A genomics-informed study of oxalate and cellulase regulation by brown rot wood-degrading fungi
Abstract
Wood-degrading fungi that selectively remove carbohydrates (brown rot) combine Fenton-based oxidation and enzymatic hydrolysis to degrade wood. These two steps are incompatible in close proximity. To explain this, brown rot fungi may stagger oxidative reactions ahead of hydrolysis, but the scale and environmental controls for such a mechanism have not been resolved in solid wood. Here, we focused on one reaction control parameter, oxalate. In coordination with Fe3+-reducing compounds (e.g., 2,5-dimethoxyhydroquinone), oxalate can either promote Fenton chemistry by mobilizing Fe3+ as mono-oxalates (facilitative) or inhibit Fenton chemistry (protective) by restricting reducibility and the formation of Fenton’s reagent as Fe3+/Fe2-(oxalate)2,3. We sectioned wood wafers colonized directionally by Postia placenta and Gloeophyllum trabeum to map end-to-end the expression of oxalate synthesis genes and to overlay enzyme activities, metabolites, and wood modifications. Near advancing hyphal fronts, oxaloacetase expression was up upregulated for both fungi, while regulation patterns of paralogous of isocitrate lyases and glyoxylate dehydrogenases varied, suggesting different physiological roles. Oxalate decarboxylase (ODC) expression in G. trabeum was induced in more decayed wood behind the hyphal front, but was constitutively expressed in all P. placenta sections. Relative ODC activities increased and oxalate levels stabilized in more decayed wood behind the hyphal front. Endoglucanasemore »
- Authors:
-
- University of Minnesota, Minneapolis, MN (United States)
- Publication Date:
- Research Org.:
- Univ. of Minnesota, Minneapolis, MN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
- OSTI Identifier:
- 1538275
- Alternate Identifier(s):
- OSTI ID: 1703838
- Grant/Contract Number:
- SC0004012; SC0012742; 00039202
- Resource Type:
- Journal Article: Accepted Manuscript
- Journal Name:
- Fungal Genetics and Biology
- Additional Journal Information:
- Journal Volume: 112; Journal Issue: C; Journal ID: ISSN 1087-1845
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Fenton; reactive oxygen species; oxalate decarboxylase; wood; lignocellulose
Citation Formats
Presley, Gerald N., Zhang, Jiwei, and Schilling, Jonathan S. A genomics-informed study of oxalate and cellulase regulation by brown rot wood-degrading fungi. United States: N. p., 2016.
Web. doi:10.1016/j.fgb.2016.08.004.
Presley, Gerald N., Zhang, Jiwei, & Schilling, Jonathan S. A genomics-informed study of oxalate and cellulase regulation by brown rot wood-degrading fungi. United States. https://doi.org/10.1016/j.fgb.2016.08.004
Presley, Gerald N., Zhang, Jiwei, and Schilling, Jonathan S. 2016.
"A genomics-informed study of oxalate and cellulase regulation by brown rot wood-degrading fungi". United States. https://doi.org/10.1016/j.fgb.2016.08.004. https://www.osti.gov/servlets/purl/1538275.
@article{osti_1538275,
title = {A genomics-informed study of oxalate and cellulase regulation by brown rot wood-degrading fungi},
author = {Presley, Gerald N. and Zhang, Jiwei and Schilling, Jonathan S.},
abstractNote = {Wood-degrading fungi that selectively remove carbohydrates (brown rot) combine Fenton-based oxidation and enzymatic hydrolysis to degrade wood. These two steps are incompatible in close proximity. To explain this, brown rot fungi may stagger oxidative reactions ahead of hydrolysis, but the scale and environmental controls for such a mechanism have not been resolved in solid wood. Here, we focused on one reaction control parameter, oxalate. In coordination with Fe3+-reducing compounds (e.g., 2,5-dimethoxyhydroquinone), oxalate can either promote Fenton chemistry by mobilizing Fe3+ as mono-oxalates (facilitative) or inhibit Fenton chemistry (protective) by restricting reducibility and the formation of Fenton’s reagent as Fe3+/Fe2-(oxalate)2,3. We sectioned wood wafers colonized directionally by Postia placenta and Gloeophyllum trabeum to map end-to-end the expression of oxalate synthesis genes and to overlay enzyme activities, metabolites, and wood modifications. Near advancing hyphal fronts, oxaloacetase expression was up upregulated for both fungi, while regulation patterns of paralogous of isocitrate lyases and glyoxylate dehydrogenases varied, suggesting different physiological roles. Oxalate decarboxylase (ODC) expression in G. trabeum was induced in more decayed wood behind the hyphal front, but was constitutively expressed in all P. placenta sections. Relative ODC activities increased and oxalate levels stabilized in more decayed wood behind the hyphal front. Endoglucanase (EG) activity, on the other hand, peaked for both fungi in later decay stages. These oxalate optimization patterns are in line with previous whole-block ‘spiking’ experiments tracking oxalate, but we provide here information on its genetic controls across a spatial gradient. As a complement, we also demonstrate in vitro the plausibility of a protective role for oxalate, to emphasize that these fungi might be optimizing oxalate at a given level to maximize Fenton reactions but to minimize oxidative damage.},
doi = {10.1016/j.fgb.2016.08.004},
url = {https://www.osti.gov/biblio/1538275},
journal = {Fungal Genetics and Biology},
issn = {1087-1845},
number = C,
volume = 112,
place = {United States},
year = {Tue Aug 16 00:00:00 EDT 2016},
month = {Tue Aug 16 00:00:00 EDT 2016}
}
Web of Science
Works referenced in this record:
Degradation of cellulose by basidiomycetous fungi
journal, May 2008
- Baldrian, Petr; Valášková, Vendula
- FEMS Microbiology Reviews, Vol. 32, Issue 3
A Mechanism for Production of Hydroxyl Radicals by the Brown-Rot Fungus Coniophora Puteana: Fe(III) Reduction by Cellobiose Dehydrogenase and Fe(II) Oxidation at a Distance from the Hyphae
journal, January 1997
- Hyde, S. M.; Wood, P. M.
