion of Mn(II) Oxidation and Remediation of Coal Mine Drainage in Passive Treatment Systems by Diverse Fungal and Bacterial Communities Santelli, C. M.; Pfister, D. H.; Lazarus, D. Applied and Environmental Microbiology, Vol. 76, Issue 14 https://doi.org/10.1128/AEM.03029-09	journal	May 2010
Fungal laccases – occurrence and properties Baldrian, Petr FEMS Microbiology Reviews, Vol. 30, Issue 2 https://doi.org/10.1111/J.1574-4976.2005.00010.X	journal	March 2006
A critical review of cellobiose dehydrogenases Henriksson, Gunnar; Johansson, Gunnar; Pettersson, Göran Journal of Biotechnology, Vol. 78, Issue 2 https://doi.org/10.1016/s0168-1656(00)00206-6	journal	March 2000
Biodegradation and biological treatments of cellulose, hemicellulose and lignin: an overview Pérez, J.; Muñoz-Dorado, J.; de la Rubia, T. International Microbiology, Vol. 5, Issue 2 https://doi.org/10.1007/s10123-002-0062-3	journal	April 2002
DeconMSn: a software tool for accurate parent ion monoisotopic mass determination for tandem mass spectra Mayampurath, A. M.; Jaitly, N.; Purvine, S. O. Bioinformatics, Vol. 24, Issue 7 https://doi.org/10.1093/bioinformatics/btn063	journal	February 2008
High-quality draft assemblies of mammalian genomes from massively parallel sequence data Gnerre, S.; MacCallum, I.; Przybylski, D. Proceedings of the National Academy of Sciences, Vol. 108, Issue 4 https://doi.org/10.1073/pnas.1017351108	journal	December 2010
DeconMSn: a software tool for accurate parent ion monoisotopic mass determination for tandem mass spectra Mayampurath, A. M.; Jaitly, N.; Purvine, S. O. Bioinformatics, Vol. 24, Issue 7 https://doi.org/10.1093/bioinformatics/btn063	journal	February 2008
Microbial degradation of lignin: how a bulky recalcitrant polymer is efficiently recycled in nature and how we can take advantage of this Ruiz-Dueñas, Francisco J.; Martínez, Ángel T. Microbial Biotechnology, Vol. 2, Issue 2 https://doi.org/10.1111/j.1751-7915.2008.00078.x	journal	March 2009
Defining manganese(II) removal processes in passive coal mine drainage treatment systems through laboratory incubation experiments Luan, Fubo; Santelli, Cara M.; Hansel, Colleen M. Applied Geochemistry, Vol. 27, Issue 8 https://doi.org/10.1016/j.apgeochem.2012.03.010	journal	August 2012
A First Insight into Pycnoporus sanguineus BAFC 2126 Transcriptome Rohr, Cristian O.; Levin, Laura N.; Mentaberry, Alejandro N. PLoS ONE, Vol. 8, Issue 12 https://doi.org/10.1371/journal.pone.0081033	journal	December 2013
Association of Mutations in a Lysosomal Protein with Classical Late-Infantile Neuronal Ceroid Lipofuscinosis Sleat, D. E. Science, Vol. 277, Issue 5333 https://doi.org/10.1126/science.277.5333.1802	journal	September 1997
Self-made frits for nanoscale columns in proteomics Maiolica, Alessio; Borsotti, Dario; Rappsilber, Juri PROTEOMICS, Vol. 5, Issue 15 https://doi.org/10.1002/pmic.200402010	journal	October 2005
Manganese(II) oxidation by manganese peroxidase from the basidiomycete Phanerochaete chrysosporium. Kinetic mechanism and role of chelators. Wariishi, H.; Valli, K.; Gold, M. H. Journal of Biological Chemistry, Vol. 267, Issue 33 https://doi.org/10.1016/s0021-9258(18)35893-9	journal	November 1992
Mn(II) oxidation is the principal function of the extracellular Mn-peroxidase from Phanerochaete chrysosporium Glenn, Jeffrey K.; Akileswaran, Lakshmi; Gold, Michael H. Archives of Biochemistry and Biophysics, Vol. 251, Issue 2, p. 688-696 https://doi.org/10.1016/0003-9861(86)90378-4	journal	December 1986
Measurement of protein using bicinchoninic acid Smith, P. K.; Krohn, R. I.; Hermanson, G. T. Analytical Biochemistry, Vol. 150, Issue 1 https://doi.org/10.1016/0003-2697(85)90442-7	journal	October 1985
The carbon starvation response of Aspergillus niger during submerged cultivation: Insights from the transcriptome and secretome Nitsche, Benjamin M.; Jørgensen, Thomas R.; Akeroyd, Michiel BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-380	journal	January 2012
A Proteomic View on Genome-Based Signal Peptide Predictions Antelmann, H. Genome Research, Vol. 11, Issue 9 https://doi.org/10.1101/gr.182801	journal	September 2001
Target-Decoy Search Strategy for Mass Spectrometry-Based Proteomics Elias, Joshua E.; Gygi, Steven P. Methods in Molecular Biology https://doi.org/10.1007/978-1-60761-444-9_5	book	December 2009
Comparative Proteomics Profile of Lipid-Cumulating Oleaginous Yeast: An iTRAQ-Coupled 2-D LC-MS/MS Analysis Shi, Jiahua; Feng, Huixing; Lee, Jaslyn PLoS ONE, Vol. 8, Issue 12 https://doi.org/10.1371/journal.pone.0085532	journal	December 2013
