Chapter 6 Reactive Oxygen Species in Phanerochaete chrysosporium Relationship Between Extracellular Oxidative and Intracellular Antioxidant Systems

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Abstract

The basidiomycete Phanerochaete chrysosporium is a model of ligninolytic fungus which has been studied for a long time. The lignin degradation mediated by this fungus occurs through oxidative processes involving a large set of extracellular enzymes including lignin oxidases and lignin-degrading auxiliary enzymes. In this context, the production of reactive oxygen species (ROS) by this fungus occurs in physiological conditions, that is, during the wood degradation. Ligninolytic basidiomycetes have thus had to develop strategies to protect themselves against oxidative damages induced during lignin oxidation. The excretion of extracellular ligninolytic enzymes is indeed linked at least partially to the fungal intracellular redox state, suggesting a relationship between the intracellular antioxidant system and the production of extracellular ROS by this fungus. This review describes the extracellular systems involved in ROS production, the intracellular systems protecting against ROS, as well as the relationship between them.

Section snippets

Extracellular Reactive Oxygen Species (ROS) Formation

Lignin plays a key role in the carbon cycle as the most abundant aromatic compound in nature, providing the protective matrix surrounding the cellulose microfibrils of plant cell walls. This amorphous and insoluble polymer lacks stereoregularity and, in contrast to cellulose and hemicellulose, it is not susceptible to hydrolytic attack. Lignin is made up of phenylpropanoid units which are linked by a variety of carbonā€“carbon and carbonā€“oxygen bonds, making it very difficult to degrade. However,

Intracellular ROS Formation

The major part of oxygen consumed by aerobic cells is converted into water in mitochondria via a four-electron reduction reaction, catalyzed by cytochrome c oxidase (respiratory complex IV). A much smaller part is converted into H2O2 as a result of two-electron reduction, catalyzed by a number of enzymes. It should be emphasized that in addition to the most active ensemble of oxidoreductases, known as the respiratory chain, intact mitochondria contain a number of oxidoreductases both in the

The glutathione

Glutathione (Ī³-l-glutamyl-l-cysteinyl-glycine) is synthesized through the activity of two enzymes, the Ī³-l-glutamyl-l-cysteine ligase (GCL) and the glutathione synthetase (GS). In P. chrysosporium, one GCL (PcGCL) and also one GS (PcGS) are predicted from the sequenced genome (Table I). In addition, glutathione has been detected in this fungus (Belinky et al., 2003). Glutathione plays a major role in ROS detoxification, reacting directly with different compounds such as hydrogen peroxide or

Relationship Between Intracellular ROS and Lignin Degradation

The formation of LiP is particularly dependent on exposure of cultures to high oxygen tensions; indeed, cultures of P. chrysosporium which are oxygen starved at the pellet centre produce much lower levels of LiPs and MnPs (Dosoretz et al., 1990). It has been thus proposed that a high partial pressure of oxygen in the culture headspace is needed to make sufficient oxygen available to the submerged hyphae (Michel et al., 1992). Oxygen has, however, the potential to give rise to toxic oxygen-free

References (126)

  • M. Finel

    Genetic inactivation of the H(+)-translocating NADH:ubiquinone oxidoreductase of Paracoccus denitrificans is facilitated by insertion of the ndh gene from Escherichia coli

    FEBS Letters

    (1996)
  • H.J. Forman et al.

    Dihydroorotate-dependent superoxide production in rat brain and liver. A function of the primary dehydrogenase

    Archives of Biochemistry and Biophysics

    (1976)
  • H.J. Forman et al.

    The chemistry of cell signaling by reactive oxygen and nitrogen species and 4-hydroxynonenal

    Archives of Biochemistry and Biophysics

    (2008)
  • J.K. Glenn et al.

    An extracellular H2O2-requiring enzyme preparation involved in lignin biodegradation by the white rot basidiomycete Phanerochaete chrysosporium

    Biochemical and Biophysical Research Communications

    (1983)
  • V.G. Grivennikova et al.

    Generation of superoxide by the mitochondrial Complex I

    Biochimica et Biophysica Acta

    (2006)
  • V. Haedens et al.

    Genetic control of an epigenetic cell degeneration syndrome in Podospora anserina

    Fungal Genetics and Biology

    (2005)
  • K.E. Hammel et al.

    Role of fungal peroxidases in biological ligninolysis

    Current Opinion in Plant Biology

    (2008)
  • H.M. Hassan et al.

    Roles of manganese and iron in the regulation of the biosynthesis of manganese-superoxide dismutase in Escherichia coli

    FEMS Microbiology Reviews

    (1994)
  • A. Heinfling et al.

    A study on reducing substrates of manganese-oxidizing peroxidases from Pleurotus eryngii and Bjerkandera adusta

    FEBS Letters

    (1998)
  • E. Herrero et al.

    Redox control and oxidative stress in yeast cells

    Biochimica et Biophysica Acta-General Subjects

    (2008)
  • T.R. Hurd et al.

    Detection of reactive oxygen species-sensitive thiol proteins by redox difference gel electrophoresis: Implications for mitochondrial redox signaling

    Journal of Biological Chemistry

    (2007)
  • T.M. Johnson et al.

    Production and characterization of recombinant lignin peroxidase isozyme H2 from Phanerochaete chrysosporium using recombinant baculovirus

    Archives of Biochemistry and Biophysics

    (1992)
  • T. Joseph-Horne et al.

