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Fungal metabolism of environmentally persistent compounds: Substrate recognition and metabolic response

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Abstract

Mechanism of lignin biodegradation caused by basidiomycetes and the history of lignin biodegradation studies were briefly reviewed. The important roles of fungal extracellular ligninolytic enzymes such as lignin and manganese peroxidases (LiP and MnP) were also summarized. These enzymes were unique in their catalytic mechanisms and substrate specificities. Either LiP or MnP system is capable of oxidizing a variety of aromatic substrates via a one-electron oxidation. Extracellular fungal system for aromatic degradation is non-specific, which recently attracts many people working in a bioremediation field. On the other hand, an intracellular degradation system for aromatic compounds is rather specific in the fungal cell. Structurally similar compounds were prepared and metabolized, indicating that an intracellular degradation strategy consisted of the cellular systems for substrate recognition and metabolic response. It was assumed that lignin-degrading fungi might be needed to develop multiple metabolic pathways for a variety of aromatic compounds caused by the action of non-specific ligninolytic enzymes on lignin. Our recent results on chemical stress responsible factors analyzed using mRNA differential display techniques were also mentioned.

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References

  1. Crawford, R. L. (1981)Lignin Biodegradation and Transformation, John Wiley & Sons, NY, USA.

    Google Scholar 

  2. Sarkanen, K. V. and C. H. Ludwig (1971).Lignins: Occurence, Formation, Structure and Reactions. John Wiley & Sons, NY, USA.

    Google Scholar 

  3. Freudenburg, K. (1968)Constitution and Biosynthesis of Lignin. pp. 47–122, Springer-Verlag, NY, USA.

    Google Scholar 

  4. Gold, M. H., H. Wariishi, and K. Valli (1989)Biocatalysis in Agricultural Biotechnology, pp. 127–140. In J. R. Whitaker and P. Sonnet (eds.).ACS Symposium Series 389 American Chemical Society Washington D.C., USA.

    Google Scholar 

  5. Kirk, T. K. and R. L. Farrell (1987) Enzymatic combustion: The microbial degradation of lignin.Annu. Rev. Microbiol. 41: 465–505.

    Article  CAS  Google Scholar 

  6. Tien, M. (1987) Proporties of ligninase fromPhanerochaete chrysosporium and their possible applications.CRC Crit. Rev. Microbiol. 15: 141–168.

    CAS  Google Scholar 

  7. Kirk, T. K., W. J. Connors, and J. G. Zeikus (1976) Requirement of a growth substrate during lignin decomposition by two wood-rotting fungi.Appl. Environ. Microbiol. 32: 192–194.

    CAS  Google Scholar 

  8. Higuchi, T. (1971) Formation and biological degradation of lignins.Adv. Enzymol. 34: 207–283.

    CAS  Google Scholar 

  9. Hata, K. (1966) Investigations on lignins and lignification: Studies on lignins isolated from spruce wood decayed byPoria subiacida BII.Holzforschung 20: 142–147.

    Article  CAS  Google Scholar 

  10. Kirk, T. K., and H.-M. Chang (1975) Decomposition of lignin by white-rot fungi: Characterization of heavily degraded lignins from decayed spruce.Holzforschung 29: 56–64.

    Article  CAS  Google Scholar 

  11. Tai, D., M. Terazawa, C.-L. Chen, H.-M. Chang, and T. K. Kirk (1983)Recent Advances in Lignin Biodegradation Research. pp. 43–63. In: T. Higuchi, H.-M. Chang and T. K. Kirk (eds.) Um Publisher Ltd. Tokyo, Japan.

    Google Scholar 

  12. Birdsall, H. H. and W. E. Eslyn (1974) Formation of conidial spores ofPhanerochaete chrysosporium Mycotoxit. 109: 123–133.

    Google Scholar 

  13. Gold, M. H. and T. M. Cheng (1978) Induction of colonial growth and replica plating of the white rot basidiomy cetePhanaerochaete chrysosporium.Arch. Microbiol. 121: 37–41.

