Skip to main content
SpringerLink
Log in

Microbial degradation of nonylphenol and other alkylphenols—our evolving view

  • Mini Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Because the endocrine disrupting effects of nonylphenol (NP) and octylphenol became evident, the degradation of long-chain alkylphenols (AP) by microorganisms was intensively studied. Most NP-degrading bacteria belong to the sphingomonads and closely related genera, while NP metabolism is not restricted to defined fungal taxa. Growth on NP and its mineralization was demonstrated for bacterial isolates, whereas ultimate degradation by fungi still remains unclear. While both bacterial and fungal degradation of short-chain AP, such as cresols, and the bacterial degradation of long-chain branched AP involves aromatic ring hydroxylation, alkyl chain oxidation and the formation of phenolic polymers seem to be preferential elimination pathways of long-chain branched AP in fungi, whereby both intracellular and extracellular oxidative enzymes may be involved. The degradation of NP by sphingomonads does not proceed via the common degradation mechanisms reported for short-chain AP, rather, via an unusual ipso-substitution mechanism. This fact underlies the peculiarity of long-chain AP such as NP isomers, which possess highly branched alkyl groups mostly containing a quaternary α-carbon. In addition to physicochemical parameters influencing degradation rates, this structural characteristic confers to branched isomers of NP a biodegradability different to that of the widely used linear isomer of NP. Potential biotechnological applications for the removal of AP from contaminated media and the difficulties of analysis and application inherent to the hydrophobic NP, in particular, are also discussed. The combination of bacteria and fungi, attacking NP at both the phenolic and alkylic moiety, represents a promising perspective.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ahel M, McEvoy J, Giger W (1993) Bioaccumulation of the lipophilic metabolites of nonionic surfactants in freshwater organisms. Environ Pollut 79:243–248

    CAS  PubMed  Google Scholar 

  • Ahn M-Y, Dec J, Kim J-E, Bollag J-M (2002) Treatment of 2,4-dichlorophenol polluted soil with free and immobilized laccase. J Environ Qual 31:1509–1515

    CAS  PubMed  Google Scholar 

  • Ajithkumar B, Ajithkumar VP, Iriye R (2003) Degradation of 4-amylphenol and 4-hexylphenol by a new activated sludge isolate of Pseudomonas veronii and proposal for a new subspecies status. Res Microbiol 154:17–23

    CAS  PubMed  Google Scholar 

  • Anderson JJ, Dagley S (1980) Catabolism of aromatic acids in Trichosporon cutaneum. J Bacteriol 141:534–543

    CAS  PubMed  PubMed Central  Google Scholar 

  • Auriol M, Filali-Meknassi Y, Tyagi RD, Adams CD, Surampalli RY (2006) Endocrine disrupting compounds removal from wastewater, a new challenge. Process Biochem 41:525–539

    CAS  Google Scholar 

  • Ayala M, Torres E (2004) Enzymatic activation of alkanes: constraints and prospective. Appl Catal A Gen 272:1–13

    CAS  Google Scholar 

  • Bertoni G, Bolognese F, Galli E, Barbieri P (1996) Cloning of the genes for and characterization of the early stages of toluene and o-xylene catabolism in Pseudomonas stutzeri OX1. Appl Environ Microbiol 62:3704–3711

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bollag J-M, Shuttleworth KL, Anderson DH (1988) Laccase-mediated detoxification of phenolic compounds. Appl Environ Microbiol 54:3086–3091

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bossert ID, Young LY (1986) Anaerobic oxidation of p-cresol by a denitrifying bacterium. Appl Environ Microbiol 52:1117–1122

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bossert ID, Whited G, Gibson DT, Young LY (1989) Anaerobic oxidation of p-cresol mediated by a partially purified methylhydroxylase from a denitrifying bacterium. J Bacteriol 171:2956–2962

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bumpus J, Tien M, Wright D, Aust S (1985) Oxidation of persistent environmental pollutants by a white rot fungus. Science 228:1434–1436

    CAS  PubMed  Google Scholar 

  • Buswell JA (1975) Metabolism of phenol and cresols by Bacillus stearothermophilus. J Bacteriol 124:1077–1083

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chang BV, Yang CM, Cheng CH, Yuan SY (2004a) Biodegradation of phthalate esters by two bacteria strains. Chemosphere 55:533–538

    CAS  PubMed  Google Scholar 

  • Chang BV, Yu CH, Yuan SY (2004b) Degradation of nonylphenol by anaerobic microorganisms from river sediment. Chemosphere 55:493–500

    CAS  PubMed  Google Scholar 

  • Chang BV, Chiang F, Yuan SY (2005a) Anaerobic degradation of nonylphenol in sludge. Chemosphere 59:1415–1420

    CAS  PubMed  Google Scholar 

  • Chang BV, Chiang F, Yuan SY (2005b) Biodegradation of nonylphenol in sewage sludge. Chemosphere 60:1652–1659

    CAS  PubMed  Google Scholar 

  • Chapman PJ, Hopper DJ (1968) The bacterial metabolism of 2,4-xylenol. Biochem J 110:491–498

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cirja M, Ivashechkin P, Schäffer A, Pinnekamp J, Ostrowski R, Corvini PFX (2005) Optimization of a lab-scale membrane bioreactor designed for fate studies of radio-labelled hydrophobic micropollutants during the wastewater treatment. E-proceedings of the emerging pollutants and emerging technologies—National Young Researchers Conference of the International Water Association, 27–28 October 2005, Aachen, Germany

  • Coldham NG, Sivapathasundaram S, Dave M, Ashfield LA, Pottinger TG, Goodall C, Sauer MJ (1998) Biotransformation, tissue distribution, and persistence of 4-nonylphenol residues in juvenile rainbow trout (Oncorhynchus mykiss). Drug Metab Dispos 26:347–354

    CAS  PubMed  Google Scholar 

  • Corti A, Frassinetti S, Vallini G, D’Antone S, Fichi C, Solaro R (1995) Biodegradation of nonionic surfactants. I. Biotransformation of 4-(1-nonyl)phenol by a Candida maltosa isolate. Environ Pollut 90:83–87

