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 »
- Authors:
-
- Oregon State Univ., Corvallis, OR (United States)
- Univ. of Minnesota, Saint Paul, MN (United States)
- 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}
}
Figures / Tables:
Works referenced in this record:
Changes in oxidative enzyme activity during interspecific mycelial interactions involving the white-rot fungus Trametes versicolor
journal, June 2010
- Hiscox, Jennifer; Baldrian, Petr; Rogers, Hilary J.
- Fungal Genetics and Biology, Vol. 47, Issue 6
Functions of fungal melanin beyond virulence
journal, March 2017
- Cordero, Radames J. B.; Casadevall, Arturo
- Fungal Biology Reviews, Vol. 31, Issue 2
Fungal peptide synthetases: an update on functions and specificity signatures
journal, August 2013
- Kalb, Daniel; Lackner, Gerald; Hoffmeister, Dirk
- Fungal Biology Reviews, Vol. 27, Issue 2
Interspecific combative interactions between wood-decaying basidiomycetes
journal, March 2000
- Boddy, Lynne
- FEMS Microbiology Ecology, Vol. 31, Issue 3
Localizing gene regulation reveals a staggered wood decay mechanism for the brown rot fungus Postia placenta
journal, September 2016
- Zhang, Jiwei; Presley, Gerald N.; Hammel, Kenneth E.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 39
Microarray analysis of differential gene expression elicited in Trametes versicolor during interspecific mycelial interactions
journal, August 2010
- Eyre, Catherine; Muftah, Wafa; Hiscox, Jennifer
- Fungal Biology, Vol. 114, Issue 8
DeconMSn: a software tool for accurate parent ion monoisotopic mass determination for tandem mass spectra
journal, February 2008
- Mayampurath, A. M.; Jaitly, N.; Purvine, S. O.
- Bioinformatics, Vol. 24, Issue 7
Biochemistry and molecular biology of exocellular fungal β-(1,3)- and β-(1,6)-glucanases
journal, March 2007
- Martin, Kirstee; McDougall, Barbara M.; McIlroy, Simon
- FEMS Microbiology Reviews, Vol. 31, Issue 2
Secondary Fungal Metabolites and Their Biological Activities, III. Further Metabolites from Dual Cultures of the Antagonistic Basidiomycetes Heterobasidion annosum and Gloeophyllum abietinum
journal, January 1993
- Sonnenbichler, Johann; Peipp, Heinrich; Dietrich, Jürgen
- Biological Chemistry Hoppe-Seyler, Vol. 374, Issue 7-12
SignalP 5.0 improves signal peptide predictions using deep neural networks
journal, February 2019
- Almagro Armenteros, José Juan; Tsirigos, Konstantinos D.; Sønderby, Casper Kaae
- Nature Biotechnology, Vol. 37, Issue 4
Evolutionary dynamics of host specialization in wood-decay fungi
journal, August 2018
- Krah, Franz-Sebastian; Bässler, Claus; Heibl, Christoph
- BMC Evolutionary Biology, Vol. 18, Issue 1
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks
journal, March 2012
- Trapnell, Cole; Roberts, Adam; Goff, Loyal
- Nature Protocols, Vol. 7, Issue 3
Gene Regulation Shifts Shed Light on Fungal Adaption in Plant Biomass Decomposers
journal, November 2019
- Zhang, Jiwei; Silverstein, Kevin A. T.; Castaño, Jesus David
- mBio, Vol. 10, Issue 6
Measurement of cellulase activities
journal, January 1987
- Ghose, T. K.
- Pure and Applied Chemistry, Vol. 59, Issue 2
Distinct Growth and Secretome Strategies for Two Taxonomically Divergent Brown Rot Fungi
journal, January 2017
- Presley, Gerald N.; Schilling, Jonathan S.
- Applied and Environmental Microbiology, Vol. 83, Issue 7
Specificity of Bacillus thuringiensis Delta-Endotoxin
journal, January 1987
- Jaquet, Françoise; Hütter, Ralf; Lüthy, Peter
- Applied and Environmental Microbiology, Vol. 53, Issue 3
Differential Gene Expression in Pycnoporus coccineus during Interspecific Mycelial Interactions with Different Competitors
journal, August 2013
- Arfi, Yonathan; Levasseur, Anthony; Record, Eric
- Applied and Environmental Microbiology, Vol. 79, Issue 21
Measurement of protein using bicinchoninic acid
journal, October 1985
- Smith, P. K.; Krohn, R. I.; Hermanson, G. T.