    Article  Google Scholar 

  14. Jeffries, T. W., S. Choi, and T. K. Kirk (1981) Ligninolytic enzyme system ofPhanaerochaete chrysosporium: Synthesized in the absence of lignin in response to nitrogen storvation.Appl. Environ. Microbiol. 42: 290–296.

    CAS  Google Scholar 

  15. Cold, M. H., J. K. Glenn, M. B. Mayfield, M. A. Morgan, and H. Kutsuki (1983)Recent Advances in Lignim Biodegradation Research. pp. 219–232. In: T. Higuchi, H.-M. Chang and T. K. Kirk (eds.) Uni Publisher Ltd. Tokyo, Japan.

    Google Scholar 

  16. Kirk, T. K. and M. Tien (1983)Recent Advances in Lignin Biodegradation Research. pp. 219–232. In: T. Higuchi, H.-M. Chang and T. K. Kirk (eds.) Uni Publisher Ltd., Tokyo, Japan.

    Google Scholar 

  17. Clenn, J. K., M. A. Morgan, M. C. Mayfield, M. Kuwahara, and M. H. Gold (1983) An extracellular H2O2-requiring enzyme preparation involved in lignin biodegradation by the white rot basidiomycetePhanerochaete chrysosporium Biochem. Biophys. Res. Commun. 114: 1077–1083.

    Article  Google Scholar 

  18. Tien, M. and T. K. Kirk (1983) Lignin-degrading enzymes from the hymenomycetePhanerochaete chrysosporium Science 221: 661–663.

    Article  CAS  Google Scholar 

  19. Kuwahara, M., J. K. Glenn, M. A. Morgan, and M. H. Gold (1984) Seperation and characterization of two extracellular H2O2-dependent oxidases from ligninolytic cultures ofPhanerochaete chrysosporium.FEBS Lett. 169: 247–250.

    Article  CAS  Google Scholar 

  20. Ichinose, H., H. Wariishi, and H. Tanaka (1999) Bioconversion of recalcitrant 4-methyldibenzothiophene to water-extractable products using lignin-degrading basidiomyceteCoriolus versicolor Biotechnol. Prog. 15: 706–714.

    Article  CAS  Google Scholar 

  21. Bavendamm, W. (1928) Über das Vorkommen und den nachweis von oxydasen bei holzzerstlösrenden pilzen.Z. Pflanzenler. 38: 257–276.

    CAS  Google Scholar 

  22. Ander, P. and K.-E. Eriksson (1978) Involvement of phenoloxidases in fungal Degradation of lignin.Prog. Ind. Alicrobiol. 14: 1–58.

    CAS  Google Scholar 

  23. Bournnais, R. and M. G. Paice (1990) Oxidation of nonphenolic substrates: An expanded role for laccase in lignin biodegradation.FEBS Lett. 267: 99–102.

    Article  Google Scholar 

  24. Kawai, S., M. Atsukai, N. Ohya, K. Okita, T. Ito, and H. Ohashi (1999) Aromatic ring cleavage of a non-phenolic β-O-4 lignin model dimer by laccase ofTrametes versicolor in the presence of 1-hydroxybenzotriazoleFEBS Lett. 170: 51–57.

    CAS  Google Scholar 

  25. Majcherczyk, A., C. Johannes, and A. Huttermann (1998) Oxidation of polycyclic aromatic hydrocarbons (PAH) by laccase ofTrametes versicolor Enzyme Microb. Technol. 22: 335–341.

    Article  CAS  Google Scholar 

  26. Gold, M. H., Mayfield, M. G., Godfery, B., Brown, J., Wariishi, H., and Alic, M. (1993)Plant Peroxidases: Biochemistry and Physiology. pp. 87–95, University of Geneva, Swiss.

    Google Scholar 

  27. Glenn, J. K. and M. H. Gold (1985) Purification and characterization of an extracellular Mn(II)-dependent peroxidase from the lignin-degrading basidiomycete,Phanerochacte chrysosporium.Arch. Biochem. Biophys. 242: 329–341.