    CAS  PubMed  Google Scholar 

  • Corvini PFX, Meesters RJW, Schäffer A, Schröder HFr, Vinken R, Hollender J (2004a) Degradation of a nonylphenol single isomer by Sphingomonas sp. strain TTNP3 leads to a hydroxylation-induced migration product. Appl Environ Microbiol 70:6897–6900

    CAS  PubMed  PubMed Central  Google Scholar 

  • Corvini PFX, Vinken R, Hommes G, Mundt M, Meesters R, Schröder HF, Hollender J, Schmidt B (2004b) Microbial degradation of a single branched isomer of nonylphenol by Sphingomonas TTNP3. Water Sci Technol 50:195–202

    Google Scholar 

  • Corvini PFX, Vinken R, Hommes G, Schmidt B, Dohmann M (2004c) Degradation of the radioactive and non-labelled branched 3′,5′-dimethyl 3′-heptyl-phenol nonylphenol isomer by Sphingomonas TTNP3. Biodegradation 15:9–18

    CAS  PubMed  Google Scholar 

  • Corvini PFX, Elend M, Hollender J, Ji R, Preiss A, Vinken R, Schäffer A (2005) Metabolism of 4(2′,6′-dimethyl-2′-heptyl)-phenol by Sphingomonas sp. strain TTNP3. Environ Chem Lett 2:185–189

    CAS  Google Scholar 

  • Corvini PFX, Hollender J, Ji R, Schumacher S, Prell J, Hommes G, Priefer U, Vinken R, Schäffer A (2006a) The degradation of α-quaternary nonylphenol isomers by Sphingomonas sp. strain TTNP3 involves a type II ipso-substitution mechanism. Appl Microbiol Biotechnol 70:114–122

    CAS  PubMed  Google Scholar 

  • Corvini PFX, Meesters R, Mundt M, Schäffer A, Schmidt B, Schröder HFr, Verstraete W, Vinken R, Hollender J (2006b) Contribution to the detection and identification of oxidation metabolites of nonylphenol in Sphingomonas sp. strain TTNP3. Biodegradation (in press)

  • Craft DL, Madduri KM, Eshoo M, Wilson CR (2003) Identification and characterization of the CYP52 family of Candida tropicalis ATCC 20336, important for the conversion of fatty acids and alkanes to á,ω-dicarboxylic acids. Appl Environ Microbiol 69:5983–5991

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dachs J, Van Ry DA, Eisenreich SJ (1999) Occurrence of estrogenic nonylphenols in the urban and coastal atmosphere of the lower Hudson River estuary. Environ Sci Technol 33:2676–2679

    CAS  Google Scholar 

  • Darby JM, Taylor DG, Hopper DJ (1987) Hydroquinone as the ring-fission substrate in the catabolism of 4-ethylphenol and 4-hydroxyacetophenone by Pseudomonas putida JD1. J Gen Microbiol 133:2137–2146

    CAS  Google Scholar 

  • Dec J, Haider K, Bollag J (2003) Release of substituents from phenolic compounds during oxidative coupling reactions. Chemosphere 52:549–556

    CAS  PubMed  Google Scholar 

  • de Vries YP, Takahara Y, Ikunaga Y, Ushiba Y, Hasegawa M, Kasahara Y, Shimomura H, Hayashi S, Hirai Y, Ohta H (2001) Organic nutrient-dependent degradation of branched nonylphenol by Sphingomonas sp. YT isolated from a river sediment sample. Microbes Environ 16:240–249

    Google Scholar 

  • Di Corcia A, Costantino A, Crescenzi C, Marinoni E, Samperi R (1998) Characterization of recalcitrant intermediates of the branched alkyl side chain of nonylphenol ethoxylate surfactants. Environ Sci Technol 32:2401–2409

    Google Scholar 

  • Dittmann J, Heyser W, Bucking H (2002) Biodegradation of aromatic compounds by white rot and ectomycorrhizal fungal species and the accumulation of chlorinated benzoic acid in ectomycorrhizal pine seedlings. Chemosphere 49:297–306

    CAS  PubMed  Google Scholar 

  • Doerge DR, Twaddle NC, Churchwell MI, Chang HC, Newbold RR, Delclos KB (2002) Mass spectrometric determination of p-nonylphenol metabolism and disposition following oral administration to sprague–dawley rats. Reprod Toxicol 16:45–56

    CAS  PubMed  Google Scholar 

  • Dubroca J, Brault A, Kollmann A, Touton I, Jolivalt G, Kerhoas L, Mougin C (2005) Biotransformation of nonylphenol surfactants in soils amended with contaminated sewage sludges. In: Lichtfouse E, Dudd S, Robert D (eds) Environmental chemistry: green chemistry and pollutants in ecosystems. Springer, Berlin Heidelberg New York, pp 305–315

    Google Scholar 

  • Duran N, Esposito E (2000) Potential applications of oxidative enzymes and phenoloxidase-like compounds in wastewater and soil treatment: a review. Appl Catal B Environ 28:83–99

    CAS  Google Scholar 

  • Eggert C, Temp U, Dean J, Eriksson K (1996) A fungal metabolite mediates degradation of non-phenolic lignin structures and synthetic lignin by laccase. FEBS Lett 391:144–148

    CAS  PubMed  Google Scholar 

  • Ekelund R, Bergmanb Å, Granmo Å, Berggren M (1990) Bioaccumulation of 4-nonylphenol in marine animals—a re-evaluation. Environ Pollut 64:107–120

    CAS  PubMed  Google Scholar 

  • Ekelund R, Granmo Å, Magnusson K, Berggren M (1993) Biodegradation of 4-nonylphenol in seawater and sediment. Environ Pollut 79:59–61

    CAS  PubMed  Google Scholar 

  • Espadaler I, Caixach J, Om J, Ventura F, Cortina M, Pauné F, Rivera J (1997) Identification of organic pollutants in Ter river and its system of reservoirs supplying water to Barcelona (Catalonia, Spain): a study by GC/MS and FAB/MS. Water Res 31:1996–2004

    CAS  Google Scholar 

  • Ewers J, Rubio MA, Knackmuss HJ, Freier-Schröder D (1989) Bacterial metabolism of 2,6-xylenol. Appl Environ Microbiol 55:2904–2908