- Microbiology, Vol. 143, Issue 1
Subcellular localization of glyoxylate cycle key enzymes involved in oxalate biosynthesis of wood-destroying basidiomycete Fomitopsis palustris grown on glucose
journal, June 2006
- Sakai, Shunsuke; Nishide, Tatsunori; Munir, Erman
- Microbiology, Vol. 152, Issue 6
Analysis of Character Correlations Among Wood Decay Mechanisms, Mating Systems, and Substrate Ranges in Homobasidiomycetes
journal, March 2001
- Hibbett, David S.; Donoghue, Michael J.
- Systematic Biology, Vol. 50, Issue 2
Colocalizing incipient reactions in wood degraded by the brown rot fungus Postia placenta
journal, September 2013
- Schilling, Jonathan S.; Duncan, Shona M.; Presley, Gerald N.
- International Biodeterioration & Biodegradation, Vol. 83
Biodegradative mechanism of the brown rot basidiomycete Gloeophyllum trabeum : evidence for an extracellular hydroquinone-driven fenton reaction
journal, March 1999
- Kerem, Zohar; Jensen, Kenneth A.; Hammel, Kenneth E.
- FEBS Letters, Vol. 446, Issue 1
Investigating oxalate biosynthesis in the wood-decaying fungus Gloeophyllum trabeum using 13C metabolic flux analysis
journal, January 2015
- Zhuang, Liangpeng; Guo, Weihua; Yoshida, Makoto
- RSC Advances, Vol. 5, Issue 126
Purification and Characterization of Isocitrate Lyase from the Wood-Destroying Basidiomycete Fomitopsis palustris Grown on Glucose
journal, March 2002
- Munir, Erman; Hattori, Takefumi; Shimada, Mikio
- Archives of Biochemistry and Biophysics, Vol. 399, Issue 2
The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes
journal, June 2012
- Floudas, Dimitrios; Binder, Manfred; Riley, Robert
- Science, Vol. 336, Issue 6089
Proteomic and Functional Analysis of the Cellulase System Expressed by Postia placenta during Brown Rot of Solid Wood
journal, September 2011
- Ryu, Jae San; Shary, Semarjit; Houtman, Carl J.
- Applied and Environmental Microbiology, Vol. 77, Issue 22
Possible biochemical roles of oxalic acid as a low molecular weight compound involved in brown-rot and white-rot wood decays
journal, March 1997
- Shimada, Mikio; Akamtsu, Yasumi; Tokimatsu, Toshiaki
- Journal of Biotechnology, Vol. 53, Issue 2-3
Analyzing real-time PCR data by the comparative CT method
journal, June 2008
- Schmittgen, Thomas D.; Livak, Kenneth J.
- Nature Protocols, Vol. 3, Issue 6
Effect of pH and Oxalate on Hydroquinone-Derived Hydroxyl Radical Formation during Brown Rot Wood Degradation
journal, October 2003
- Varela, E.; Tien, M.
- Applied and Environmental Microbiology, Vol. 69, Issue 10
Evidence for cleavage of lignin by a brown rot basidiomycete
journal, July 2008
- Yelle, Daniel J.; Ralph, John; Lu, Fachuang
- Environmental Microbiology, Vol. 10, Issue 7
Oxalate-Metabolising Genes of the White-Rot Fungus Dichomitus squalens Are Differentially Induced on Wood and at High Proton Concentration
journal, February 2014
- Mäkelä, Miia R.; Sietiö, Outi-Maaria; de Vries, Ronald P.
- PLoS ONE, Vol. 9, Issue 2
Gene Expression Analysis of Copper Tolerance and Wood Decay in the Brown Rot Fungus Fibroporia radiculosa
journal, December 2012
- Tang, Juliet D.; Parker, Leslie A.; Perkins, Andy D.