Self-made frits for nanoscale columns in proteomics Maiolica, Alessio; Borsotti, Dario; Rappsilber, Juri PROTEOMICS, Vol. 5, Issue 15 https://doi.org/10.1002/pmic.200402010	journal	October 2005
High-quality draft assemblies of mammalian genomes from massively parallel sequence data Gnerre, S.; MacCallum, I.; Przybylski, D. Proceedings of the National Academy of Sciences, Vol. 108, Issue 4 https://doi.org/10.1073/pnas.1017351108	journal	December 2010
Development of Quantitative Proteomics Using iTRAQ Based on the Immunological Response of Galleria mellonella Larvae Challenged with Fusarium oxysporum Microconidia Muñoz-Gómez, Amalia; Corredor, Mauricio; Benítez-Páez, Alfonso PLoS ONE, Vol. 9, Issue 11 https://doi.org/10.1371/journal.pone.0112179	journal	November 2014
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 Hori, Chiaki; Gaskell, Jill; Igarashi, Kiyohiko Applied and Environmental Microbiology, Vol. 80, Issue 7 https://doi.org/10.1128/aem.03652-13	journal	January 2014
Secretomes: The fungal strike force Girard, Vincent; Dieryckx, Cindy; Job, Claudette PROTEOMICS, Vol. 13, Issue 3-4 https://doi.org/10.1002/pmic.201200282	journal	January 2013
The intra- and extracellular proteome of Aspergillus niger growing on defined medium with xylose or maltose as carbon substrate Lu, Xin; Sun, Jibin; Nimtz, Manfred Microbial Cell Factories, Vol. 9, Issue 1 https://doi.org/10.1186/1475-2859-9-23	journal	January 2010
Diversity of the exoproteome of Fusarium graminearum grown on plant cell wall Phalip, Vincent; Delalande, François; Carapito, Christine Current Genetics, Vol. 48, Issue 6 https://doi.org/10.1007/s00294-005-0040-3	journal	November 2005
Quantitative iTRAQ Secretome Analysis of Aspergillus niger Reveals Novel Hydrolytic Enzymes Adav, Sunil S.; Li, An A.; Manavalan, Arulmani Journal of Proteome Research, Vol. 9, Issue 8 https://doi.org/10.1021/pr100148j	journal	August 2010
OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes Li, L. Genome Research, Vol. 13, Issue 9 https://doi.org/10.1101/gr.1224503	journal	September 2003
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 Hori, Chiaki; Gaskell, Jill; Igarashi, Kiyohiko Applied and Environmental Microbiology, Vol. 80, Issue 7 https://doi.org/10.1128/AEM.03652-13	journal	January 2014
A Proteomic View on Genome-Based Signal Peptide Predictions Antelmann, H. Genome Research, Vol. 11, Issue 9 https://doi.org/10.1101/gr.182801	journal	September 2001
Proteomic and transcriptional analyses of Arthrobotrys oligospora cell wall related proteins reveal complexity of fungal virulence against nematodes Liang, Lianming; Wu, Heng; Liu, Zhiheng Applied Microbiology and Biotechnology, Vol. 97, Issue 19 https://doi.org/10.1007/s00253-013-5178-1	journal	August 2013
Quantitative iTRAQ Secretome Analysis of Aspergillus niger Reveals Novel Hydrolytic Enzymes Adav, Sunil S.; Li, An A.; Manavalan, Arulmani Journal of Proteome Research, Vol. 9, Issue 8 https://doi.org/10.1021/pr100148j	journal	August 2010
Fungal laccases – occurrence and properties Baldrian, Petr FEMS Microbiology Reviews, Vol. 30, Issue 2 https://doi.org/10.1111/j.1574-4976.2005.00010.x	journal	March 2006
Comparative Bacterial Proteomics: Analysis of the Core Genome Concept Callister, Stephen J.; McCue, Lee Ann; Turse, Joshua E. PLoS ONE, Vol. 3, Issue 2 https://doi.org/10.1371/journal.pone.0001542	journal	February 2008
Microbial Communities Promoting Mn(II) Oxidation in Ashumet Pond, a Historically Polluted Freshwater Pond Undergoing Remediation Santelli, Cara M.; Chaput, Dominique L.; Hansel, Colleen M. Geomicrobiology Journal, Vol. 31, Issue 7 https://doi.org/10.1080/01490451.2013.875605	journal	July 2014
MycoCosm portal: gearing up for 1000 fungal genomes Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1183	journal	December 2013
Compositions of fungal secretomes indicate a greater impact of phylogenetic history than lifestyle adaptation Krijger, Jorrit-Jan; Thon, Michael R.; Deising, Holger B. BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-722	journal	January 2014
Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes Levasseur, Anthony; Drula, Elodie; Lombard, Vincent Biotechnology for Biofuels, Vol. 6, Issue 1, Article No. 41 https://doi.org/10.1186/1754-6834-6-41	journal	January 2013
Laccase-Catalyzed Oxidation of Mn2+ in the Presence of Natural Mn3+ Chelators as a Novel Source of Extracellular H2O2 Production and Its Impact on Manganese Peroxidase Schlosser, D.; Hofer, C. Applied and Environmental Microbiology, Vol. 68, Issue 7 https://doi.org/10.1128/AEM.68.7.3514-3521.2002	journal	July 2002
Fungal laccases – occurrence and properties Baldrian, Petr FEMS Microbiology Reviews, Vol. 30, Issue 2 https://doi.org/10.1111/j.1574-4976.2005.00010.x	journal	March 2006