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fedorak PM, Westlake DWS (1986) Fungal metabolism of n-alkylbenzenes. Appl Environ Microbiol 51:435–437

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ferreira-Leach AM, Hill EM (2001) Bioconcentration and distribution of 4-tert-octylphenol residues in tissues of the rainbow trout (Oncorhynchus mykiss). Mar Environ Res 51:75–89

    CAS  PubMed  Google Scholar 

  • Field JA, de Jong E, Feijoo-Costa G, de Bont JAM (1993) Screening for ligninolytic fungi applicable to the biodegradation of xenobiotics. Trends Biotechnol 11:44–49

    CAS  Google Scholar 

  • Fishman A, Tao Y, Wood TK (2004) Toluene 3-monooxygenase of Ralstonia pickettii PKO1 is a para-hydroxylating enzyme. J Bacteriol 186:3117–3123

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fraaije MW, van den Heuvel RHH, Roelofs JCAA, van Berkel WJH (1998) Kinetic mechanism of vanillyl-alcohol oxidase with short-chain 4-alkylphenols. Eur J Biochem 253:712–719

    CAS  PubMed  Google Scholar 

  • Fujii K, Urano N, Kimura S, Nomura Y, Karube I (2000a) Microbial degradation of nonylphenol in some aquatic environments. Fish Sci 66:44–48

    CAS  Google Scholar 

  • Fujii K, Urano N, Ushio H, Satomi M, Iida, H, Ushio-Sata N, Kimura S (2000b) Profile of a nonylphenol-degrading microflora and its potential for bioremedial applications. J Biochem 128:909–916

    CAS  PubMed  Google Scholar 

  • Fujii K, Urano N, Ushio H, Satomi M, Kimura S (2001) Sphingomonas cloacae sp. Nov., a nonylphenol-degrading bacterium isolated from wastewater of a sewage-treatment plant in Tokyo. Int J Syst Evol Microbiol 51:603–610

    CAS  PubMed  Google Scholar 

  • Fujii K, Yamamoto R, Tanaka T, Hirakawa T, Kikuchi S (2003) Potential of a new biotreatment: Sphingomonas cloacae S-3T degrades nonylphenol in industrial wastewater. J Ind Microbiol Biotech 30:531–535

    CAS  Google Scholar 

  • Furukawa H, Wieser M, Morita H, Sugio T, Nagasawa T (1999) Purification and characterization of vanillyl-alcohol oxidase of Byssochlamys fulva V107. J Biosci Bioeng 87:285–290

    CAS  PubMed  Google Scholar 

  • Gabriel FLP, Giger W, Guenther K, Kohler HPE (2005a) Differential degradation of nonylphenol isomers by Sphingomonas xenophaga Bayram. Appl Environ Microbiol 71:1123–1129

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gabriel FLP, Heidlberger A, Rentsch D, Giger W, Guenther K, Kohler HPE (2005b) A novel metabolic pathway for degradation of 4-nonylphenol environmental contaminants by Sphingomonasxenophaga Bayram. Ipso-hydroxylation and intramolecular rearrangement. J Biol Chem 280:15526–15533

    CAS  PubMed  Google Scholar 

  • Garcia-Pena I, Hernandez S, Auria R, Revah S (2005) Correlation of biological activity and reactor performance in biofiltration of toluene with the fungus Paecilomyces variotii CBS115145. Appl Environ Microbiol 71:4280–4285

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garzillo A, Colao M, Caruso C, Caporale C, Celletti D, Buonocore V (1998) Laccase from the white-rot fungus Trametes trogii. Appl Microbiol Biotechnol 49:545–551

    CAS  PubMed  Google Scholar 

  • Gianfreda L, Rao MA (2004) Potential of extra cellular enzymes in remediation of polluted soils: a review. Enzyme Microb Technol 35:339–354

    CAS  Google Scholar 

  • Gianfreda L, Xu F, Bollag J-M (1999) Laccases: a useful group of enzymes. Bioremediation J 3:1–26

    CAS  Google Scholar 

  • Giger W, Brunner PH, Schaffner C (1984) 4-nonylphenol in sewage-sludge-accumulation of toxic metabolites from nonionic surfactants. Science 225:623–625

    CAS  PubMed  Google Scholar 

  • Giger W, Ahel M, Koch M, Laubscher HU, Schaffner C, Schneider J (1987) Behaviour of alkylphenolpolyethoxylate surfactants and of nitrilotriacetate in sewage treatment. Water Sci Technol 19:449–460

    CAS  Google Scholar 

  • Granmo A, Ekelund R, Magnusson K et al (1989) Lethal and sublethal toxicity of 4-nonylphenol to the common mussel (Mytilus-edulis-l). Environ Pollut 59:115–127

    CAS  PubMed  Google Scholar 

  • Guenther K, Kleist E, Thiele B (2005) Estrogen-active nonylphenols from an isomer-specific viewpoint: a systematic numbering system and future trends. Anal Bioanal Chem 384(2):542–546

    PubMed  Google Scholar 

  • Günther K, Schlosser D, Fritsche W (1995) Phenol and cresol metabolism in Bacillus pumilis isolated from contaminated groundwater. J Basic Microbiol 35:83–92

    PubMed  Google Scholar 

  • Hammel KE (1995) Organopollutant degradation by ligninolytic fungi. In: Hammel KE, Young LY, Cerniglia CE (eds) Degradation of toxic organic chemicals. Wiley-Liss, New York, pp 331–346

    Google Scholar 

  • Hanne LF, Kirk LL, Appel SM, Narayan AD, Bains KK (1993) Degradation and induction specificity in actinomycetes that degrade p-nitrophenol. Appl Environ Microbiol 59:3505–3508

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harwood CS, Parales RE (1996) The β-ketoadipiate pathway and the biology of self-identity. Annu Rev Microbiol 50:553–590

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Heinaru E, Truu J, Stottmeister U, Heinaru A (2000) Three types of phenol and p-cresol catabolism in phenol- and p-cresol-degrading bacteria isolated from river water continuously polluted with phenolic compounds. FEMS Microbiol Ecol 31:195–205