- Analytical Biochemistry, Vol. 150, Issue 1
Armed and dangerous – Chemical warfare in wood decay communities
journal, September 2017
- Hiscox, Jennifer; Boddy, Lynne
- Fungal Biology Reviews, Vol. 31, Issue 4
Mushroom Hunting by Using Bioinformatics: Application of a Predictive Framework Facilitates the Selective Identification of Sesquiterpene Synthases in Basidiomycota
journal, October 2013
- Quin, Maureen B.; Flynn, Christopher M.; Wawrzyn, Grayson T.
- ChemBioChem, Vol. 14, Issue 18
Multiple Multi-Copper Oxidase Gene Families in Basidiomycetes – What for?
journal, April 2011
- Kues, Ursula; Ruhl, Martin
- Current Genomics, Vol. 12, Issue 2
Functional differentiation of chitinases in the white-rot fungus Phanerochaete chrysosporium
journal, August 2016
- Karlsson, Magnus; Stenlid, Jan; Lindahl, Björn
- Fungal Ecology, Vol. 22
Multi-genome analysis identifies functional and phylogenetic diversity of basidiomycete adenylate-forming reductases
journal, March 2018
- Brandenburger, Eileen; Braga, Daniel; Kombrink, Anja
- Fungal Genetics and Biology, Vol. 112
Production and effects of volatile organic compounds during interspecific interactions
journal, April 2016
- El Ariebi, Nawal; Hiscox, Jennifer; Scriven, Sarah A.
- Fungal Ecology, Vol. 20
Secondary metabolites from a Gloeophyllum species
journal, June 2000
- Rasser, Falk; Anke, Timm; Sterner, Olov
- Phytochemistry, Vol. 54, Issue 5
Gloeophyllins A–J, Cytotoxic Ergosteroids with Various Skeletons from a Chinese Tibet Fungus Gloeophyllum abietinum
journal, April 2015
- Han, Jun-Jie; Bao, Li; Tao, Qiao-Qiao
- Organic Letters, Vol. 17, Issue 10
Discovery of novel xylosides in co-culture of basidiomycetes Trametes versicolor and Ganoderma applanatum by integrated metabolomics and bioinformatics
journal, September 2016
- Yao, Lu; Zhu, Li-Ping; Xu, Xiao-Yan
- Scientific Reports, Vol. 6, Issue 1
Changes in volatile production during interspecific interactions between four wood rotting fungi growing in artificial media
journal, May 2008
- Evans, Jennifer A.; Eyre, Catherine A.; Rogers, Hilary J.
- Fungal Ecology, Vol. 1, Issue 2-3
Antagonistic fungal interactions influence carbon dioxide evolution from decomposing wood
journal, April 2015
- Hiscox, Jennifer; Savoury, Melanie; Vaughan, Ian P.
- Fungal Ecology, Vol. 14
Emergent properties arising from spatial heterogeneity influence fungal community dynamics
journal, June 2018
- O'Leary, Jade; Eastwood, Dan; Müller, Carsten
- Fungal Ecology, Vol. 33
Changes in Volatile Production During the Course of Fungal Mycelial Interactions Between Hypholoma fasciculare and Resinicium bicolor
journal, December 2006
- Hynes, Juliet; Müller, Carsten T.; Jones, T. Hefin
- Journal of Chemical Ecology, Vol. 33, Issue 1
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen
journal, January 2001
- Krogh, Anders; Larsson, Björn; von Heijne, Gunnar
- Journal of Molecular Biology, Vol. 305, Issue 3
Characterization of the Sclerotinia sclerotiorum cell wall proteome: Cell wall characteristics of S. sclerotiorum
journal, April 2016
- Liu, Longzhou; Free, Stephen J.