    Article  CAS  Google Scholar 

  28. Wariishi, H., K. Valli, and M. H. Gold (1989) Manganese peroxidase from the basidiomycetePhanerochaete chrysesporium: spectral characterization of the oxidized states and the catalytic cycle.Biochemistry 28: 6017–6023.

    Article  CAS  Google Scholar 

  29. Wariishi, H., K. Valli, V. Renganathan, and M. H. Gold (1989) Thiol-mediated oxidation of nonphenolic lignin model compounds by manganese peroxidase ofPhanerechaete chrysosporium.J. Biol. Chem. 264: 14185–14191.

    CAS  Google Scholar 

  30. Wariishi, H., K. Valli, and M. H. Gold (1991)In vitro depelymerization of lignin by manganese peroxidase ofPhanerochaete chrysosporium.Biochem. Biophys. Res. Commun. 176: 269–275.

    Article  CAS  Google Scholar 

  31. Wariishi, H., H. B. Dunford, I. D. MacDonald, and M. H. Gold (1989) Manganese peroxidase from the lignindegrading basidiomycetePhanerochaete chrysosporium: Transient state kinetics and reaction mechanism.J. Biol. Chem. 264: 3335–3340.

    CAS  Google Scholar 

  32. Sundaramoorthy, M., K. Kishi, M. H. Gold, and T. L. Poulos (1994) The crystal structure of manganese peroxidase fromPhanerochaete chrysosporium at 2.06-Å resolution.J. Biol. Chem. 269: 32759–32767.

    CAS  Google Scholar 

  33. Hattaka, A. (1994) Lignin-modifying enzymes from selected white-rot fungi: Production and role in lignin degradation.FEMS Microbiol. Rev. 13: 125–135.

    Article  Google Scholar 

  34. Kersten, P. J., M. Tien, B. Kalyanaraman, and T. K. Kirk (1985) The ligninase ofPhanerochaete chrysosporium generates cation radicals from methoxybenzenes.J. Biol. Chem. 260: 2609–2612.

    CAS  Google Scholar 

  35. Wariishi, H. and M. H. Gold (1990) Lignin peroxidase compounds II and III: Spectral and kinetic characterization of reactions with peroxides.J. Biol. Chem. 265: 11137–11142.

    CAS  Google Scholar 

  36. Schoemaker, H. E., P. J. Harvey, R. M. Bowen, and J. M. Palmer (1985) On the mechanism of enzymatic lignin breakdownFEBS Lett. 183: 7–12.

    Article  CAS  Google Scholar 

  37. Renganathan, V. and M. H. Gold (1986) Role of molecular oxygen in lignin peroxidase reactions.Biochemistry 25: 1626–1631.

    Article  CAS  Google Scholar 

  38. Lundquist, K. and T. K. Kirk (1978) De novosynthesis and decomposition of veratryl alcohol by a lignin-degrading basidiomycete.Phytochemistry 17: 1676–1681.

    Article  CAS  Google Scholar 

  39. Harvey, P. J., H. E. Schoemaker, R. M. Bowen, and J. M. Palmer (1985) Single-electron transfer processes and the reaction mechanism of enzymic degradation of lignin.FEBS Lett. 183: 13–16.

    Article  CAS  Google Scholar 

  40. Leisola, M. S. A., S. D. Haemmerli, R. Waldner, H. E. Schoemaker, W. H. Schmidt, and A. Fiechter (1988) Metabolism of a lignin model compound, 3,4-dimethoxybenzyl alcohol byPhanerochaete chrysosporium.Cellulose Chem. Technol. 22: 267–277.

    CAS  Google Scholar 

  41. Hammel, K. E. and M. A. Moen (1991) Depolymerization of a synthetic ligninin vitro by lignin peroxidas.Enzyme Microbial. Technol. 13: 15–18.

    Article  CAS  Google Scholar 

  42. Schoemaker, H. E., T. K. Lundell, A. Hatakka, and K. Piontek (1994) The oxidation of veratryl alcohol, dimeric lignin models and lignin by lignin.FEMS Microbiol. Rev. 13: 321–332.