    CAS  PubMed  Google Scholar 

  • Hesselsøe M, Jensen D, Skals K, Olesen T, Moldrup P Roslev P, Krog Mortensen G, Henriksen K (2001) Degradation of 4-nonylphenol in homogeneous and nonhomogeneous mixtures of soil and sewage sludge. Environ Sci Technol 35:3695–3700

    PubMed  Google Scholar 

  • Hofrichter M (2002) Review: lignin conversion by manganese peroxidase (MnP). Enzyme Microb Technol 30:454–466

    CAS  Google Scholar 

  • Hofrichter M, Scheibner K (1993) Utilization of aromatic compounds by the Penicillium strain Bi 7/2. J Basic Microbiol 33:227–232

    CAS  PubMed  Google Scholar 

  • Hofrichter M, Bublitz F, Fritsche W (1995) Cometabolic degradation of o-cresol and 2,6-dimethylphenol by Penicillium frequentans Bi 7/2. J Basic Microbiol 35:303–313

    CAS  PubMed  Google Scholar 

  • Hopper DJ (1978) Incorporation of [18O]water in the formation of p-hydroxybenzyl alcohol by the p-cresol methylhydroxylase from Pseudomonas putida. Biochem J 175:345–347

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hopper DJ, Chapman PJ (1970) Gentisic acid and its 3- and 4-methyl-substituted homologoues as intermediates in the bacterial degradation of m-cresol, 3,5-xylenol and 2,5-xylenol. Biochem J 122:19–28

    Google Scholar 

  • Hopper DJ, Cottrell L (2003) Alkylphenol biotransformations catalyzed by 4-ethylphenol methylenehydroxylase. Appl Environ Microbiol 69:3650–3652

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hopper DJ, Taylor DG (1975) Pathways for the degradation of m-cresol and p-cresol by Pseudomonas putida. J Bacteriol 122:1–6

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hopper DJ, Bossert ID, Rhodes-Roberts ME (1991) p-Cresol methylhydroxylase from a denitrifying bacterium involved in anaerobic degradation of p-cresol. J Bacteriol 173:1298–1301

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hughes EJ, Bayly RC (1983) Control of catechol meta-cleavage pathway in Alcaligenes eutrophus. J Bacteriol 154:1363–1370

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hughes EJ, Bayly RC, Skurray RA (1984) Evidence for isofunctional enzymes in the degradation of phenol, m- and p-toluate, and p-cresol via catechol meta-cleavage pathways in Alcaligenes eutrophus. J Bacteriol 158:79–83

    CAS  PubMed  PubMed Central  Google Scholar 

  • Inui H, Shiota N, Motoi Y, Ido Y, Inoue T, Kodama T, Ohkawa Y, Okhawa H (2001) Metabolism of herbicides and other chemicals in human cytochrome P450 species and in transgenic potato plants co-expressing human CYP1A1, CYP2B6 and CYP2C19. J Pestic Sci 26:28–40

    CAS  Google Scholar 

  • Ivashechkin P, Corvini P, Dohmann M (2004) Behaviour of endocrine disrupting chemicals during the treatment of municipal sewage sludge. Water Sci Technol 50:141–147

    Google Scholar 

  • Jaspers MCM, Suske WA, Schmid A, Goslings DAM, Kohler HPE, van der Meer JR (2000) HbpR, a new member of the XylR/DmpR subclass within the NtrC family of bacterial transcriptional activators, regulates expression of 2-hydroxybiphenyl metabolism in Pseudomonas azelaica HBP1. J Bacteriol 182:405–417

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jeong JJ, JH Kim, Kim CK, Hwang I, Lee K (2003) 3- and 4-alkylphenol degradation pathway in Pseudomonas sp. strain KL28: genetic organization of the lap gene cluster and substrate specificities of phenol hydroxylase and catechol 2,3-dioxygenase. Microbiology 149:3265–3277

    CAS  PubMed  Google Scholar 

  • Jigami Y, Omori T, Minoda Y, Yamada K (1974) Screening of n-alkylbenzene assimilating yeasts and identification of oxidation products from n-alkylbenzenes. Agric Biol Chem (Tokyo) 38:401–408

    CAS  Google Scholar 

  • Johannes C, Majcherczyk A (2000) Natural mediators in the oxidation of polycyclic aromatic hydrocarbons by laccase mediator systems. Appl Environ Microbiol 66:524–528

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jones KH, Trudgill PW, Hopper DJ (1993) Metabolism of p-cresol by the fungus Aspergillus fumigatus. Appl Environ Microbiol 59:1125–1130

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jones KH, Trudgill PW, Hopper DJ (1994) 4-Ethylphenol metabolism by Aspergillus fumigatus. Appl Environ Microbiol 60:1978–1983

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jonkers N, Knepper TP, de Voogt P (2001) Aerobic biodegradation studies of nonylphenol ethoxylates in river water using liquid chromatography–electrospray tandem mass spectrometry. Environ Sci Technol 35:335–40

    CAS  PubMed  Google Scholar 

  • Junghanns C, Moeder M, Krauss G, Martin C, Schlosser D (2005) Degradation of the xenoestrogen nonylphenol by aquatic fungi and their laccases. Microbiology 151:45–57. DOI 10.1099/mic.0.27431-0

    CAS  PubMed  Google Scholar 

  • Kahng HY, Malinverni JC, Majko MM, Kukor JJ (2001) Genetic and functional analysis of the tbc operons for catabolism of alkyl- and chloroaromatic compounds in Burkholderia sp. strain JS150. Appl Environ Microbiol 67:4805–4816

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kamada F, Abe S, Hiratsuka N, Wariishi H, Tanaka H (2002) Mineralization of aromatic compounds by brown-rot basidiomycetes-mechanisms involved in initial attack on the aromatic ring. Microbiology 148:1939–1946

    CAS  PubMed  Google Scholar 

  • Kamerbeek NM, Moonen MJH, van der Ven JGM, van Berkel WJH, Fraaije MW, Janssen DB (2001) 4-Hydroxyacetophenone monooxygenase from Pseudomonas fluorescens ACB. A novel flavoprotein catalyzing Baeyer–Villiger oxidation of aromatic compounds. Eur J Biochem 268:2547–2557