- Molecular Plant Pathology, Vol. 17, Issue 6
Genome mining reveals the evolutionary origin and biosynthetic potential of basidiomycete polyketide synthases
journal, December 2012
- Lackner, Gerald; Misiek, Mathias; Braesel, Jana
- Fungal Genetics and Biology, Vol. 49, Issue 12
Metabolite profiles of interacting mycelial fronts differ for pairings of the wood decay basidiomycete fungus, Stereum hirsutum with its competitors Coprinus micaceus and Coprinus disseminatus
journal, December 2007
- Peiris, Diluka; Dunn, Warwick B.; Brown, Marie
- Metabolomics, Vol. 4, Issue 1
Draft Genome of Omphalotus olearius Provides a Predictive Framework for Sesquiterpenoid Natural Product Biosynthesis in Basidiomycota
journal, June 2012
- Wawrzyn, Grayson T.; Quin, Maureen B.; Choudhary, Swati
- Chemistry & Biology, Vol. 19, Issue 6
Increase of laccase activity during interspecific interactions of white-rot fungi
journal, November 2004
- Baldrian, Petr
- FEMS Microbiology Ecology, Vol. 50, Issue 3
The whiff of decay: Linking volatile production and extracellular enzymes to outcomes of fungal interactions at different temperatures
journal, June 2019
- O'Leary, Jade; Hiscox, Jen; Eastwood, Dan C.
- Fungal Ecology, Vol. 39
Interdependence of Primary Metabolism and Xenobiotic Mitigation Characterizes the Proteome of Bjerkandera adusta during Wood Decomposition
journal, November 2017
- Moody, S. C.; Dudley, E.; Hiscox, J.
- Applied and Environmental Microbiology, Vol. 84, Issue 2
Fungal community dynamics in relation to substrate quality of decaying Norway spruce (Picea abies [L.] Karst.) logs in boreal forests
journal, April 2012
- Rajala, Tiina; Peltoniemi, Mikko; Pennanen, Taina
- FEMS Microbiology Ecology, Vol. 81, Issue 2
Secondary Fungal Metabolites and Their Biological Activities, V. Investigations Concerning the Induction of the Biosynthesis of Toxic Secondary Metabolites in Basidiomycetes
journal, January 1994
- Sonnenbichler, Johann; Dietrich, Jürgen; Peipp, Heinrich
- Biological Chemistry Hoppe-Seyler, Vol. 375, Issue 1
An efficient algorithm for large-scale detection of protein families
journal, April 2002
- Enright, A. J.
- Nucleic Acids Research, Vol. 30, Issue 7
Saprotrophic basidiomycete mycelia and their interspecific interactions affect the spatial distribution of extracellular enzymes in soil: Saprotrophic basidiomycetes affect soil enzyme distribution
journal, May 2011
- Šnajdr, Jaroslav; Dobiášová, Petra; Větrovský, Tomáš
- FEMS Microbiology Ecology, Vol. 78, Issue 1
Peroxide accumulation and cell death in filamentous fungi induced by contact with a contestant
journal, February 2005
- Silar, Philippe
- Mycological Research, Vol. 109, Issue 2
antiSMASH 3.0—a comprehensive resource for the genome mining of biosynthetic gene clusters
journal, May 2015
- Weber, Tilmann; Blin, Kai; Duddela, Srikanth
- Nucleic Acids Research, Vol. 43, Issue W1
Biosynthesis of oosponol and oospoglycol elucidated by 13C NMR
journal, January 1997
- Sonnenbichler, Johann; Sonnenbichler, Isolde; Schwarz, Dorothea
- Phytochemistry, Vol. 44, Issue 2
UniProt: a hub for protein information
journal, October 2014
- Consortium, UniPot
- Nucleic Acids Research, Vol. 43, Issue D1, p. D204-D212
Fungal chitinases: function, regulation, and potential roles in plant/pathogen interactions
journal, November 2015
- Langner, Thorsten; Göhre, Vera
- Current Genetics, Vol. 62, Issue 2
MycoCosm portal: gearing up for 1000 fungal genomes
journal, December 2013
- Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet
- Nucleic Acids Research, Vol. 42, Issue D1
Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi
journal, June 2014
- Riley, Robert; Salamov, Asaf A.; Brown, Daren W.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 27
MS-GF+ makes progress towards a universal database search tool for proteomics
journal, October 2014
- Kim, Sangtae; Pevzner, Pavel A.
- Nature Communications, Vol. 5, Issue 1
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