Antonie van Leeuwenhoek

, Volume 63, Issue 2, pp 125–144

Catabolism of benzene compounds by ascomycetous and basidiomycetous yeasts and yeastlike fungi

A literature review and an experimental approach
  • Wouter J. Middelhoven
Article

Abstract

A literature review is given on growth of yeasts on benzene compounds and on the catabolic pathways involved. Additionally, a yeast collection was screened for assimilation of phenol and 3-hydroxybenzoic acid. Fifteen ascomycetous and thirteen basidiomycetous yeast species were selected and were tested for growth on 84 benzene compounds. It appeared that 63 of these compounds supported growth of one or more yeast species. The black yeastExophiala jeanselmei assimilated 54 of these compounds.

The catechol branch of the 3-oxoadipate pathway and its hydroxyhydroquinone variant were involved in phenol and resorcinol catabolism of ascomycetes as well as of basidiomycetes. However, these two groups of yeasts showed characteristic differences in hydroxybenzoate catabolism. In the yeastlike fungusE. jeanselmei and in basidiomycetes of the generaCryptococcus, Leucosporidium andRhodotorula, the protocatechuate branch of the 3-oxoadipate pathway was induced by growth on 3- and 4-hydroxybenzoic acids. In threeTrichosporon species and in all ascomycetous yeasts tested, 4-hydroxybenzoic acid was catabolyzed via protocatechuate and hydroxyhydroquinone. These yeasts were unable to cleave protocatechuate. 3-Hydroxybenzoic and 3-hydroxycinnamic acids were catabolized in ascomycetous yeasts via the gentisate pathway, but in basidiomycetes via protocatechuate.

Incomplete oxidation of phenol, some chlorophenols, cresols and xylenols was observed in cultures ofCandida parapsilosis growing on hydroquinone. Most compounds transformed by the growing culture were also converted by the phenol monooxygenase present in cell-free extracts of this yeast. They did not support growth.

The relationship between the ability of ascomycetous yeasts to assimilate n-alkanes, amines and benzene compounds, and the presence of Coenzyme Q9 is discussed.