    CAS  PubMed  Google Scholar 

  • Keat MJ, Hopper DJ (1978a) p-Cresol and 3,5-xylenol methylhydroxylases in Pseudomonas putida N.C.I.B. 9896. Biochem J 175:649–658

    CAS  PubMed  PubMed Central  Google Scholar 

  • Keat MJ, Hopper DJ (1978b) The aromatic alcohol dehydrogenases in Pseudomonas putida N.C.I.B. 9869 grown on 3,5-xylenol and p-cresol. Biochem J 175:659–667

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kennes C, Lema JM (1994) Simultaneous biodegradation of p-cresol and phenol by the basidiomycete Phanerochaete chrysosporium. J Ind Microbiol 13:311–314

    CAS  PubMed  Google Scholar 

  • Kim YS, Katase T, Sekine S, Inoue T, Makino M, Uchiyama T, Fujimoto T, Yamashita M (2004) Variation in estrogenic activity among fractions of a commercial nonylphenol by high performance liquid chromatography. Chemosphere 54:1127–1134

    CAS  PubMed  Google Scholar 

  • Kimura M, Michizoe J, Oakazaki S, Furusaki S, Goto M, Tanaka H, Wariishi H (2004) Activation of lignin peroxidase in organic media by reversed micelles. Biotechnol Bioeng 88:495–501

    CAS  PubMed  Google Scholar 

  • Kitazume T, Takaya N, Nakayama N, Shoun H (2000) Fusarium oxysporum fatty-acid subterminal hydroxylase (CYP505) is a membrane-bound eukaryotic counterpart of Bacillus megaterium cytochrome P450BM3. J Biol Chem 275:39734–39740

    CAS  PubMed  Google Scholar 

  • Kobayashi S, Higashimura H (2003) Oxidative polymerization of phenols revisited. Prog Polym Sci 28:1015–1048

    CAS  Google Scholar 

  • Kohler HPE, van der Maarel MJEC, Kohler-Staub D (1993) Selection of Pseudomonas sp. strain HBP1 Prp for metabolism of 2-propylphenol and elucidation of the degradative pathway. Appl Environ Microbiol 59:860–866

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kollmann A, Brault A, Touton I, Dubroca J, Chaplain V, Mougin C (2003) Effect of nonylphenol surfactants on fungi following the application of sewage sludge on agricultural soils. J Environ Qual 32:1269–1276

    CAS  PubMed  Google Scholar 

  • Kottermann MJJ, Vis EH, Field JA (1998) Successive mineralization and detoxification of benzo[a]pyrene by the white-rot fungus Bjerkandera sp. strain BOS55 and indigenous microflora. Appl Environ Microbiol 64:2853–2858

    Google Scholar 

  • Kuhn EP, Zeyer J, Eicher P, Schwarzenbach RP (1988) Anaerobic degradation of alkylated benzenes in denitrifying laboratory aquifer columns. Appl Environ Microbiol 54:490–496

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kukor JJ, Olsen RH (1991) Genetic organization and regulation of a meta cleavage pathway for catechols produced from catabolism of toluene, benzene, phenol, and cresols by Pseudomonas pickettii PKO1. J Bacteriol 173:4587–4594

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lalah J, Schramm KW, Lenoir D, Henkelmann B, Hertkorn N, Matuschek G, Kettrup A, Gunther K (2001) Regioselective synthesis of a branched isomer of nonylphenol,4-(3′,6′-dimethyl-3′-heptyl)phenol, and determination of its important environmental properties. Chemistry 7:4790–4795

    CAS  PubMed  Google Scholar 

  • Lalah J, Behechti A, Severin G, Lenoir D, Gunther K, Kettrup A, Schramm K (2003a) The bioaccumulation and fate of a branched 14c-p-nonylphenol isomer in Lymnaea stagnalis L. Environ Toxicol Chem 22:1428–1436

    CAS  PubMed  Google Scholar 

  • Lalah J, Schramm K, Severin G, Lenoir D, Henkelmann B, Behechti A, Guenther K, Kettrup A (2003b) In vivo metabolism and organ distribution of a branched 14C-nonylphenol isomer in pond snails, Lymnaea stagnalis L. Aquat Toxicol 62:305–319

    CAS  PubMed  Google Scholar 

  • Lalah JO, Schramm KW, Henkelmann B, Lenoir D, Behechti A, Gunther K, Kettrup A (2003c) The dissipation, distribution and fate of a branched 14C-nonylphenol isomer in lake water/sediment systems. Environ Pollut 122:195–203

    CAS  PubMed  Google Scholar 

  • Leahy JG, Batchelor PJ, Morcomb SM (2003) Evolution of the soluble diiron monooxygenases. FEMS Microbiol Rev 27:449–479

    CAS  PubMed  Google Scholar 

  • Leonowicz A, Cho N, Luterek J, Wilkolazka A, Wojtas-Wasilewska M, Matuszewska A, Hofrichter M, Wesenberg D, Rogalski J (2001) Fungal laccase: properties and activity on lignin. J Basic Microbiol 41:185–227

    CAS  PubMed  Google Scholar 

  • Liber K, Knuth ML, Stay FS (1999) An integrated evaluation of the persistence and effects of 4-nonylphenol in an experimental littoral ecosystem. Environ Toxicol Chem 18:357–362

    CAS  Google Scholar 

  • Liers C, Ullrich R, Steffen K, Hatakka A, Hofrichter M (2006) Mineralization of 14C-labelled synthetic lignin and extracellular enzyme activities of the wood-colonizing ascomycetes Xylaria hypoxylon and Xylaria polymorpha. Appl Microbiol Biotechnol 69:573–579

    CAS  PubMed  Google Scholar 

  • Martinez AT (2002) Molecular biology and structure–function of lignin-degrading heme peroxidases. Enzyme Microb Technol 30:425–444

    CAS  Google Scholar 

  • Matsuzaki F, Wariishi H (2004) Functional diversity of cytochrome P450s of the white-rot fungus Phanerochaete chrysosporium. Biochem Biophys Res Commun 324:387–393