    Article  CAS  Google Scholar 

  43. Barr, D. P. and S. D. Aust (1994) Pollutant degradation by white rot fungi.Rev. Environ. Contam. Toxicol. 138: 49–72.

    CAS  Google Scholar 

  44. Wariishi, H., D. Sheng, and M. H. Gold (1994) Oxidation of ferrocytochromec by lignin peroxidase.Biochemistry 33: 5545–5552.

    Article  CAS  Google Scholar 

  45. Beratan, D. N., J. N. Onuchic, J. R. Winkler, and H. B. Cray (1992) Electron-tunneling pathways in proteins.Science 253: 1740–1741.

    Article  Google Scholar 

  46. Moser, C. C., J. M. Keske, K. Warncke, R. S. Farid, and L. Dutton (1992) Nature of biological electron transfer.Nature 355: 796–802.

    Article  CAS  Google Scholar 

  47. Edwards, S. L., R. Raag, H. Wariishi, M. H. Gold, and T. L. Poulos (1993) Crystal structure of lignin peroxidase.Proc. Natl. Acad. Sci. USA 90: 750–754.

    Article  CAS  Google Scholar 

  48. Poulos, T. L., S. L. Edwards, H. Wariishi, and M. H. Gold (1998) Crystallographic refinement of lignin peroxidase at 2 Å.J. Biol. Chem. 268: 4429–4440.

    Google Scholar 

  49. Piontek, K., T. Glumoff, and K. H. Winterhalter (1993) Low pH crystal structure of glycosylated lignin peroxidase fromPhanerochaete chrysosporium at 2.5 Å resolution.FEBS Lett. 315: 119–124.

    Article  CAS  Google Scholar 

  50. Blodig, W., A. Doyle, A. T. Smith, K. Winterhalter, T. Choinowski, and K. Piontek (1998) Autocatalytic formation of a hydroxy group at C beta of trp171 in lignin peroxidase.Biochemistry 37: 8832–8838.

    Article  CAS  Google Scholar 

  51. Doyle, W. A., W. Blodig, N. C. Veitch, T. Piontek, and A. T. Smith (1998) Two substrate interaction sites in lignin peroxidase revealed by site-directed mutagenesis.Biochemistry 37: 15097–152105.

    Article  CAS  Google Scholar 

  52. Johjima, T., N. Itoh, M. Kabuto, F. Tokimura, T. Nakagawa, H. Wariishi, and H. Tanaka (1999) Direct interaction of lignin and lignin peroxidase fromPhancrochaete chrysosporium.Proc. Natl. Acad. Sci. USA 96: 1985–1989.

    Article  Google Scholar 

  53. Timofeeyski, S. L., G. Nie, N. S. Reading, and S. D. Aust (2000) Substrate specificity of lignin peroxidase and a S168W variant of manganese peroxidase.Arch. Biochem. Biophys. 373: 147–153.

    Article  CAS  Google Scholar 

  54. Dunford, H. B. and J. S. Stillman (1976) On the function and mechanism of action of peroxidases.Coord. Chem. Rev. 19: 187–251.

    Article  CAS  Google Scholar 

  55. Dunford, H. B. (1991)Peroxidase in Chemistry and Biology. pp. 1–24. In: I. Everse, K. E. Evers, and M. B. Grisham (eds.). Vol. II, CRC Press, Boca Raton, FL, USA.

    Google Scholar 

  56. Dawson, J. H. (1988) Probing structure-function relations in heme-containing oxygenases and peroxidasesScience 240: 433–439.

    Article  CAS  Google Scholar 

  57. Poulos, T. L. and B. C. Finzel (1984)Peptide and Protein Reviews, pp. 115–171. In: M. T. W. Hearn (ed.) Vol. 4, Marcel Dekker, Inc., New York, USA.

    Google Scholar 

  58. Dixon, W. T. and D. Murphy (1976) Determination of the acidity constants of some phenol radical cations by means of electron spin resonance.J. Chem. Soc. Faraday Trans. Il 72: 1221–1230.

