Comparative Analysis of Secretome Profiles of Manganese(II)-Oxidizing Ascomycete Fungi
Abstract
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 thesemore »
- Authors:
- Publication Date:
- Research Org.:
- Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division
- OSTI Identifier:
- 1346607
- Alternate Identifier(s):
- OSTI ID: 1342335
- Report Number(s):
- PNNL-SA-121069
Journal ID: ISSN 1932-6203; 10.1371/journal.pone.0157844
- Grant/Contract Number:
- AC05-76RL01830; AC02-05CH11231; EAR-1249489; CBET-1336496
- Resource Type:
- Published Article
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Name: PLoS ONE Journal Volume: 11 Journal Issue: 7; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Environmental Molecular Sciences Laboratory; fungi; fungal genomics; proteases; Ascomycetes; genome analysis; plant fungal pathogens; glycoside hydrolases; Basidiomycetes
Citation Formats
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., and Pöggeler, ed., Stefanie. Comparative Analysis of Secretome Profiles of Manganese(II)-Oxidizing Ascomycete Fungi. United States: N. p., 2016.
Web. doi:10.1371/journal.pone.0157844.
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, ed., Stefanie. Comparative Analysis of Secretome Profiles of Manganese(II)-Oxidizing Ascomycete Fungi. United States. https://doi.org/10.1371/journal.pone.0157844
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., and Pöggeler, ed., Stefanie. Tue .
"Comparative Analysis of Secretome Profiles of Manganese(II)-Oxidizing Ascomycete Fungi". United States. https://doi.org/10.1371/journal.pone.0157844.
@article{osti_1346607,
title = {Comparative Analysis of Secretome Profiles of Manganese(II)-Oxidizing Ascomycete Fungi},
author = {Zeiner, Carolyn A. and Purvine, Samuel O. and Zink, Erika M. and Paša-Tolić, Ljiljana and Chaput, Dominique L. and Haridas, Sajeet and Wu, Si and LaButti, Kurt and Grigoriev, Igor V. and Henrissat, Bernard and Santelli, Cara M. and Hansel, Colleen M. and Pöggeler, ed., Stefanie},
abstractNote = {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.},
doi = {10.1371/journal.pone.0157844},
journal = {PLoS ONE},
number = 7,
volume = 11,
place = {United States},
year = {Tue Jul 19 00:00:00 EDT 2016},
month = {Tue Jul 19 00:00:00 EDT 2016}
}
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