    CAS  PubMed  Google Scholar 

  • Mayer AM, Staples RC (2002) Laccase: new functions for an old enzyme. Phytochemistry 60:551–565

    CAS  PubMed  Google Scholar 

  • McIntire W, Hopper DJ, Craig JC, Everhart ET, Webster RV, Causer MJ, Singer TP (1984) Stereochemistry of 1-(4′-hydroxyphenyl)ethanol produced by hydroxylation of 4-ethylphenol by p-cresol methylhydroxylase. Biochem J 224:617–621

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meldahl AC, Nithipatikom K, Lech JJ (1996) Metabolism of several 14C-nonylphenol isomers by rainbow trout (Oncorhynchus mykiss): in vivo and in vitro microsomal metabolites. Xenobiotica 26:1167–1180

    CAS  PubMed  Google Scholar 

  • Mester T, Tien M (2000) Oxidation mechanism of ligninolytic enzymes involved in the degradation of environmental pollutants. Int Biodeterior Biodegrad 46:51–59

    CAS  Google Scholar 

  • Meyer A, Schmid A, Held M, Westphal AH, Röthlisberger M, Kohler HPE, van Berkel WJH, Witholt B (2002) Changing the substrate reactivity of 2-hydroxybiphenyl 3-monooxygenase from Pseudomonas azelaica HBP1 by directed evolution. J Biol Chem 277:5575–5582

    CAS  PubMed  Google Scholar 

  • Meyer A, Held M, Schmid A, Kohler HPE, Witholt B (2003) Synthesis of 3-tert-butylcatechol by an engineered monooxygenase. Biotechnol Bioeng 81:518–524

    CAS  PubMed  Google Scholar 

  • Middelhoven WJ (1993) Catabolism of benzene compounds by ascomycetous and basidiomycetous yeasts and yeastlike fungi. A literature review and an experimental approach. Antonie Van Leeuwenhoek 63:125–144

    CAS  PubMed  Google Scholar 

  • Middelhoven WJ, Spaaij F (1997) Rhodotorula cresolica sp. Nov., a cresol-assimilating yeast species isolated from soil. Int J Syst Bacteriol 47:324–327

    CAS  PubMed  Google Scholar 

  • Middelhoven WJ, Scorzetti G, Fell JW (2000) Trichosporon veenhuisii sp. Nov., an alkane-assimilating anamorphic basidiomycetous yeast. Int J Syst Evol Microbiol 50:381–387

    CAS  PubMed  Google Scholar 

  • Middelhoven WJ, Scorzetti G, Fell JW (2004) Systematics of the anamorphic basidiomycetous yeast genus Trichosporon Behrend with the description of five novel species: Trichosporon vadense, T. smithiae, T. dehoogii, T. scarabaeorum and T. gamsii. Int J Syst Evol Microbiol 54:975–986

    CAS  PubMed  Google Scholar 

  • Moeder M, Schrader S, Winkler M, Popp P (2000) Solid-phase microextraction-gas chromatography-mass spectrometry of biologically active substances in water samples. J Chromatogr A 873:95–106

    CAS  PubMed  Google Scholar 

  • Moeder M, Martin C, Harynuk J, Górecki T, Vinken R, Corvini PFX (2006a) Identification of isomeric 4-nonylphenol structures by gas chromatography-tandem mass spectrometry combined with cluster analysis. J Chromatogr A 1102:245–255

    CAS  PubMed  Google Scholar 

  • Moeder M, Martin C, Schlosser D, Harynuk J, Gorecki T (2006b) Separation of technical 4-nonylphenols and their biodegradation products by comprehensive two-dimensional gas chromatography coupled to time-of-flight mass spectrometry. J Chromatogr A 1107:233–239

    CAS  PubMed  Google Scholar 

  • Mogensen AS, Haagensen F, Ahring BK (2003) Anaerobic degradation of linear alkylbenzene sulfonate. Environ Toxicol Chem 22:706–711

    CAS  PubMed  Google Scholar 

  • Montgomery-Brown J, Drewes JE, Fox P, Reinhard M (2003) Behavior of alkylphenol polyethoxylate metabolites during soil aquifer treatment. Water Res 37:3672–3681

    CAS  PubMed  Google Scholar 

  • Morimoto K, Tatsumi K (1997) Effect of humic substances on the enzymatic formation of OCDD from PCP. Chemosphere 34:1277–1283

    CAS  Google Scholar 

  • Müller JA, Galushko AS, Kappler A, Schink B (2001) Initiation of anaerobic degradation of p-cresol by formation of 4-hydroxybenzylsuccinate in Desulfobacterium cetonicum. J Bacteriol 183:752–757

    PubMed  PubMed Central  Google Scholar 

  • Nakayama N, Shoun H (1994) Fatty acid hydroxylase of the fungus Fusarium oxysporum is possibly a fused protein of cytochrome P-450 and its reductase. Biochem Biophys Res Commun 202:586–590

    CAS  PubMed  Google Scholar 

  • Nakayama N, Takemae A, Shoun H (1996) Cytochrome P450foxy, a catalytically self-sufficient fatty acid hydroxylase of the fungus Fusarium oxysporum. J Biochem (Tokyo) 119:435–440

    CAS  Google Scholar 

  • Neujahr HY, Kjellen KG (1978) Phenol hydroxylase from yeast. Reaction with phenol derivatives. J Biol Chem 253:8835–8841

    CAS  PubMed  Google Scholar 

  • Öberg LG, Glas B, Swanson SE, Rappe C, Paul KG (1990) Peroxidase-catalyzed oxidation of chlorophenols to polychlorinated dibenzo-p-dioxins and dibenzofurans. Arch Environ Contam Toxicol 19:930–938

    PubMed  Google Scholar 

  • Olsen RH, Kukor JJ, Kaphammer B (1994) A novel toluene-3-monooxygenase pathway cloned from Pseudomonas pickettii. J Bacteriol 176:3749–3756

    CAS  PubMed  PubMed Central  Google Scholar 

  • Osburn QW, Benedict JH (1966) Polyethoxylated alkyl phenols: Relationship of structure to biodegradation mechanism. J Am Oil Chem Soc 43:141–146

