skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Regulation of Gene Expression during the Onset of Ligninolytic Oxidation by Phanerochaete chrysosporium on Spruce Wood

Abstract

Since uncertainty remains about how white rot fungi oxidize and degrade lignin in wood, it would be useful to monitor changes in fungal gene expression during the onset of ligninolysis on a natural substrate. In this paper, we grew Phanerochaete chrysosporium on solid spruce wood and included oxidant-sensing beads bearing the fluorometric dye BODIPY 581/591 in the cultures. Confocal fluorescence microscopy of the beads showed that extracellular oxidation commenced 2 to 3 days after inoculation, coincident with cessation of fungal growth. Whole transcriptome shotgun sequencing (RNA-seq) analyses based on the v.2.2 P. chrysosporium genome identified 356 genes whose transcripts accumulated to relatively high levels at 96 h and were at least four times the levels found at 40 h. Transcripts encoding some lignin peroxidases, manganese peroxidases, and auxiliary enzymes thought to support their activity showed marked apparent upregulation. The data were also consistent with the production of ligninolytic extracellular reactive oxygen species by the action of manganese peroxidase-catalyzed lipid peroxidation, cellobiose dehydrogenase-catalyzed Fe3+ reduction, and oxidase-catalyzed H2O2 production, but the data do not support a role for iron-chelating glycopeptides. In addition, transcripts encoding a variety of proteins with possible roles in lignin fragment uptake and processing, including 27 likely transportersmore » and 18 cytochrome P450s, became more abundant after the onset of extracellular oxidation. Genes encoding cellulases showed little apparent upregulation and thus may be expressed constitutively. Finally, transcripts corresponding to 165 genes of unknown function accumulated more than 4-fold after oxidation commenced, and some of them may merit investigation as possible contributors to ligninolysis.« less

Authors:
 [1];  [2];  [2];  [2];  [2];  [3];  [3]
  1. Mahatma Gandhi Univ., Nalgonda (India). Dept. of Biotechnology
  2. Forest Products Lab., Madison, WI (United States)
  3. Forest Products Lab., Madison, WI (United States); Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1470155
Grant/Contract Number:  
SC0006929
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 81; Journal Issue: 22; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Korripally, Premsagar, Hunt, Christopher G., Houtman, Carl J., Jones, Don C., Kitin, Peter J., Cullen, Dan, and Hammel, Kenneth E. Regulation of Gene Expression during the Onset of Ligninolytic Oxidation by Phanerochaete chrysosporium on Spruce Wood. United States: N. p., 2015. Web. doi:10.1128/AEM.02064-15.
Korripally, Premsagar, Hunt, Christopher G., Houtman, Carl J., Jones, Don C., Kitin, Peter J., Cullen, Dan, & Hammel, Kenneth E. Regulation of Gene Expression during the Onset of Ligninolytic Oxidation by Phanerochaete chrysosporium on Spruce Wood. United States. doi:https://doi.org/10.1128/AEM.02064-15
Korripally, Premsagar, Hunt, Christopher G., Houtman, Carl J., Jones, Don C., Kitin, Peter J., Cullen, Dan, and Hammel, Kenneth E. Fri . "Regulation of Gene Expression during the Onset of Ligninolytic Oxidation by Phanerochaete chrysosporium on Spruce Wood". United States. doi:https://doi.org/10.1128/AEM.02064-15. https://www.osti.gov/servlets/purl/1470155.
@article{osti_1470155,
title = {Regulation of Gene Expression during the Onset of Ligninolytic Oxidation by Phanerochaete chrysosporium on Spruce Wood},
author = {Korripally, Premsagar and Hunt, Christopher G. and Houtman, Carl J. and Jones, Don C. and Kitin, Peter J. and Cullen, Dan and Hammel, Kenneth E.},
abstractNote = {Since uncertainty remains about how white rot fungi oxidize and degrade lignin in wood, it would be useful to monitor changes in fungal gene expression during the onset of ligninolysis on a natural substrate. In this paper, we grew Phanerochaete chrysosporium on solid spruce wood and included oxidant-sensing beads bearing the fluorometric dye BODIPY 581/591 in the cultures. Confocal fluorescence microscopy of the beads showed that extracellular oxidation commenced 2 to 3 days after inoculation, coincident with cessation of fungal growth. Whole transcriptome shotgun sequencing (RNA-seq) analyses based on the v.2.2 P. chrysosporium genome identified 356 genes whose transcripts accumulated to relatively high levels at 96 h and were at least four times the levels found at 40 h. Transcripts encoding some lignin peroxidases, manganese peroxidases, and auxiliary enzymes thought to support their activity showed marked apparent upregulation. The data were also consistent with the production of ligninolytic extracellular reactive oxygen species by the action of manganese peroxidase-catalyzed lipid peroxidation, cellobiose dehydrogenase-catalyzed Fe3+ reduction, and oxidase-catalyzed H2O2 production, but the data do not support a role for iron-chelating glycopeptides. In addition, transcripts encoding a variety of proteins with possible roles in lignin fragment uptake and processing, including 27 likely transporters and 18 cytochrome P450s, became more abundant after the onset of extracellular oxidation. Genes encoding cellulases showed little apparent upregulation and thus may be expressed constitutively. Finally, transcripts corresponding to 165 genes of unknown function accumulated more than 4-fold after oxidation commenced, and some of them may merit investigation as possible contributors to ligninolysis.},
doi = {10.1128/AEM.02064-15},
journal = {Applied and Environmental Microbiology},
number = 22,
volume = 81,
place = {United States},
year = {2015},
month = {9}
}

