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

Zeiner, Carolyn A.; Purvine, Samuel O.; Zink, Erika M.; Paša-Tolić, Ljiljana; Chaput, Dominique L.; Wu, Si; Santelli, Cara M.; Hansel, Colleen M.

doi:10.1016/J.FGB.2017.06.004

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, particularly filamentous Ascomycetes, 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 in this study we use a combination of iTRAQ proteomics and extracellular enzyme activity assays to compare the protein composition of the secretomes of four manganese(II)-oxidizing Ascomycete fungi over a three-week time course. We demonstrate that the fungi exhibit striking differences in the regulation of extracellular lignocellulose-degrading 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 Alternaria alternata SRC1lrK2f and Paraconiothyrium sporulosum AP3s5-JAC2a 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. In conclusion, thismore »« less

Authors:

Zeiner, Carolyn A. ^[1]; Purvine, Samuel O. ^[2]; Zink, Erika M. ^[3]; Paša-Tolić, Ljiljana ^[2]; Chaput, Dominique L. ^[4]; Wu, Si ^[5]; Santelli, Cara M. ^[6]; Hansel, Colleen M. ^[7]

Harvard Univ., Cambridge, MA (United States). School of Engineering and Applied Sciences (SEAS)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Lab.
Smithsonian Inst., Washington, DC (United States). National Museum of Natural History, Dept. of Mineral Sciences
Univ. of Oklahoma, Norman, OK (United States). Dept. of Chemistry and Biochemistry
Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Earth Sciences
Woods Hole Oceanographic Inst., Woods Hole, MA (United States). Dept. of Marine Chemistry and Geochemistry

Publication Date:: Sat Jul 01 00:00:00 EDT 2017

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)

OSTI Identifier:: 1368406

Alternate Identifier(s):: OSTI ID: 1550384

Grant/Contract Number:: AC05-76RL01830; AC02-05CH11231; EAR-1249489; CBET-133649

Resource Type:: Accepted Manuscript

Journal Name:: Fungal Genetics and Biology

Additional Journal Information:: Journal Volume: 106; Journal Issue: C; Journal ID: ISSN 1087-1845

Publisher:: Elsevier

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; Secretome; Filamentous fungi; Ascomycota; iTRAQ; Proteomics; Carbon degradation

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.

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                    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.  https://doi.org/10.1016/J.FGB.2017.06.004

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                    Zeiner, Carolyn A., Purvine, Samuel O., Zink, Erika M., Paša-Tolić, Ljiljana, Chaput, Dominique L., Wu, Si, Santelli, Cara M., and Hansel, Colleen M. Sat .  
"Quantitative iTRAQ-based secretome analysis reveals species-specific and temporal shifts in carbon utilization strategies among manganese(II)-oxidizing Ascomycete fungi".  United States.  https://doi.org/10.1016/J.FGB.2017.06.004.  https://www.osti.gov/servlets/purl/1368406.

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@article{osti_1368406,

  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, particularly filamentous Ascomycetes, 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 in this study we use a combination of iTRAQ proteomics and extracellular enzyme activity assays to compare the protein composition of the secretomes of four manganese(II)-oxidizing Ascomycete fungi over a three-week time course. We demonstrate that the fungi exhibit striking differences in the regulation of extracellular lignocellulose-degrading 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 Alternaria alternata SRC1lrK2f and Paraconiothyrium sporulosum AP3s5-JAC2a 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. In conclusion, this work highlights the diversity of operative metabolic strategies among understudied yet ubiquitous cellulose-degrading Ascomycetes, enhancing our understanding of their contribution to 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         = {Sat Jul 01 00:00:00 EDT 2017},

  month        = {Sat Jul 01 00:00:00 EDT 2017}

}

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https://doi.org/10.1016/J.FGB.2017.06.004

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