    CAS  Google Scholar 

  • Park J, Dec J, Kim J, Bollag J (2000) Dehalogenation of xenobiotics as a consequence of binding to humic materials. Arch Environ Contam Toxicol 38:405–410

    CAS  PubMed  Google Scholar 

  • Pavel H, Forsman M, Shingler V (1994) An aromatic effector specificity mutant of the transcriptional regulator DmpR overcomes the growth constraints of Pseudomonas sp. strain CF600 on para-substituted methylphenols. J Bacteriol 176:7550–7557

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pedersen RT, Hill EM (2000a) Identification of novel metabolites of the xenoestrogen 4-tert-octylphenol in primary rat hepatocytes. Chem Biol Interact 128:189–209

    CAS  PubMed  Google Scholar 

  • Pedersen RT, Hill EM (2000b) Biotransformation of the xenoestrogen 4-tert-octylphenol in hepatocytes of rainbow trout (Oncorhynchus mykiss). Xenobiotica 30:867–879

    CAS  PubMed  Google Scholar 

  • Pedersen RT, Hill EM (2002) Tissue distribution and depuration of 4-tert-octylphenol residues in the cyprinid fish, Scardinius erythrophthalmus. Environ Sci Technol 36:3275–3283

    CAS  PubMed  Google Scholar 

  • Perron N, Welander U (2004) Degradation of phenol and cresols at low temperatures using a suspended-carrier biofilm process. Chemosphere 55:45–50

    CAS  PubMed  Google Scholar 

  • Poh CL, Bayly RC (1980) Evidence for isofunctional enzymes used in m-cresol and 2,5-xylenol degradation via the gentisate pathway in Pseudomonas alcaligenes. J Bacteriol 143:59–69

    CAS  PubMed  PubMed Central  Google Scholar 

  • Powlowski JB, Dagley S (1985) Beta-ketoadipate pathway in Trichosporon cutaneum modified for methyl-substituted metabolites. J Bacteriol 163:1126–1135

    CAS  PubMed  PubMed Central  Google Scholar 

  • Powlowski J, Shingler V (1994) Genetics and biochemistry of phenol degradation by Pseudomonas sp. CF600. Biodegradation 5:219–236

    CAS  PubMed  Google Scholar 

  • Preuss TG, Coors A, Jones PD, Giesy JP, Ratte HT (2004) Estrogenic potency of defined nonylphenol isomers. 2nd joint annual meeting of the Society of Environmental Toxicology and Chemistry German Language Branch e.V. and the German Chemical Society Division of Environmental Chemistry and Ecotoxicology, 6–8 October 2004, Aachen, Germany

  • Pryor SW, Hay AG, Walker LP (2002) Nonylphenol in anaerobically digested sewage sludge from New York state. Environ Sci Technol 36:3678–3682

    CAS  PubMed  Google Scholar 

  • Razo-Flores E, Donlon B, Field J, Lettinga G (1996) Biodegradability of N-substituted aromatics and alkylphenols under methanogenic conditions using granular sludge. Water Sci Technol 33:45–57

    Google Scholar 

  • Reddy CA (1995) The potential for white-rot fungi in the treatment of pollutants. Curr Opin Biotechnol 6:320–328

    CAS  Google Scholar 

  • Reeve CD, Carver MA, Hopper DJ (1989) The purification and characterisation of 4-ethylphenol methylenehydroxylase, a flavocytochrome from Pseudomonas putida JD1. Biochem J 263:431–437

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reeve CD, Carver MA, Hopper DJ (1990) Stereochemical aspects of the oxidation of 4-ethylphenol by the bacterial enzyme 4-ethylphenol methylenehydroxylase. Biochem J 269:815–819

    CAS  PubMed  PubMed Central  Google Scholar 

  • Romine MF, Stillwell LC, Wong KK, Thurston SJ, Sisk EC, Sensen C, Gaasterland T, Fredrickson JK, Saffer JD (1999) Complete sequence of a 184-kilobase catabolic plasmid from Sphingomonas aromaticivorans F199. J Bacteriol 181:1585–1602

    CAS  PubMed  PubMed Central  Google Scholar 

  • Routledge EJ, Sumpter JP (1997) Structural features of alkylphenolic chemicals associated with estrogenic activity. J Biol Chem 272:3280–3288

    CAS  PubMed  Google Scholar 

  • Ruß AS, Vinken R, Schuphan I, Schmidt B (2005) Synthesis of branched para-nonylphenol isomers: occurrence and quantification in two commercial mixtures. Chemosphere 60:1624–1635

    PubMed  Google Scholar 

  • Ryan DR, Leukes WD, Burton SG (2005) Fungal bioremediation of phenolic wastewaters in an airlift reactor. Biotechnol Prog 21:1068–1074

    CAS  PubMed  Google Scholar 

  • Sack U, Heinze T, Deck J, Cerniglia C, Martens R, Zadrazil F, Fritsche W (1997) Comparison of phenanthrene and pyrene degradation by different wood-decaying fungi. Appl Environ Microbiol 63:3919–3925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Saito T, Hong P, Kato K, Okazaki M, Inagaki H, Maeda S, Yokogawa Y (2003) Purification and characterization of an extracellular laccase of a fungus (family Chaetomiaceae) isolated from soil. Enzyme Microb Technol 33:520–526

    CAS  Google Scholar 

  • Saito I, Onuki A, Seto H (2004a) Indoor air pollution by alkylphenols in Tokyo. Indoor Air 14:325–332

    CAS  PubMed  Google Scholar 

  • Saito T, Kato K, Yokogawa Y, Nishida M, Yamashita N (2004b) Detoxification of bisphenol A and nonylphenol by purified extracellular laccase from a fungus isolated from soil. J Biosci Bioeng 98:64–66

    CAS  PubMed  Google Scholar 

  • Sariaslani F, Harper D, Higgins I (1974) Microbial degradation of hydrocarbons. Catabolism of 1-phenylalkanes by Nocardia salmonicolor. Biochem J 140:31–45

