A genomics-informed study of oxalate and cellulase regulation by brown rot wood-degrading fungi

Presley, Gerald N.; Zhang, Jiwei; Schilling, Jonathan S.

doi:10.1016/j.fgb.2016.08.004

A genomics-informed study of oxalate and cellulase regulation by brown rot wood-degrading fungi

Journal Article · Tue Aug 16 00:00:00 EDT 2016 · Fungal Genetics and Biology

DOI:https://doi.org/10.1016/j.fgb.2016.08.004· OSTI ID:1538275

Presley, Gerald N. ^[1]; Zhang, Jiwei ^[2]; Schilling, Jonathan S. ^[2]

University of Minnesota, Minneapolis, MN (United States); DOE/OSTI
University of Minnesota, Minneapolis, MN (United States)

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.

View Accepted Manuscript (DOE)

Research Organization:: University of Minnesota, Minneapolis, MN (United States)

Sponsoring Organization:: National Science Foundation (NSF); USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0004012; SC0012742

OSTI ID:: 1538275

Alternate ID(s):: OSTI ID: 1703838

Journal Information:: Fungal Genetics and Biology, Journal Name: Fungal Genetics and Biology Journal Issue: C Vol. 112; ISSN 1087-1845

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (39)

Purification and Characterization of Isocitrate Lyase from the Wood-Destroying Basidiomycete Fomitopsis palustris Grown on Glucose Munir, Erman; Hattori, Takefumi; Shimada, Mikio Archives of Biochemistry and Biophysics, Vol. 399, Issue 2 https://doi.org/10.1006/abbi.2002.2770	journal	March 2002
New role for glyoxylate cycle enzymes in wood-rotting basidiomycetes in relation to biosynthesis of oxalic acid Munir, Erman; Yoon, Jeong-Jun; Tokimatsu, Toshiaki Journal of Wood Science, Vol. 47, Issue 5 https://doi.org/10.1007/BF00766787	journal	October 2001
Significant levels of extracellular reactive oxygen species produced by brown rot basidiomycetes on cellulose Cohen, Roni; Jensen, Kenneth A.; Houtman, Carl J. FEBS Letters, Vol. 531, Issue 3 https://doi.org/10.1016/S0014-5793(02)03589-5	journal	October 2002
Biodegradative mechanism of the brown rot basidiomycete Gloeophyllum trabeum : evidence for an extracellular hydroquinone-driven fenton reaction Kerem, Zohar; Jensen, Kenneth A.; Hammel, Kenneth E. FEBS Letters, Vol. 446, Issue 1 https://doi.org/10.1016/S0014-5793(99)00180-5	journal	March 1999
Lignin demethylation and polysaccharide decomposition in spruce sapwood degraded by brown rot fungi Filley, T. R.; Cody, G. D.; Goodell, B. Organic Geochemistry, Vol. 33, Issue 2 https://doi.org/10.1016/S0146-6380(01)00144-9	journal	February 2002
Possible biochemical roles of oxalic acid as a low molecular weight compound involved in brown-rot and white-rot wood decays Shimada, Mikio; Akamtsu, Yasumi; Tokimatsu, Toshiaki Journal of Biotechnology, Vol. 53, Issue 2-3 https://doi.org/10.1016/S0168-1656(97)01679-9	journal	March 1997
Localization and induction of oxalate decarboxylase in the brown-rot wood decay fungus Postia placenta Micales, Jessie A. International Biodeterioration & Biodegradation, Vol. 39, Issue 2-3 https://doi.org/10.1016/S0964-8305(97)00009-7	journal	January 1997
Colocalizing incipient reactions in wood degraded by the brown rot fungus Postia placenta Schilling, Jonathan S.; Duncan, Shona M.; Presley, Gerald N. International Biodeterioration & Biodegradation, Vol. 83 https://doi.org/10.1016/j.ibiod.2013.04.006	journal	September 2013
An accurate normalization strategy for RT-qPCR in Hypocrea jecorina (Trichoderma reesei) Steiger, Matthias G.; Mach, Robert L.; Mach-Aigner, Astrid R. Journal of Biotechnology, Vol. 145, Issue 1 https://doi.org/10.1016/j.jbiotec.2009.10.012	journal	January 2010
SignalP 4.0: discriminating signal peptides from transmembrane regions Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar Nature Methods, Vol. 8, Issue 10 https://doi.org/10.1038/nmeth.1701	journal	September 2011