    Article  CAS  Google Scholar 

  59. Andrawis, A., K. A. Johnson, and M. Tien (1988) Studies on compound I formation of the lignin peroxidase fromPhancrochaete chrysosporium.J. Biol. Chem. 263: 1195–1198.

    CAS  Google Scholar 

  60. Marquez, L., H. Wariishi, H. B. Dunford, and M. H. Gold (1988) Spectroscopic and kinetic properties of the oxidized intermediates of lignin peroxidase fromPhancrochacte chrysosporium.J. Biol. Chem. 263: 10549–10552.

    CAS  Google Scholar 

  61. Hammel, K. E., W. Z. Gai, B. Green, and M. A. Moen (1992) Oxidative degradation of phenanthrene by the ligninolytic fungusPhanerochaete chrysosporium.Appl. Environ. Microbiol. 58: 1832–1838.

    CAS  Google Scholar 

  62. Valli, K., B. J. Brock, D. Joshi, and M. H. Gold (1992) Degradation of 2,4-dinitrotoluene by the lignin degrading fungusPhanerochaete chrysosporium Appl. Environ. Microbiol. 58: 221–228.

    CAS  Google Scholar 

  63. Valli K. and M. H. Gold (1992) Degradation of 2,4-dichlorophenol by the lignin-degrading fungusPhanerochaete chrysosporium J. Bacteriol. 173: 345–52.

    Google Scholar 

  64. Mileski, G. J., J. A. Bumpus, M. A. Jurek, and S. D. Aust (1988) Biodegradation of pentachlorophenol by the white rot fungusPhanerochaete chrysosporium.Appl. Environ. Microbiol. 54: 2885–2889.

    CAS  Google Scholar 

  65. Bumpus, J. A. and S. D. Aust (1987) Oxidation of persistent environmental pollutants by a white rot fungus.Appl. Environ. Microbiol. 53: 2001–2008.

    CAS  Google Scholar 

  66. Aiken, B. S. and B. E. (1996) Degradation of pentachlorophenol by the white rot fungusPhanerochaetc chrysosperium grown in ammonium lignosulphonate media. Biodegradation 7: 175–82.

    Article  CAS  Google Scholar 

  67. Takada S., M. Nakamura, T. Matsueda, R. Kondo, and K. Sakai (1996) Degradation of polychlorinated libenzo-p-dioxins and polychlorinated dibenzofurans by the white rot fungusPhanerochaete sordida YK-624.Appl. Environ. Microbiol. 62: 4323–4328.

    CAS  Google Scholar 

  68. Dietrich, D., W. J. Hickey, and R. Lamar (1995) Degradation of 4,4′-dichloro-biphenyl 3,3′,4,4′-tetrachlorobiphenyl, and 2,2′,4,4′,5,5′-hexachlorobiphenyl by the white rot fungusPhanerochaete chrysosporium.Appl. Environ. Microbiol. 61: 3904–3909.

    CAS  Google Scholar 

  69. Yadav, J. S., R. E. Wallace, and C. A. Reddy (1995) Mineralization of mono- and dichlorobenzenes and simultaneous degradation of chloro- and methyl-substituted benzenes by the white rot fungusPhanerochaete chrysosperium.Appl. Environ. Microbiol. 61: 677–680.

    CAS  Google Scholar 

  70. Yadav, J. S., J. E. Quensen III, J. M. Tiedje, and C. A. Reddy (1995) Degradation of polychlorinated biphenyl mixtures (Aroclors 1242, 1254, and 1260) by the white rot fungusPhanerochaete chrysosporium as evidenced by congener specific analysis.Appl. Environ. Microbiol. 61: 2560–2565.

    CAS  Google Scholar 

  71. Kremar, P. and R. Ulrich (1998) Degradation of polychlorinated biphenyl mixtures by the lignin-degrading fungusPhanerochaete chrysosporium.Folia Merebiologica 43: 79–84.