    Fungal respiration: A fusion of standard and alternative components

    Biochimica et Biophysica Acta

    (2001)
  • P.J. Kersten et al.

    Extracellular oxidative systems of the lignin-degrading Basidiomycete Phanerochaete chrysosporium

    Fungal Genetics and Biology

    (2007)
  • A.J. Lambert et al.

    Inhibitors of the quinone-binding site allow rapid superoxide production from mitochondrial NADH:ubiquinone oxidoreductase (complex I)

    Journal of Biological Chemistry

    (2004)
  • J.L. Lavin et al.

    Comparative genomics of the oxidative phosphorylation system in fungi

    Fungal Genetics and Biology

    (2008)
  • A. Levasseur et al.

    FOLy: An integrated database for the classification and functional annotation of fungal oxidoreductases potentially involved in the degradation of lignin and related aromatic compounds

    Fungal Genetics and Biology

    (2008)
  • F. Malagnac et al.

    Two NADPH oxidase isoforms are required for sexual reproduction and ascospore germination in the filamentous fungus Podospora anserina

    Fungal Genetics and Biology

    (2004)
  • S. McGoldrick et al.

    Glutathione transferase-like proteins encoded in genomes of yeasts and fungi: Insights into evolution of a multifunctional protein superfamily

    FEMS Microbiology Letters

    (2005)
  • A.M. Melo et al.

    The external calcium-dependent NADPH dehydrogenase from Neurospora crassa mitochondria

    Journal of Biological Chemistry

    (2001)
  • D. Miura et al.

    Metabolomic differential display analysis of the white-rot basidiomycete Phanerochaete chrysosporium grown under air and 100% oxygen

    FEMS Microbiology Letters

    (2004)
  • F.L. Muller et al.

    Complex III releases superoxide to both sides of the inner mitochondrial membrane

    Journal of Biological Chemistry

    (2004)
  • A.B. Orth et al.

    Characterization of a cDNA encoding a manganese peroxidase from Phanerochaete chrysosporium: Genomic organization of lignin and manganese peroxidase-encoding genes

    Gene

    (1994)
  • E.A. Pease et al.

    Manganese-dependent peroxidase from Phanerochaete chrysosporium. Primary structure deduced from cDNA sequence

    Journal of Biological Chemistry

    (1989)
  • D. Pribnow et al.

    Characterization of a cDNA encoding a manganese peroxidase, from the lignin-degrading basidiomycete Phanerochaete chrysosporium

    Journal of Biological Chemistry

    (1989)
  • A.G. Rasmusson et al.

    Physiological, biochemical and molecular aspects of mitochondrial complex I in plants

    Biochimica et Biophysica Acta

    (1998)
  • J.P. Reichheld et al.

    AtNTRB is the major mitochondrial thioredoxin reductase in Arabidopsis thaliana

    FEBS Letters

    (2005)
  • N. Rouhier et al.

    The plant multigenic family of thiol peroxidases

    Free Radical Biology and Medicine

    (2005)
  • B.B. Seo et al.

    Modulation of oxidative phosphorylation of human kidney 293 cells by transfection with the internal rotenone-insensitive NADH-quinone oxidoreductase (NDI1) gene of Saccharomyces cerevisiae

    Biochimica et Biophysica Acta

    (1999)
  • B.B. Seo et al.

    Use of the NADH-quinone oxidoreductase (NDI1) gene of Saccharomyces cerevisiae as a possible cure for complex I defects in human cells

    Journal of Biological Chemistry

    (2000)
  • P. Silar

    Peroxide accumulation and cell death in filamentous fungi induced by contact with a contestant

    Mycological Research

    (2005)
  • A. Agbas et al.

    The role of methionine oxidation/reduction in the regulation of immune response

    Current Signal Transduction Therapy

    (2009)
  • L. Akileswaran et al.

    1, 4-benzoquinone reductase from Phanerochaete chrysosporium: cDNA cloning and regulation of expression

    Applied and Environmental Microbiology

    (1999)
  • S.L.A. Andrade et al.

    Crystal structure of the NADH: Quinone oxidoreductase WrbA from Escherichia coli

    Journal of Bacteriology

    (2007)
  • C.D. Archer et al.

    Mutants defective in the energy-conserving NADH dehydrogenase of Salmonella typhimurium identified by a decrease in energy-dependent proteolysis after carbon starvation

    Proceedings of the National Academy of Sciences of the United States of America

    (1993)
  • M.J. Artolozaga et al.

    Pyranose 2-oxidase from Phanerochaete chrysosporiumā€”Further biochemical characterisation

    Applied Microbiology and Biotechnology

    (1997)
  • P.A. Belinky et al.

    Reactive oxygen species and induction of lignin peroxidase in Phanerochaete chrysosporium

    Applied and Environmental Microbiology

    (2003)
  • D. Bironaite et al.

    Interaction of quinones with Arabidopsis thaliana thioredoxin reductase

    Biochimica et Biophysica Acta

    (1998)
  • H. Bouws et al.

    Fungal secretomesā€”Nature's toolbox for white biotechnology

    Applied and Microbiology and Biotechnology

    (2008)
  • B.J. Brock et al.

    Purification and characterization of a 1,4 benzoquinone reductase from the basidiomycete Phanerochaete chrysosporium

    Applied and Environmental Microbiology

    (1995)
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