Analyzing real-time PCR data by the comparative CT method Schmittgen, Thomas D.; Livak, Kenneth J. Nature Protocols, Vol. 3, Issue 6 https://doi.org/10.1038/nprot.2008.73	journal	June 2008
Investigating oxalate biosynthesis in the wood-decaying fungus Gloeophyllum trabeum using ¹³C metabolic flux analysis Zhuang, Liangpeng; Guo, Weihua; Yoshida, Makoto RSC Advances, Vol. 5, Issue 126 https://doi.org/10.1039/C5RA19203J	journal	January 2015
Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion Martinez, Diego; Challacombe, Jean; Morgenstern, Ingo Proceedings of the National Academy of Sciences, Vol. 106, Issue 6 https://doi.org/10.1073/pnas.0809575106	journal	February 2009
Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi Riley, Robert; Salamov, Asaf A.; Brown, Daren W. Proceedings of the National Academy of Sciences, Vol. 111, Issue 27 https://doi.org/10.1073/pnas.1400592111	journal	June 2014
A physiological role for oxalic acid biosynthesis in the wood-rotting basidiomycete Fomitopsis palustris Munir, E.; Yoon, J. J.; Tokimatsu, T. Proceedings of the National Academy of Sciences, Vol. 98, Issue 20 https://doi.org/10.1073/pnas.191389598	journal	September 2001
Comparison of wood decay among diverse lignicolous fungi Worrall, James J.; Anagnost, Susan E.; Zabel, Robert A. Mycologia, Vol. 89, Issue 2 https://doi.org/10.1080/00275514.1997.12026772	journal	March 1997
Analysis of Character Correlations Among Wood Decay Mechanisms, Mating Systems, and Substrate Ranges in Homobasidiomycetes Hibbett, David S.; Donoghue, Michael J. Systematic Biology, Vol. 50, Issue 2 https://doi.org/10.1080/10635150151125879	journal	March 2001
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 Hyde, S. M.; Wood, P. M. Microbiology, Vol. 143, Issue 1 https://doi.org/10.1099/00221287-143-1-259	journal	January 1997
Subcellular localization of glyoxylate cycle key enzymes involved in oxalate biosynthesis of wood-destroying basidiomycete Fomitopsis palustris grown on glucose Sakai, Shunsuke; Nishide, Tatsunori; Munir, Erman Microbiology, Vol. 152, Issue 6 https://doi.org/10.1099/mic.0.28702-0	journal	June 2006
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 Hunt, Christopher G.; Houtman, Carl J.; Jones, Don C. Environmental Microbiology, Vol. 15, Issue 3 https://doi.org/10.1111/1462-2920.12039	journal	December 2012
Fungal hydroquinones contribute to brown rot of wood Suzuki, Melissa R.; Hunt, Christopher G.; Houtman, Carl J. Environmental Microbiology, Vol. 8, Issue 12 https://doi.org/10.1111/j.1462-2920.2006.01160.x	journal	December 2006
Evidence for cleavage of lignin by a brown rot basidiomycete Yelle, Daniel J.; Ralph, John; Lu, Fachuang Environmental Microbiology, Vol. 10, Issue 7 https://doi.org/10.1111/j.1462-2920.2008.01605.x	journal	July 2008
Purification and characterization of oxalate decarboxylase from Coriolus versicolor Dutton, Martin V.; Kathiara, Mona; Gallagher, Imelda M. FEMS Microbiology Letters, Vol. 116, Issue 3 https://doi.org/10.1111/j.1574-6968.1994.tb06722.x	journal	March 1994
A metabolic role of the glyoxylate and tricarboxylic acid cycles for development of the copper-tolerant brown-rot fungusFomitopsis palustris Yoon, Jeong-Jun; Hattori, Takefumi; Shimada, Mikio FEMS Microbiology Letters, Vol. 217, Issue 1 https://doi.org/10.1111/j.1574-6968.2002.tb11449.x	journal	November 2002
Degradation of cellulose by basidiomycetous fungi Baldrian, Petr; Valášková, Vendula FEMS Microbiology Reviews, Vol. 32, Issue 3 https://doi.org/10.1111/j.1574-6976.2008.00106.x	journal	May 2008
The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes Floudas, Dimitrios; Binder, Manfred; Riley, Robert Science, Vol. 336, Issue 6089 https://doi.org/10.1126/science.1221748	journal	June 2012