    Article  Google Scholar 

  72. D'Annibale, A., C. Crestini, V. Vinciguerra, and G. G. Sermanni (1998) The biodegradation of recalcitrant effluents from an olive mill by a white-rot fungus.J. Biotechnol. 61: 209–218.

    Article  Google Scholar 

  73. Valli K., H. Wariishi, and M. H. Gold (1992) Degradation of 2,7-dichlorodibenzo-p-dioxin by the lignin-degrading basidiomycetePhanerochaete chrysosporium.J. Bacteriol. 174: 2131–2137.

    CAS  Google Scholar 

  74. Joshi, D. K. and M. H. Gold (1994) Oxidation of dibenzo-p-dioxin by lignin peroxidase from the basidiomycetePhancrochaete chrysosporium Biochemistry 33: 10969–10976.

    Article  CAS  Google Scholar 

  75. Bumpus, J. A., M. Tien, D. Wright, and S. D. Aust (1985) Oxidation of persistent environmental pollutants by a white rot fungusScience 228: 1434–1436.

    Article  CAS  Google Scholar 

  76. Reddy, G. V. and M. H. Gold (1999) A two-component tetrachlorohydroquinone reductive dehalogenase system from the lignin-degrading basidiomycetePhanerochaete chrysosporium.Biochem. Biophys. Res. Commun. 257: 901–905.

    Article  CAS  Google Scholar 

  77. Bezalel L., Y. Hadar, P. P. Pu, J. P. Freeman, and C. E. Cerniglia (1996) Metabolism of phenanthrene by the white rot fungusPleurotus ostreatus.Appl. Environ. Microbiol. 62: 2547–2553.

    CAS  Google Scholar 

  78. Ichinose, H., H. Wariishi, and H. Tanaka (1999)Proceedings of the 5th Asia-Pacific Biochemical Engineering Conference. November 15–18. Phuket, Thailand.

  79. Itoh, N., M. Yoshida, M. Miyamoto, H. Ichinose, H. Wariishiand, and H. Tanaka (1997) Fungal cleavage of thioether bond found in Yperite.FEBS Lett. 412: 281–284.

    Article  CAS  Google Scholar 

  80. Liang, P. and A. B. Pardee (1992) Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction.Science 257: 967–971.

    Article  CAS  Google Scholar 

  81. Ito, T., K. Kito, N. Adachi, Y. Mitsui, H. Hagiwara, and Y. Sakaki (1994) Fluorescent differential display: arbitrarily primed RT-PCR fingerprinting on an automated DNA sequencer.FEBS Lett. 351: 231–236.

    Article  CAS  Google Scholar 

  82. Iimura, Y. and K. Tatsumi (1997) Isolation of mRNAs induced by a hazardous chemical in white-rot fungus,Coriolus versicolor, by differential display.FEBS Lett. 412: 370–374.

    Article  CAS  Google Scholar 

  83. Leung, G. S. W., M. Zhang, W. J. Xie, and H. S. Kwan (1999) Identification by RNA fingerprinting of genes differentially expressed during the development of the basidiomyceteLentinula edodes.Mol. Gen. Genet. 262: 977–990.

    Article  Google Scholar 

  84. Reiser, J., A. Muheim, M. Hardegger, G. Frank, and A. Fiechter (1994) Arylalcohol dehydrogenase from the white-rot fungusPhancrochaete chrysosporium. Gene cloning, sequence analysis expression, and purification of the recombinant enzyme.J. Biol. Chem. 269: 28152–28159.

    CAS  Google Scholar 

  85. Robbe, N. F., J. Ware, R. M. Bertina, P. Modrich, and D. W. Stafford (1989) Nucleotide sequence of a cDNA for a member of the human 90-kDa heat-shock protein family.Gene 53: 235–245.

    Article  Google Scholar 

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    Hiroyuki Wariishi

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Wariishi, H. Fungal metabolism of environmentally persistent compounds: Substrate recognition and metabolic response. Biotechnol. Bioprocess Eng. 5, 422–430 (2000). https://doi.org/10.1007/BF02931942

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