Key words

ascomycetes basidiomycetes benzene compounds hydroxybenzoic acids phenols yeast catabolism 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anderson JJ & Dagley S (1980) Catabolism of aromatic acids inTrichosporon cutaneum. J. Bacteriol. 141: 534–543PubMedGoogle Scholar
  2. Anderson JJ & Dagley S (1981) Catabolism of tryptophan, anthranilate and 2,3-dihydroxybenzoate inTrichosporon cutaneum. J. Bacteriol. 146: 291–297PubMedGoogle Scholar
  3. Cain RB, Bilton RF & Darrah JA (1968) The metabolism of aromatic acids by microorganisms: metabolic pathways in the fungi. Biochem. J. 108: 797–828PubMedGoogle Scholar
  4. Catellani D, Fiechi A & Galli E (1971) (+)-γ-Carboxymethyl-γ-methyl-δ-butenolide, a 1,2-ring-fission product of 4-methylcatechol byPseudomonas desmolyticum. Biochem. J. 121: 89–92PubMedGoogle Scholar
  5. Chapman PJ & Ribbons DW (1974) Metabolism of resorcinylic compounds by bacteria: alternative pathways for resorcinol catabolism inPseudomonas putida. J. Bacteriol. 125: 985–998Google Scholar
  6. Cook KA & Cain RB (1974) Regulation of aromatic metabolism in the fungi: metabolic control of the 3-oxoadipate pathway in the yeastRhodotorula mucilaginosa. J. Gen. Microbiol. 85: 37–50PubMedGoogle Scholar
  7. Di Menna ME (1959) Some physiological characters of yeasts from soils and allied habitats. J. Gen. Microbiol. 20: 13–23PubMedGoogle Scholar
  8. Durham DR (1984) Initial reactions involved in the dissimilation of mandelate byRhodotorula graminis. J. Bacteriol. 160: 778–780PubMedGoogle Scholar
  9. Durham DR, McNamee CG & Stewart DB (1984) Dissimilation of aromatic compounds inRhodotorula graminis: biochemical characterization of pleiotropically negative mutants. J. Bacteriol. 160: 771–777PubMedGoogle Scholar
  10. Gaal A & Neujahr HY (1979) Metabolism of phenol and resorcinol inTrichosporon cutaneum. J. Bacteriol. 137: 13–21PubMedGoogle Scholar
  11. Gaal A & Neujahr HY (1980)cis,cis-Muconate cyclase fromTrichosporon cutaneum. Biochem. J. 191: 37–43PubMedGoogle Scholar
  12. Gaal A & Neujahr HY (1981) Induction of phenol-metabolizing enzymes inTrichosporon cutaneum. Arch. Microbiol. 130: 54–58PubMedGoogle Scholar
  13. Gross SR, Gafford RD & Tatum EL (1956) The metabolism of protocatechuic acid byNeurospora. J. Biol. Chem. 219: 781–795PubMedGoogle Scholar
  14. Guého E, Smith M Th, de Hoog GS, Billon-Grand G, Christen R & Batenburg-van der Vegte WH (1992) Contributions to a revision of the genusTrichosporon. Antonie van Leeuwenhoek 61: 289–316PubMedGoogle Scholar
  15. Harris G & Ricketts RW (1962) Metabolism of phenolic compounds by yeasts. Nature No 4870, 473–474Google Scholar
  16. Hashimoto K (1970) Oxidation of phenols by yeast. I. A new oxidation product from p-cresol by an isolated strain of yeast. J. Gen. Appl. Microbiol. 16: 1–13Google Scholar
  17. Hashimoto K (1973) Oxidation of phenols by yeast. II. Oxidation of cresols byCandida tropicalis. J. Gen. Appl. Microbiol. 19: 171–187Google Scholar
  18. Henderson MEK (1961a) Isolation, identification and growth of some hyphomycetes and yeast-like fungi which utilize aromatic compounds related to lignin. J. Gen. Microbiol. 26: 149–154PubMedGoogle Scholar
  19. Henderson MEK (1961b) The metabolism of aromatic compounds related to lignin by some hyphomycetes and yeast-like fungi from soil. J. Gen. Microbiol. 26: 155–165PubMedGoogle Scholar
  20. Hofmann KH & Krüger AK (1985) Induction and inactivation of phenol hydroxylase and catechol oxygenase inCandida maltosa L4 in dependence on the carbon source. J. Basic Microbiol. 25: 373–379Google Scholar
  21. Hofmann KH & Vogt U (1987) Induction of phenol assimilation in chemostat cultures ofCandida maltosa L4. J. Basic Microbiol. 27: 441–447Google Scholar
