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Title: Functional Genomics, Transcriptomics, and Proteomics Reveal Distinct Combat Strategies Between Lineages of Wood-Degrading Fungi With Redundant Wood Decay Mechanisms

Abstract

Wood-degrading fungi vary in their strategies for deconstructing wood, and their competitive successes shape the rate and fate of carbon released from wood, Earth’s largest pool of aboveground terrestrial carbon. In this study, one-on-one interspecific interactions between two model brown rot (carbohydrate-selective) fungi, Gloeophyllum trabeum and Rhodonia (Postia) placenta, were studied on wood wafers where a clearly resolved interaction zone (IZ) could be generated, reproducibly. Comparative RNAseq and proteomics between the IZ and non-interacting hyphae of each species identified combative strategies for each fungus. Glycoside hydrolases were a relatively smaller portion of the interaction secretome compared to non-interacting hyphae. The interaction zone showed higher pectinase specific activity than all other sampling locations, and higher laminarinase specific activity (branched ß-glucan proxy) was seen in the IZ secretome relative to equivalent hyphae in single-species cultures. Our efforts also identified two distinct competitive strategies in these two fungi with a shared nutritional mode (brown rot) but polyphyletic ancestral lineages. Gloeophyllum trabeum (Gloeophyllum clade) employed secondary metabolite (SM) synthesis in response to a competitor, as shown by the upregulation of several SM-synthesizing genes in the interaction. R. placenta (Antrodia clade) instead upregulated a larger variety of uncharacterized oxidoreductases in interacting hyphae, suggesting that anmore » oxidative burst may be a response to competitors in this fungus. Both species produced several hypothetical proteins exclusively in the interaction zone, leaving abundant unknowns on the battlefield. This work supports the existence of multiple interaction strategies among brown rot fungi and highlights the functional diversity among wood decay fungi.« less

Authors:
 [1];  [2];  [3];  [2]
  1. Oregon State Univ., Corvallis, OR (United States)
  2. Univ. of Minnesota, Saint Paul, MN (United States)
  3. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Office of Biological and Ecological Research (BER); National Science Foundation (NSF)
OSTI Identifier:
1668263
Report Number(s):
PNNL-SA-152430
Journal ID: ISSN 1664-302X
Grant/Contract Number:  
AC05-76RL01830; SC0004012; SC0012742; 00039202
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 11; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; fungal interactions; secondary metabolites; brown rot; microbial ecology; wood decay basidiomycetes

Citation Formats

Presley, Gerald N., Zhang, Jiwei, Purvine, Samuel O., and Schilling, Jonathan S. Functional Genomics, Transcriptomics, and Proteomics Reveal Distinct Combat Strategies Between Lineages of Wood-Degrading Fungi With Redundant Wood Decay Mechanisms. United States: N. p., 2020. Web. doi:10.3389/fmicb.2020.01646.
Presley, Gerald N., Zhang, Jiwei, Purvine, Samuel O., & Schilling, Jonathan S. Functional Genomics, Transcriptomics, and Proteomics Reveal Distinct Combat Strategies Between Lineages of Wood-Degrading Fungi With Redundant Wood Decay Mechanisms. United States. https://doi.org/10.3389/fmicb.2020.01646
Presley, Gerald N., Zhang, Jiwei, Purvine, Samuel O., and Schilling, Jonathan S. Tue . "Functional Genomics, Transcriptomics, and Proteomics Reveal Distinct Combat Strategies Between Lineages of Wood-Degrading Fungi With Redundant Wood Decay Mechanisms". United States. https://doi.org/10.3389/fmicb.2020.01646. https://www.osti.gov/servlets/purl/1668263.
@article{osti_1668263,
title = {Functional Genomics, Transcriptomics, and Proteomics Reveal Distinct Combat Strategies Between Lineages of Wood-Degrading Fungi With Redundant Wood Decay Mechanisms},
author = {Presley, Gerald N. and Zhang, Jiwei and Purvine, Samuel O. and Schilling, Jonathan S.},
abstractNote = {Wood-degrading fungi vary in their strategies for deconstructing wood, and their competitive successes shape the rate and fate of carbon released from wood, Earth’s largest pool of aboveground terrestrial carbon. In this study, one-on-one interspecific interactions between two model brown rot (carbohydrate-selective) fungi, Gloeophyllum trabeum and Rhodonia (Postia) placenta, were studied on wood wafers where a clearly resolved interaction zone (IZ) could be generated, reproducibly. Comparative RNAseq and proteomics between the IZ and non-interacting hyphae of each species identified combative strategies for each fungus. Glycoside hydrolases were a relatively smaller portion of the interaction secretome compared to non-interacting hyphae. The interaction zone showed higher pectinase specific activity than all other sampling locations, and higher laminarinase specific activity (branched ß-glucan proxy) was seen in the IZ secretome relative to equivalent hyphae in single-species cultures. Our efforts also identified two distinct competitive strategies in these two fungi with a shared nutritional mode (brown rot) but polyphyletic ancestral lineages. Gloeophyllum trabeum (Gloeophyllum clade) employed secondary metabolite (SM) synthesis in response to a competitor, as shown by the upregulation of several SM-synthesizing genes in the interaction. R. placenta (Antrodia clade) instead upregulated a larger variety of uncharacterized oxidoreductases in interacting hyphae, suggesting that an oxidative burst may be a response to competitors in this fungus. Both species produced several hypothetical proteins exclusively in the interaction zone, leaving abundant unknowns on the battlefield. This work supports the existence of multiple interaction strategies among brown rot fungi and highlights the functional diversity among wood decay fungi.},
doi = {10.3389/fmicb.2020.01646},
journal = {Frontiers in Microbiology},
number = ,
volume = 11,
place = {United States},
year = {Tue Jul 28 00:00:00 EDT 2020},
month = {Tue Jul 28 00:00:00 EDT 2020}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Figures / Tables:

FIGURE 1 FIGURE 1: (A) Diagrammatic representation of the two culture types and sampling regime used to generate the different types of decayed wood pieces that were extracted for secretomic or transcriptomic analysis. Competition microcosms used to simulate interspecific interactions between Gloeophyllum trabeum and Rhodonia placenta in this study. Pre-inoculated wood blocksmore » for each species are used as inocula for each end of a thin aspen wafer placed across them. The two species grow together and contact in the middle of the wafer where the interaction zone and surrounding hyphae 5 mm outside of the interaction zone is sampled for protein and RNA for proteomic and transcriptomic analysis. Single species cultures were the same cultures generated in previous studies (Zhang et al., 2016, 2019; Presley et al., 2018). Gene expression data from single species cultures was adapted from Zhang et al. (2016, 2019) while proteomics data from this culture type was adapted from Presley et al. (2018). (B) Pictures of the two culture types from the top down.« less

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Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.