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

Abstract

Fungi generate a wide range of extracellular hydrolytic and oxidative enzymes and reactive metabolites, collectively known as the secretome, that synergistically drive plant litter decomposition in the environment. While secretome studies of model organisms have greatly expanded our knowledge of these enzymes, few have extended secretome characterization to environmental isolates or directly compared temporal patterns of enzyme utilization among diverse species. Thus, the mechanisms of carbon (C) degradation by many ubiquitous soil fungi remain poorly understood. Here we use a combination of iTRAQ proteomics and custom bioinformatic analyses to compare the protein composition of the secretomes of four manganese(II)-oxidizing Ascomycete fungi over a three-week time course. We demonstrate that although the fungi produce a similar suite of extracellular enzymes, they exhibit striking differences in the regulation of these enzymes among species and over time, revealing species-specific and temporal shifts in C utilization strategies as they degrade the same substrate. Specifically, our findings suggest that Paraconiothyrium sporulosum AP3s5-JAC2a and Alternaria alternata SRC1lrK2f employ sequential enzyme secretion patterns concomitant with decreasing resource availability, Stagonospora sp. SRC1lsM3a preferentially degrades proteinaceous substrate before switching to carbohydrates, and Pyrenochaeta sp. DS3sAY3a utilizes primarily peptidases to aggressively attack carbon sources in a concentrated burst. This workmore » highlights the diversity of operative metabolic strategies among cellulose-degrading Ascomycetes and enhances our understanding of their role in C turnover in the environment.« less

Authors:
; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1406789
Report Number(s):
PNNL-SA-122328
Journal ID: ISSN 1087-1845; 48100; KP1704020
DOE Contract Number:
AC05-76RL01830
Resource Type:
Journal Article
Resource Relation:
Journal Name: Fungal Genetics and Biology; Journal Volume: 106; Journal Issue: C
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; secretome.; filamentous fungi; Ascomycota; iTRAQ; proteomics; carbon degradation; lignocellulose; Environmental Molecular Sciences Laboratory

Citation Formats

Zeiner, Carolyn A., Purvine, Samuel O., Zink, Erika M., Paša-Tolić, Ljiljana, Chaput, Dominique L., Wu, Si, Santelli, Cara M., and Hansel, Colleen M.. Quantitative iTRAQ-based secretome analysis reveals species-specific and temporal shifts in carbon utilization strategies among manganese(II)-oxidizing Ascomycete fungi. United States: N. p., 2017. Web. doi:10.1016/j.fgb.2017.06.004.
Zeiner, Carolyn A., Purvine, Samuel O., Zink, Erika M., Paša-Tolić, Ljiljana, Chaput, Dominique L., Wu, Si, Santelli, Cara M., & Hansel, Colleen M.. Quantitative iTRAQ-based secretome analysis reveals species-specific and temporal shifts in carbon utilization strategies among manganese(II)-oxidizing Ascomycete fungi. United States. doi:10.1016/j.fgb.2017.06.004.
Zeiner, Carolyn A., Purvine, Samuel O., Zink, Erika M., Paša-Tolić, Ljiljana, Chaput, Dominique L., Wu, Si, Santelli, Cara M., and Hansel, Colleen M.. Fri . "Quantitative iTRAQ-based secretome analysis reveals species-specific and temporal shifts in carbon utilization strategies among manganese(II)-oxidizing Ascomycete fungi". United States. doi:10.1016/j.fgb.2017.06.004.
@article{osti_1406789,
title = {Quantitative iTRAQ-based secretome analysis reveals species-specific and temporal shifts in carbon utilization strategies among 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 Wu, Si and Santelli, Cara M. and Hansel, Colleen M.},
abstractNote = {Fungi generate a wide range of extracellular hydrolytic and oxidative enzymes and reactive metabolites, collectively known as the secretome, that synergistically drive plant litter decomposition in the environment. While secretome studies of model organisms have greatly expanded our knowledge of these enzymes, few have extended secretome characterization to environmental isolates or directly compared temporal patterns of enzyme utilization among diverse species. Thus, the mechanisms of carbon (C) degradation by many ubiquitous soil fungi remain poorly understood. Here we use a combination of iTRAQ proteomics and custom bioinformatic analyses to compare the protein composition of the secretomes of four manganese(II)-oxidizing Ascomycete fungi over a three-week time course. We demonstrate that although the fungi produce a similar suite of extracellular enzymes, they exhibit striking differences in the regulation of these enzymes among species and over time, revealing species-specific and temporal shifts in C utilization strategies as they degrade the same substrate. Specifically, our findings suggest that Paraconiothyrium sporulosum AP3s5-JAC2a and Alternaria alternata SRC1lrK2f employ sequential enzyme secretion patterns concomitant with decreasing resource availability, Stagonospora sp. SRC1lsM3a preferentially degrades proteinaceous substrate before switching to carbohydrates, and Pyrenochaeta sp. DS3sAY3a utilizes primarily peptidases to aggressively attack carbon sources in a concentrated burst. This work highlights the diversity of operative metabolic strategies among cellulose-degrading Ascomycetes and enhances our understanding of their role in C turnover in the environment.},
doi = {10.1016/j.fgb.2017.06.004},
journal = {Fungal Genetics and Biology},
number = C,
volume = 106,
place = {United States},
year = {Fri Sep 01 00:00:00 EDT 2017},
month = {Fri Sep 01 00:00:00 EDT 2017}
}