- Applied and Environmental Microbiology, Vol. 79, Issue 5
Oxalate regulation by two brown rot fungi decaying oxalate-amended and non-amended wood
journal, November 2005
- Schilling, Jonathan S.; Jellison, Jody
- Holzforschung, Vol. 59, Issue 6
A physiological role for oxalic acid biosynthesis in the wood-rotting basidiomycete Fomitopsis palustris
journal, September 2001
- Munir, E.; Yoon, J. J.; Tokimatsu, T.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 20
SignalP 4.0: discriminating signal peptides from transmembrane regions
journal, September 2011
- Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar
- Nature Methods, Vol. 8, Issue 10
Significant levels of extracellular reactive oxygen species produced by brown rot basidiomycetes on cellulose
journal, October 2002
- Cohen, Roni; Jensen, Kenneth A.; Houtman, Carl J.
- FEBS Letters, Vol. 531, Issue 3
Spatial mapping of extracellular oxidant production by a white rot basidiomycete on wood reveals details of ligninolytic mechanism: Mapping of fungal oxidant production on wood
journal, December 2012
- Hunt, Christopher G.; Houtman, Carl J.; Jones, Don C.
- Environmental Microbiology, Vol. 15, Issue 3
Signature Wood Modifications Reveal Decomposer Community History
journal, March 2015
- Schilling, Jonathan S.; Kaffenberger, Justin T.; Liew, Feng Jin
- PLOS ONE, Vol. 10, Issue 3
Laccase and Its Role in Production of Extracellular Reactive Oxygen Species during Wood Decay by the Brown Rot Basidiomycete Postia placenta
journal, February 2010
- Wei, D.; Houtman, C. J.; Kapich, A. N.
- Applied and Environmental Microbiology, Vol. 76, Issue 7
Detection and Quantification of Oxalic Acid from the Brown-Rot Decay Fungus, Postia placenta
journal, January 1996
- Jordan, C. R.; Dashek, W. V.; Highley, T. L.
- hfsg, Vol. 50, Issue 4
Lignin demethylation and polysaccharide decomposition in spruce sapwood degraded by brown rot fungi
journal, February 2002
- Filley, T. R.; Cody, G. D.; Goodell, B.
- Organic Geochemistry, Vol. 33, Issue 2
Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion
journal, February 2009
- Martinez, Diego; Challacombe, Jean; Morgenstern, Ingo
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 6
De Novo Synthesis of 4,5-Dimethoxycatechol and 2,5-Dimethoxyhydroquinone by the Brown Rot FungusGloeophyllum trabeum
journal, February 1999
- Paszczynski, Andrzej; Crawford, Ronald; Funk, David
- Applied and Environmental Microbiology, Vol. 65, Issue 2
New role for glyoxylate cycle enzymes in wood-rotting basidiomycetes in relation to biosynthesis of oxalic acid
journal, October 2001
- Munir, Erman; Yoon, Jeong-Jun; Tokimatsu, Toshiaki
- Journal of Wood Science, Vol. 47, Issue 5
A metabolic role of the glyoxylate and tricarboxylic acid cycles for development of the copper-tolerant brown-rot fungusFomitopsis palustris
journal, November 2002
- Yoon, Jeong-Jun; Hattori, Takefumi; Shimada, Mikio
- FEMS Microbiology Letters, Vol. 217, Issue 1
Measurement of cellulase activities
journal, January 1987
- Ghose, T. K.
- Pure and Applied Chemistry, Vol. 59, Issue 2
Comparison of wood decay among diverse lignicolous fungi
journal, March 1997
- Worrall, James J.; Anagnost, Susan E.; Zabel, Robert A.
- Mycologia, Vol. 89, Issue 2
Purification and characterization of oxalate decarboxylase from Coriolus versicolor
journal, March 1994
- Dutton, Martin V.; Kathiara, Mona; Gallagher, Imelda M.
- FEMS Microbiology Letters, Vol. 116, Issue 3
Wood Decay by Brown-Rot Fungi: Changes in Pore Structure and Cell Wall Volume
journal, January 1991
- Flournoy, Douglas S.; Kirk, T. Kent; Highley, T. L.
- Holzforschung, Vol. 45, Issue 5
Fungal hydroquinones contribute to brown rot of wood
journal, December 2006
- Suzuki, Melissa R.; Hunt, Christopher G.; Houtman, Carl J.
- Environmental Microbiology, Vol. 8, Issue 12
A biopulping mechanism: Creation of acid groups on fiber
journal, July 2004
- Hunt, C.; Kenealy, W.; Horn, E.
- Holzforschung, Vol. 58, Issue 4
Localization and induction of oxalate decarboxylase in the brown-rot wood decay fungus Postia placenta
journal, January 1997
- Micales, Jessie A.
- International Biodeterioration & Biodegradation, Vol. 39, Issue 2-3
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
Metal Accumulation without Enhanced Oxalate Secretion in Wood Degraded by Brown Rot Fungi
journal, August 2006
- Schilling, J. S.; Jellison, J.
- Applied and Environmental Microbiology, Vol. 72, Issue 8
An accurate normalization strategy for RT-qPCR in Hypocrea jecorina (Trichoderma reesei)
journal, January 2010
- Steiger, Matthias G.; Mach, Robert L.; Mach-Aigner, Astrid R.
- Journal of Biotechnology, Vol. 145, Issue 1