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

Citation Metrics:
Cited by: 22 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

P450ome of the white rot fungus Phanerochaete chrysosporium: structure, evolution and regulation of expression of genomic P450 clusters
journal, October 2006

  • Yadav, J. S.; Doddapaneni, H.; Subramanian, V.
  • Biochemical Society Transactions, Vol. 34, Issue 6
  • DOI: 10.1042/BST0341165

Comparative Transcriptome and Secretome Analysis of Wood Decay Fungi Postia placenta and Phanerochaete chrysosporium
journal, April 2010

  • Vanden Wymelenberg, A.; Gaskell, J.; Mozuch, M.
  • Applied and Environmental Microbiology, Vol. 76, Issue 11
  • DOI: 10.1128/AEM.00058-10

Characterization of a Δ12-fatty acid desaturase gene from Ceriporiopsis subvermispora, a selective lignin-degrading fungus
journal, February 2010

  • Watanabe, Takahito; Tsuda, Saeko; Nishimura, Hiroshi
  • Applied Microbiology and Biotechnology, Vol. 87, Issue 1
  • DOI: 10.1007/s00253-010-2438-1

Characterization of a hydroxyl-radical-producing glycoprotein and its presumptive genes from the white-rot basidiomycete Phanerochaete chrysosporium
journal, February 2007


Mass spectrometric characterization of the oxidation of the fluorescent lipid peroxidation reporter molecule C11-BODIPY581/591
journal, June 2004


Depolymerization of a synthetic lignin in vitro by lignin peroxidase
journal, January 1991


Transcriptomic Responses of Phanerochaete chrysosporium to Oak Acetonic Extracts: Focus on a New Glutathione Transferase
journal, August 2014

  • Thuillier, Anne; Chibani, Kamel; Belli, Gemma
  • Applied and Environmental Microbiology, Vol. 80, Issue 20
  • DOI: 10.1128/AEM.02103-14

Substrate-specific transcription of the enigmatic GH61 family of the pathogenic white-rot fungus Heterobasidion irregulare during growth on lignocellulose
journal, June 2012

  • Yakovlev, Igor; Vaaje-Kolstad, Gustav; Hietala, Ari M.
  • Applied Microbiology and Biotechnology, Vol. 95, Issue 4
  • DOI: 10.1007/s00253-012-4206-x

Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components
journal, August 2011

  • Quinlan, R. J.; Sweeney, M. D.; Lo Leggio, L.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 37, p. 15079-15084
  • DOI: 10.1073/pnas.1105776108

Reactive oxygen species as agents of wood decay by fungi
journal, April 2002

  • Hammel, Kenneth E.; Kapich, Alexander N.; Jensen, Kenneth A.
  • Enzyme and Microbial Technology, Vol. 30, Issue 4
  • DOI: 10.1016/S0141-0229(02)00011-X

Enzymatic "Combustion": The Microbial Degradation of Lignin
journal, October 1987


Cell wall alterations in loblolly pine wood decayed by the white-rot fungus, Ceriporiopsis subvermispora
journal, March 1997


Peroxyl radicals are potential agents of lignin biodegradation
journal, November 1999


Mineralization and solubilization of synthetic lignin by manganese peroxidases from Nematoloma frowardii and Phlebia radiata
journal, January 1999


Transcriptome and Secretome Analyses of Phanerochaete chrysosporium Reveal Complex Patterns of Gene Expression
journal, April 2009

  • Vanden Wymelenberg, A.; Gaskell, J.; Mozuch, M.
  • Applied and Environmental Microbiology, Vol. 75, Issue 12
  • DOI: 10.1128/AEM.00314-09

A Novel Extracellular Multicopper Oxidase from Phanerochaete chrysosporium with Ferroxidase Activity
journal, October 2003


Discovery of LPMO activity on hemicelluloses shows the importance of oxidative processes in plant cell wall degradation
journal, April 2014

  • Agger, J. W.; Isaksen, T.; Varnai, A.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 17
  • DOI: 10.1073/pnas.1323629111

Oxidative degradation of non-phenolic lignin during lipid peroxidation by fungal manganese peroxidase
journal, November 1994


Cellobiose Dehydrogenase – A Flavocytochrome from Wood-Degrading, Phytopathogenic and Saprotropic Fungi
journal, June 2006


Novel Scheme for Biosynthesis of Aryl Metabolites from L-Phenylalanine in the Fungus Bjerkandera adusta
journal, April 2000


Fungal enzyme sets for plant polysaccharide degradation
journal, July 2011

  • van den Brink, Joost; de Vries, Ronald P.
  • Applied Microbiology and Biotechnology, Vol. 91, Issue 6, p. 1477-1492
  • DOI: 10.1007/s00253-011-3473-2

Induction of Extracellular Hydroxyl Radical Production by White-Rot Fungi through Quinone Redox Cycling
journal, April 2009

  • Gomez-Toribio, V.; Garcia-Martin, A. B.; Martinez, M. J.
  • Applied and Environmental Microbiology, Vol. 75, Issue 12
  • DOI: 10.1128/AEM.02137-08

Evidence from Serpula lacrymans that 2,5-Dimethoxyhydroquinone Is a Lignocellulolytic Agent of Divergent Brown Rot Basidiomycetes
journal, February 2013

  • Korripally, Premsagar; Timokhin, Vitaliy I.; Houtman, Carl J.
  • Applied and Environmental Microbiology, Vol. 79, Issue 7
  • DOI: 10.1128/AEM.03880-12

The Putative Endoglucanase PcGH61D from Phanerochaete chrysosporium Is a Metal-Dependent Oxidative Enzyme that Cleaves Cellulose
journal, November 2011


Cello-Oligosaccharide Oxidation Reveals Differences between Two Lytic Polysaccharide Monooxygenases (Family GH61) from Podospora anserina
journal, November 2012

  • Bey, Mathieu; Zhou, Simeng; Poidevin, Laetitia
  • Applied and Environmental Microbiology, Vol. 79, Issue 2
  • DOI: 10.1128/AEM.02942-12

Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists
journal, February 2015

  • Kohler, Annegret; Kuo, Alan; Nagy, Laszlo G.
  • Nature Genetics, Vol. 47, Issue 4
  • DOI: 10.1038/ng.3223

The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013

  • Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1178

Fungal cytochrome P450 database
journal, January 2008


Genomics of wood-degrading fungi
journal, November 2014


Effects of Coumarate 3-Hydroxylase Down-regulation on Lignin Structure
journal, January 2006

  • Ralph, John; Akiyama, Takuya; Kim, Hoon
  • Journal of Biological Chemistry, Vol. 281, Issue 13, p. 8843-8853
  • DOI: 10.1074/jbc.M511598200

Changes in the Size and Volume of Pores in Sweetgum Wood During Simultaneous Rot by Phanerochaete chrysosporium Burds.
journal, January 1993


Role of fungal peroxidases in biological ligninolysis
journal, June 2008


Influence of Populus Genotype on Gene Expression by the Wood Decay Fungus Phanerochaete chrysosporium
journal, July 2014

  • Gaskell, Jill; Marty, Amber; Mozuch, Michael
  • Applied and Environmental Microbiology, Vol. 80, Issue 18
  • DOI: 10.1128/AEM.01604-14

Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis
journal, March 2012

  • Fernandez-Fueyo, E.; Ruiz-Duenas, F. J.; Ferreira, P.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 14, p. 5458-5463
  • DOI: 10.1073/pnas.1119912109

Oxidizability of unsaturated fatty acids and of a non-phenolic lignin structure in the manganese peroxidase-dependent lipid peroxidation system
journal, February 2010


Role of Quinones in Toxicology
journal, March 2000

  • Bolton, Judy L.; Trush, Michael A.; Penning, Trevor M.
  • Chemical Research in Toxicology, Vol. 13, Issue 3
  • DOI: 10.1021/tx9902082

Cytochrome P450 of wood-rotting basidiomycetes and biotechnological applications: Cytochrome P450s of Basidiomycetes
journal, January 2013

  • Ichinose, Hirofumi
  • Biotechnology and Applied Biochemistry, Vol. 60, Issue 1
  • DOI: 10.1002/bab.1061

Significant Alteration of Gene Expression in Wood Decay Fungi Postia placenta and Phanerochaete chrysosporium by Plant Species
journal, May 2011

  • Vanden Wymelenberg, Amber; Gaskell, Jill; Mozuch, Michael
  • Applied and Environmental Microbiology, Vol. 77, Issue 13
  • DOI: 10.1128/AEM.00508-11

Cellobiose dehydrogenase (cellobiose oxidase) from Phanerochaete chrysosporium as a wood-degrading enzyme. Studies on cellulose, xylan and synthetic lignin
journal, January 1995

  • Henriksson, G.; Ander, P.; Pettersson, B.
  • Applied Microbiology and Biotechnology, Vol. 42, Issue 5
  • DOI: 10.1007/BF00171963

Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78
journal, May 2004

  • Martinez, Diego; Larrondo, Luis F.; Putnam, Nik
  • Nature Biotechnology, Vol. 22, Issue 6
  • DOI: 10.1038/nbt967

Extracellular oxidative systems of the lignin-degrading Basidiomycete Phanerochaete chrysosporium
journal, February 2007


Extracellular lipid peroxidation of selective white-rot fungus, Ceriporiopsis subvermispora
journal, November 1999


Identification of a phenolic 3-O-methyltransferase in the lignin-degrading fungus Phanerochaete chrysosporium
journal, June 1997


Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes
journal, January 2013

  • Levasseur, Anthony; Drula, Elodie; Lombard, Vincent
  • Biotechnology for Biofuels, Vol. 6, Issue 1, Article No. 41
  • DOI: 10.1186/1754-6834-6-41

Expression of Phanerochaete chrysosporium Genes Encoding Lignin Peroxidases, Manganese Peroxidases, and Glyoxal Oxidase in Wood
journal, September 1998