  22. Hofmann KH & Vogt U (1988) Abbau von Phenol durch Hefen in Gegenwart von n-Hexadekan unter Wachstumsbedingungen im Rührreaktor. Zentralbl. Mikrobiol. 143: 87–91Google Scholar
  23. Hofmann KH & Schauer F (1988) Utilization of phenol by hydrocarbon-assimilating yeasts. Antonie van Leeuwenhoek 54: 179–188PubMedGoogle Scholar
  24. Hopper DJ, Chapman PJ & Dagley S (1968) Enzymatic formation of D-malate. Biochem. J. 110: 798–800PubMedGoogle Scholar
  25. Jayasankar NP & Bhat JV (1966) Isolation and properties of catechol-cleaving yeasts from coir rets. Antonie van Leeuwenhoek 32: 125–134PubMedGoogle Scholar
  26. Karasevich YN & Ivoilov US (1977) Preparatory metabolism of p-hydroxybenzoic acid inCandida tropicalis. Microbiology 46: 687–695Google Scholar
  27. Kluyver AJ & van Zijp JCM (1951) The production of homogentisic acid out of phenylacetic acid byAspergillus niger. Antonie van Leeuwenhoek 17: 315–324PubMedGoogle Scholar
  28. Krug M & Straube G (1986) Degradation of phenolic compounds by the yeastCandida tropicalis HP 15. II. Some properties of the first two enzymes of the degradation pathway. J. Basic Microbiol. 26: 271–281PubMedGoogle Scholar
  29. Lack L (1961) Enzymaticcis-trans isomerization of maleyl pyruvic acid. J. Biol. Chem. 236: 2835–2840PubMedGoogle Scholar
  30. Marusich WC, Jensen RA & Zamir LO (1981) Induction of phenylalanine ammonia-lyase during utilization of phenylalanine as a carbon or nitrogen source inRhodotorula glutinis. J. Bacteriol. 146: 1013–1019PubMedGoogle Scholar
  31. Middelhoven WJ, de Kievit H & Biesbroek AL (1985) Yeast species utilizing uric acid, adenine, n-alkylamines or diamines as sole source of carbon and energy. Antonie van Leeuwenhoek 51: 289–301PubMedGoogle Scholar
  32. Middelhoven WJ, de Hoog GS & Notermans S (1989) Carbon assimilation and extracellular antigens of some yeast-like fungi. Antonie van Leeuwenhoek 55: 165–175PubMedGoogle Scholar
  33. Middelhoven WJ & Notermans S (1988) Species-specific extracellular antigen production by ascomycetous yeasts, detected by ELISA. J. Gen. Appl. Microbiol. 34: 15–26Google Scholar
  34. Middelhoven WJ, de Jong IM & de Winter M (1991)Arxula adeninivorans, a yeast assimilating many nitrogenous and aromatic compounds. Antonic van Leeuwenhoek 59: 129–137Google Scholar
  35. Middelhoven WJ, Koorevaar M & Schuur GW (1992a) Degradation of benzene compounds by yeasts in acidic soils. Plant and Soil 145: 37–43Google Scholar
  36. Middelhoven WJ, Coenen A, Kraakman B & Sollewijn Gelpke MD (1992b) Degradation of some phenols and hydroxybenzoates by the imperfect ascomycetous yeastsCandida parapsilosis andArxula adeninivorans: evidence for an operative gentisate pathway. Antonie van Leeuwenhoek 62: 181–187PubMedGoogle Scholar
  37. Mills C, Child JJ & Spencer JFT (1971) The utilization of aromatic compounds by yeasts. Antonie van Leeuwenhoek 37: 281–287PubMedGoogle Scholar
  38. Moore K, Subba Rao PV & Towers GHN (1968) Degradation of phenylalanine and tyrosine bySporobolomyces roseus. Biochem. J. 106: 507–514PubMedGoogle Scholar
  39. Mörsen A & Rehm H-J (1990) Degradation of phenol by a defined mixed culture immobilized by adsorption on activated carbon and sintered glass. Appl. Microbiol. Biotechnol. 33: 206–212Google Scholar
  40. Mörtberg M & Neujahr HY (1987) In situ and in vitro kinetics of phenol hydroxylase. Biochem. Biophys. Res. Commun. 146: 41–46PubMedGoogle Scholar
  41. Mörtberg & Neujahr (1988) Activation enthalpies and pH dependence of phenol hydroxylase fromTrichosporon cutaneum, in vitro and in situ. FEBS Letters 242: 75–78PubMedGoogle Scholar
  42. Neujahr HY & Gaal A (1973) Phenol hydroxylase from yeast. Purification and properties of the enzyme fromTrichosporon cutaneum. Europ. J. Biochem. 35: 386–400PubMedGoogle Scholar