Cited By (10)

Terrestrial and marine Antarctic fungi extracts active against Xanthomonas citri subsp. citri Vieira, G.; Purić, J.; Morão, L. G. Letters in Applied Microbiology, Vol. 67, Issue 1 https://doi.org/10.1111/lam.12890	journal	May 2018
Genome-scale data resolve ancestral rock-inhabiting lifestyle in Dothideomycetes (Ascomycota) Ametrano, Claudio G.; Grewe, Felix; Crous, Pedro W. IMA Fungus, Vol. 10, Issue 1 https://doi.org/10.1186/s43008-019-0018-2	journal	October 2019
Oxygen isotope analysis of bacterial and fungal manganese oxidation Sutherland, K. M.; Wankel, S. D.; Hansel, C. M. Geobiology, Vol. 16, Issue 4 https://doi.org/10.1111/gbi.12288	journal	April 2018
A new promising phylogenetic marker to study the diversity of fungal communities: The Glycoside Hydrolase 63 gene Pérez-Izquierdo, L.; Morin, E.; Maurice, J. P. Molecular Ecology Resources, Vol. 17, Issue 6 https://doi.org/10.1111/1755-0998.12678	journal	May 2017
Proteomic enzyme analysis of the marine fungus Paradendryphiella salina reveals alginate lyase as a minimal adaptation strategy for brown algae degradation Pilgaard, Bo; Wilkens, Casper; Herbst, Florian-Alexander Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-48823-9	journal	August 2019
Evaluation of Unconventional Protein Secretion by Saccharomyces cerevisiae and other Fungi Miura, Natsuko; Ueda, Mitsuyoshi Cells, Vol. 7, Issue 9 https://doi.org/10.3390/cells7090128	journal	August 2018
101 Dothideomycetes genomes: A test case for predicting lifestyles and emergence of pathogens Haridas, S.; Albert, R.; Binder, M. Studies in Mycology, Vol. 96 https://doi.org/10.1016/j.simyco.2020.01.003	journal	June 2020
Evaluation of Unconventional Protein Secretion by Saccharomyces cerevisiae and other Fungi Miura, Natsuko; Ueda, Mitsuyoshi Cells, Vol. 7, Issue 9 https://doi.org/10.3390/cells7090128	journal	August 2018
Proteomic enzyme analysis of the marine fungus Paradendryphiella salina reveals alginate lyase as a minimal adaptation strategy for brown algae degradation Pilgaard, Bo; Wilkens, Casper; Herbst, Florian-Alexander Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-48823-9	journal	August 2019
Transcriptomics Analysis of the Chinese Pear Pathotype of Alternaria alternata Gives Insights into Novel Mechanisms of HSAF Antifungal Activities He, Feng; Li, Bingxin; Ai, Gan International Journal of Molecular Sciences, Vol. 19, Issue 7 https://doi.org/10.3390/ijms19071841	journal	June 2018

Similar Records

Quantitative iTRAQ-based secretome analysis reveals species-specific and temporal shifts in carbon utilization strategies among manganese(II)-oxidizing Ascomycete fungi

Journal Article · 2017 · Fungal Genetics and Biology · OSTI ID:1406789

Zeiner, Carolyn A.; Purvine, Samuel O.; Zink, Erika M.; +5 more

Mechanisms of Manganese(II) Oxidation by Filamentous Ascomycete Fungi Vary with Species and Time as a Function of Secretome Composition

Journal Article · 2021 · Frontiers in Microbiology · OSTI ID:1781657

Zeiner, Carolyn A.; Purvine, Samuel O.; Zink, Erika M.; +5 more

Quantitative iTRAQ-based secretome analysis reveals species-specific and temporal shifts in carbon utilization strategies among manganese(II)-oxidizing Ascomycete fungi

Journal Article · 2017 · Fungal Genetics and Biology · OSTI ID:1368406

Zeiner, Carolyn A.; Purvine, Samuel O.; Zink, Erika M.; +5 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Environmental Molecular Sciences Laboratory
fungi
fungal genomics
proteases
Ascomycetes
genome analysis
plant fungal pathogens
glycoside hydrolases
Basidiomycetes

Title: Comparative Analysis of Secretome Profiles of Manganese(II)-Oxidizing Ascomycete Fungi

Citation Formats

References (105)

Cited By (10)

Similar Records

Related Subjects