A Simple Method That Uses Differential Staining and Light Microscopy To Assess the Selectivity of Wood Delignification by White Rot Fungi
journal, January 1994


Organization and Differential Regulation of a Cluster of Lignin Peroxidase Genes of Phanerochaete chrysosporium
journal, June 1999


Biosynthetic Pathway for Veratryl Alcohol in the Ligninolytic Fungus Phanerochaete chrysosporium
journal, January 1994

  • Jensen, Kenneth A.; Evans, Kathryn M. C.; Kirk, T. Kent
  • Applied and Environmental Microbiology, Vol. 60, Issue 2
  • DOI: 10.1128/AEM.60.2.709-714.1994

    Works referencing / citing this record:

    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
    • DOI: 10.1128/mbio.02176-19

    Genetic Bases of Fungal White Rot Wood Decay Predicted by Phylogenomic Analysis of Correlated Gene-Phenotype Evolution
    journal, November 2016

    • Nagy, László G.; Riley, Robert; Bergmann, Philip J.
    • Molecular Biology and Evolution, Vol. 34, Issue 1
    • DOI: 10.1093/molbev/msw238

    Lignin-degrading peroxidases in white-rot fungus Trametes hirsuta 072. Absolute expression quantification of full multigene family
    journal, March 2017


    Degradation of antifungal anthraquinone compounds is a probable physiological role of DyP secreted by Bjerkandera adusta
    journal, April 2019


    Transcription of lignocellulose-decomposition associated genes, enzyme activities and production of ethanol upon bioconversion of waste substrate by Phlebia radiata
    journal, May 2018

    • Mäkinen, Mari A.; Risulainen, Netta; Mattila, Hans
    • Applied Microbiology and Biotechnology, Vol. 102, Issue 13
    • DOI: 10.1007/s00253-018-9045-y

    Oak extractive-induced stress reveals the involvement of new enzymes in the early detoxification response of Phanerochaete chrysosporium: Early fungal responses to oak extractives
    journal, October 2018

    • Fernández-González, Antonio José; Valette, Nicolas; Kohler, Annegret
    • Environmental Microbiology, Vol. 20, Issue 10
    • DOI: 10.1111/1462-2920.14409

    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
    • DOI: 10.1073/pnas.1608454113

    Oxidoreductases and Reactive Oxygen Species in Conversion of Lignocellulosic Biomass
    journal, September 2018

    • Bissaro, Bastien; Várnai, Anikó; Røhr, Åsmund K.
    • Microbiology and Molecular Biology Reviews, Vol. 82, Issue 4
    • DOI: 10.1128/mmbr.00029-18

    Time-scale dynamics of proteome and transcriptome of the white-rot fungus Phlebia radiata: growth on spruce wood and decay effect on lignocellulose
    journal, September 2016


    Deciphering lignocellulose deconstruction by the white rot fungus Irpex lacteus based on genomic and transcriptomic analyses
    journal, March 2018


    Gene Co-expression Network Reveals Potential New Genes Related to Sugarcane Bagasse Degradation in Trichoderma reesei RUT-30
    journal, October 2018

    • Borin, Gustavo Pagotto; Carazzolle, Marcelo Falsarella; dos Santos, Renato Augusto Corrêa
    • Frontiers in Bioengineering and Biotechnology, Vol. 6
    • DOI: 10.3389/fbioe.2018.00151

    Heterologous Production and Characterization of Two Glyoxal Oxidases from Pycnoporus cinnabarinus
    journal, June 2016

    • Daou, Marianne; Piumi, François; Cullen, Daniel
    • Applied and Environmental Microbiology, Vol. 82, Issue 16
    • DOI: 10.1128/aem.00304-16

    Time-scale dynamics of proteome and transcriptome of the white-rot fungus Phlebia radiata: growth on spruce wood and decay effect on lignocellulose
    journal, September 2016


    Dynamics of the Phanerochaete carnosa transcriptome during growth on aspen and spruce
    journal, November 2018