  43. Neujahr HY & Gaal A (1975) Phenol hydroxylase from yeast. Sulfhydryl groups in phenol hydroxylase fromTrichosporon cutaneum. Europ. J. Biochem. 58: 351–357PubMedGoogle Scholar
  44. Neujahr HY & Kjellén KG (1978) Phenol hydroxylase from yeast. Reaction with phenol derivatives. J. Biol. Chem. 253: 8835–8841PubMedGoogle Scholar
  45. Neujahr HY & Kjellén KG (1980) Phenol hydroxylase from yeast. A lysyl residue essential for binding of reduced nicotinamide adenine dinucleotide phosphate. Biochemistry 19: 4967–4972PubMedGoogle Scholar
  46. Neujahr HY, Lindsjö S & Varga JM (1974) Oxidation of phenols by cells and cell-free extracts fromCandida tropicalis. Antonie van Leeuwenhoek 40: 209–216PubMedGoogle Scholar
  47. Neujahr HY & Varga JM (1970) Degradation of phenol by intact cells and cell-free preparations ofTrichosporon cutaneum. Europ. J. Biochem. 13: 37–44PubMedGoogle Scholar
  48. Powlowski JB & Dagley S (1985) β-Ketoadipate pathway inTrichosporon cutaneum modified for methyl-substituted metabolites. J. Bacteriol. 163: 1126–1135PubMedGoogle Scholar
  49. Powlowski JB, Ingebrand J & Dagley S (1985) Enzymology of the β-Ketoadipate pathway inTrichosporon cutaneum. J. Bacteriol. 163: 1136–1141PubMedGoogle Scholar
  50. Sahasrabudhe SR, Lala D & Modi VV (1986) Degradation of orcinol byAspergillus niger. Canad. J. Microbiol. 32: 535–538Google Scholar
  51. Sejlitz T & Neujahr HY (1987) Phenol hydroxylase from yeast. A model for phenol binding and an improved purification procedure. Europ. J. Biochem. 170: 343–349PubMedGoogle Scholar
  52. Skoda M & Udaka S (1980) Preferential utilization of phenol rather than glucose byTrichosporon cutaneum possessing a partially constitutive catechol-1,2-dioxygenase. Appl. Environm. Microbiol. 39: 1129–1133Google Scholar
  53. Spånning A & Neujahr HY (1987) Growth and enzyme synthesis during continuous growth ofTrichosporon cutaneum on phenol. Biotechnol. Bioengin. 29: 464–468Google Scholar
  54. Sparnins VL, Anderson JJ, Omans J & Dagley S (1978) Degradation of 4-phenylacetic acid byTrichosporon cutaneum. J. Bacteriol. 136: 449–451PubMedGoogle Scholar
  55. Sparnins VL, Burbee DG & Dagley S (1979) Catabolism of L-tyrosine inTrichosporon cutaneum. J. Bacteriol. 138: 425–430PubMedGoogle Scholar
  56. Subba Rao PV, Fritig B, Vose JR & Towers GHN (1971) An aromatic 3,4-dioxygenase fromTilletiopsis washingtonensis — oxidation of 3,4-dihydroxyphenylacetic acid to β-carboxymethylmuconolactone. Phytochemistry 10: 51–56Google Scholar
  57. Thatcher DR & Cain RB (1974) Metabolism of aromatic compounds by fungi. I. Purification and physical properties of 3-carboxy-cis-cis-muconate cyclase fromAspergillus niger. Europ. J. Biochem. 48: 549–556PubMedGoogle Scholar
  58. Utkin LM (1950) Homogentisic acid in the metabolism of molds. Biokhymia 15: 330–333Google Scholar
  59. Varga JM & Neujahr HY (1970) Isolation from soil of phenolutilizing organisms and metabolic studies on the pathway of phenol degradation. Plant and Soil 33: 565–571Google Scholar
  60. Walker N (1973) Metabolism of chlorophenols byRhodotorula glutinis. Soil Biol. Biochem. 5: 525–530Google Scholar
  61. Yang RD & Humphrey AE (1975) Dynamic and steady state studies of phenol degradation in pure and mixed cultures. Biotechnol. Bioengin. 17: 1211–1235Google Scholar
  62. Zimmermann R (1958) Ueber phenolspaltende Hefen. Naturwissenschaften 45: 165Google Scholar

Copyright information

© Kluwer Academic Publishers 1993

Authors and Affiliations

  • Wouter J. Middelhoven
    • 1
  1. 1.Department of MicrobiologyWageningen Agricultural UniversityWageningenThe Netherlands

Personalised recommendations