title: 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. 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.
authors.affiliation: School of Engineering and Applied Sciences, Harvard University, Cambridge, Massachusetts, United States of America.
authors.forename: Carolyn A
authors.initials: CA
authors.lastname: Zeiner
authors.affiliation: Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America.
authors.forename: Samuel O
authors.initials: SO
authors.lastname: Purvine
authors.affiliation: Biological Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America.
authors.forename: Erika M
authors.initials: EM
authors.lastname: Zink
authors.affiliation: Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America.
authors.forename: Ljiljana
authors.initials: L
authors.lastname: Paša-Tolić
authors.affiliation: Department of Mineral Sciences, National Museum of Natural History, Smithsonian Institution, Washington, DC, United States of America.
authors.forename: Dominique L
authors.initials: DL
authors.lastname: Chaput
authors.affiliation: U.S. Department of Energy Joint Genome Institute, Walnut Creek, California, United States of America.
authors.forename: Sajeet
authors.initials: S
authors.lastname: Haridas
authors.affiliation: Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America.
authors.forename: Si
authors.initials: S
authors.lastname: Wu
authors.affiliation: U.S. Department of Energy Joint Genome Institute, Walnut Creek, California, United States of America.
authors.forename: Kurt
authors.initials: K
authors.lastname: LaButti
authors.affiliation: U.S. Department of Energy Joint Genome Institute, Walnut Creek, California, United States of America.
authors.forename: Igor V
authors.initials: IV
authors.lastname: Grigoriev
authors.affiliation: Architecture et Fonction des Macromolécules Biologiques, UMR7257, Centre National de la Recherche Scientifique and Aix-Marseille Université, 13288 Marseille Cedex 9, France.|Department of Biological Sciences, King Abdulaziz University, P.O. Box 80203, Jeddah, 21589, Saudi Arabia.
authors.forename: Bernard
authors.initials: B
authors.lastname: Henrissat
authors.affiliation: Department of Earth Sciences, University of Minnesota, Minneapolis, Minnesota, United States of America.
authors.forename: Cara M
authors.initials: CM
authors.lastname: Santelli
authors.affiliation: Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, United States of America.
authors.forename: Colleen M
authors.initials: CM
authors.lastname: Hansel
mesh_terms: D001203:Ascomycota / Q000201:enzymology*; D001673:Biodegradation, Environmental; D002244:Carbon / Q000378:metabolism; D002413:Cations, Divalent; D044602:Cellulases / Q000145:classification / Q000378:metabolism*; D019295:Computational Biology; D006026:Glycoside Hydrolases / Q000145:classification / Q000378:metabolism*; D017665:Hydroxyl Radical / Q000378:metabolism; D008031:Lignin / Q000378:metabolism*; D008345:Manganese / Q000378:metabolism*; D058977:Molecular Sequence Annotation; D010084:Oxidation-Reduction; D011096:Polygalacturonase / Q000145:classification / Q000378:metabolism*; D012988:Soil Microbiology; D013045:Species Specificity
chemical_list: D002413:Cations, Divalent; C036909:lignocellulose; D017665:Hydroxyl Radical; D008345:Manganese; D002244:Carbon; D008031:Lignin; D044602:Cellulases; D006026:Glycoside Hydrolases; C023305:hemicellulase; D011096:Polygalacturonase