Metal Accumulation without Enhanced Oxalate Secretion in Wood Degraded by Brown Rot Fungi Schilling, J. S.; Jellison, J. Applied and Environmental Microbiology, Vol. 72, Issue 8 https://doi.org/10.1128/AEM.00281-06	journal	August 2006
Gene Expression Analysis of Copper Tolerance and Wood Decay in the Brown Rot Fungus Fibroporia radiculosa Tang, Juliet D.; Parker, Leslie A.; Perkins, Andy D. Applied and Environmental Microbiology, Vol. 79, Issue 5 https://doi.org/10.1128/AEM.02916-12	journal	December 2012
Laccase and Its Role in Production of Extracellular Reactive Oxygen Species during Wood Decay by the Brown Rot Basidiomycete Postia placenta Wei, D.; Houtman, C. J.; Kapich, A. N. Applied and Environmental Microbiology, Vol. 76, Issue 7 https://doi.org/10.1128/AEM.02929-09	journal	February 2010
Proteomic and Functional Analysis of the Cellulase System Expressed by Postia placenta during Brown Rot of Solid Wood Ryu, Jae San; Shary, Semarjit; Houtman, Carl J. Applied and Environmental Microbiology, Vol. 77, Issue 22 https://doi.org/10.1128/AEM.05496-11	journal	September 2011
De Novo Synthesis of 4,5-Dimethoxycatechol and 2,5-Dimethoxyhydroquinone by the Brown Rot FungusGloeophyllum trabeum Paszczynski, Andrzej; Crawford, Ronald; Funk, David Applied and Environmental Microbiology, Vol. 65, Issue 2 https://doi.org/10.1128/AEM.65.2.674-679.1999	journal	February 1999
Effect of pH and Oxalate on Hydroquinone-Derived Hydroxyl Radical Formation during Brown Rot Wood Degradation Varela, E.; Tien, M. Applied and Environmental Microbiology, Vol. 69, Issue 10 https://doi.org/10.1128/AEM.69.10.6025-6031.2003	journal	October 2003
Measurement of cellulase activities Ghose, T. K. Pure and Applied Chemistry, Vol. 59, Issue 2 https://doi.org/10.1351/pac198759020257	journal	January 1987
Oxalate-Metabolising Genes of the White-Rot Fungus Dichomitus squalens Are Differentially Induced on Wood and at High Proton Concentration Mäkelä, Miia R.; Sietiö, Outi-Maaria; de Vries, Ronald P. PLoS ONE, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pone.0087959	journal	February 2014
Signature Wood Modifications Reveal Decomposer Community History Schilling, Jonathan S.; Kaffenberger, Justin T.; Liew, Feng Jin PLOS ONE, Vol. 10, Issue 3 https://doi.org/10.1371/journal.pone.0120679	journal	March 2015
A biopulping mechanism: Creation of acid groups on fiber Hunt, C.; Kenealy, W.; Horn, E. Holzforschung, Vol. 58, Issue 4 https://doi.org/10.1515/HF.2004.066	journal	July 2004
Oxalate regulation by two brown rot fungi decaying oxalate-amended and non-amended wood Schilling, Jonathan S.; Jellison, Jody Holzforschung, Vol. 59, Issue 6 https://doi.org/10.1515/HF.2005.109	journal	November 2005
Wood Decay by Brown-Rot Fungi: Changes in Pore Structure and Cell Wall Volume Flournoy, Douglas S.; Kirk, T. Kent; Highley, T. L. Holzforschung, Vol. 45, Issue 5 https://doi.org/10.1515/hfsg.1991.45.5.383	journal	January 1991
Detection and Quantification of Oxalic Acid from the Brown-Rot Decay Fungus, Postia placenta Jordan, C. R.; Dashek, W. V.; Highley, T. L. hfsg, Vol. 50, Issue 4 https://doi.org/10.1515/hfsg.1996.50.4.312	journal	January 1996

Similar Records

Distinct Growth and Secretome Strategies for Two Taxonomically Divergent Brown Rot Fungi

Journal Article · Thu Jan 26 19:00:00 EST 2017 · Applied and Environmental Microbiology · OSTI ID:1536859

Oxidation states of iron and manganese in lignocellulose altered by the brown rot fungus Gloeophyllum trabeum measured in-situ using X-ray absorption near edge spectroscopy (XANES)

Journal Article · Tue Dec 22 19:00:00 EST 2020 · International Biodeterioration and Biodegradation · OSTI ID:1819462

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Fenton
lignocellulose
oxalate decarboxylase
reactive oxygen species
wood

A genomics-informed study of oxalate and cellulase regulation by brown rot wood-degrading fungi

Citation Formats

References (39)

Similar Records

Related Subjects