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sarkar JM, Malcolm RL, Bollag JM (1988) Enzymatic coupling of 2,4-dichlorophenol to stream fulvic acid in the presence of oxidoreductases. Soil Sci Soc Am J 52:688–694

    CAS  Google Scholar 

  • Scheller U, Zimmer T, Becher D, Schauer F, Schunck W-H (1998) Oxygenation cascade in conversion of n-alkanes to alpha,omega-dioic acids catalyzed by cytochrome P450 52A3. J Biol Chem 273:32528–32534

    CAS  PubMed  Google Scholar 

  • Schlosser D, Höfer C (2002) Laccase-catalyzed oxidation of Mn2+ in the presence of natural Mn3+ chelators as a novel source of extracellular H2O2 production and its impact on manganese peroxidase. Appl Environ Microbiol 68:3514–3521

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt B, Patti H, Niewersch C, Schuphan I (2003) Biotransformation of [ring-U-14C]4-n-nonylphenol by Agrostemma githago cell culture in a two-liquid-phase system. Biotechnol Lett 25:1375–1381

    CAS  PubMed  Google Scholar 

  • Schmidt B, Patti H, Hommes G, Schuphan I (2004) Metabolism of the nonylphenol isomer [ring-U-14C]-4-(3′,5′-dimethyl-3′-heptyl)-phenol by cell suspension cultures of Agrostemma githago and soybean. J Environ Sci Health B Pestic Food Contam Agric Wastes 39:533–549

    Google Scholar 

  • Shields MS, Montgomery SO, Chapman PJ, Cuskey SM, Pritchard PH (1989) Novel pathway of toluene catabolism in the trichloroethylene degrading bacterium G4. Appl Environ Microbiol 55:1624–1629

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shields MS, Reagin MJ, Gerger RR, Campbell R, Somerville C (1995) TOM, a new aromatic degradative plasmid from Burkholderia (Pseudomonas) cepacia G4. Appl Environ Microbiol 61:1352–1356

    CAS  PubMed  PubMed Central  Google Scholar 

  • Soares A, Guieysse B, Delgado O, Mattiasson B (2003a) Aerobic biodegradation of nonylphenol by cold-adapted bacteria. Biotechnol Lett 25:731–738

    CAS  PubMed  Google Scholar 

  • Soares A, Guieysse B, Mattiasson B (2003b) Biodegradation of nonylphenol in a continuous packed-bed bioreactor. Biotechnol Lett 25:927–933

    CAS  PubMed  Google Scholar 

  • Soares A, Jonasson K, Terrazas E, Guieysse B, Mattiasson B (2005a) The ability of white-rot fungi to degrade the endocrine-disrupting compound nonylphenol. Appl Microbiol Biotechnol 66:719–725

    CAS  PubMed  Google Scholar 

  • Soares A, Murto M, Guieysse B, Mattiasson B (2005b) Biodegradation of nonylphenol in a continuous bioreactor at low temperatures and effects on the microbial population. Appl Microbiol Biotechnol 69(5):597–606

    PubMed  Google Scholar 

  • Soares A, Guieysse B, Mattiasson B (2006) Influence of agitation on the removal of nonylphenol by the white-rot fungi Trametes versicolor and Bjerkandera sp. BOL 13. Biotechnol Lett 28:139–143

    CAS  PubMed  Google Scholar 

  • Song B, Palleroni NJ, Haggblom MM (2000) Description of strain 3CB-1, a genomovar of Thauera aromatica, capable of degrading 3-chlorobenzoate coupled to nitrate reduction. Int J Syst Evol Microbiol 50:551–558

    CAS  PubMed  Google Scholar 

  • Soto AM, Justica H, Wray JW, Sonnenschein C (1991) Para-nonylphenol: an estrogenic xenobiotic released from polystyrene. Environ Health Perspect 92:167–173

    CAS  PubMed  PubMed Central  Google Scholar 

  • Staples CA, Naylor CG, Williams JB, Gledhill WE (2001) Ultimate biodegradation of alkylphenol ethoxylate surfactants and their biodegradation intermediates. Environ Toxicol Chem 20:2450–2455

    CAS  PubMed  Google Scholar 

  • Steffen K, Hatakka A, Hofrichter M (2002) Removal and mineralization of polycyclic aromatic hydrocarbons by litter-decomposing basidiomycetous fungi. Appl Microbiol Biotechnol 60:212–217

    CAS  PubMed  Google Scholar 

  • Stephanou E, Giger W (1982) Persistent organic-chemicals in sewage effluents. 2. Quantitative-determinations of nonylphenols and nonylphenol ethoxylates by glass-capillary gas chromatography. Environ Sci Technol 16:800–805

    CAS  PubMed  Google Scholar 

  • Sundaram KMS, Szeto S (1981) The dissipation of nonylphenol in stream and pond water under stimulated field conditions. J Environ Sci Health B16:767–776

    CAS  Google Scholar 

  • Tanaka T, Tonosaki T, Nose M, Tomidokoro N, Kadomura N, Fujii T, Taniguchi M (2001) Treatment of model soils contaminated with phenolic endocrine-disrupting chemicals with laccase from Trametes sp. in a rotating reactor. J Biosci Bioeng 92:312–316

    CAS  PubMed  Google Scholar 

  • Tanaka T, Nose M, Endo A, Fujii T, Taniguchi M (2003) Treatment of nonylphenol with laccase in a rotating reactor. J Biosci Bioeng 96:541–546

    CAS  PubMed  Google Scholar 

  • Tanghe T, Devriese G, Verstraete W (1998) Nonylphenol degradation in lab scale activated sludge units is temperature dependent. Water Res 32:2889–2896

    CAS  Google Scholar 

  • Tanghe T, Devriese G, Verstraete W (1999a) Nonylphenol and estrogenic activity in aquatic environmental samples. J Environ Qual 28:702–709

    CAS  Google Scholar 

  • Tanghe T, Dhooge W, Verstraete W (1999b) Isolation of a bacterial strain able to degrade branched nonylphenol. Appl Environ Microbiol 65:746–751

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tanghe T, Dhooge W, Verstraete W (2000) Formation of the metabolic intermediate 2,4,4-trimethyl-2-pentanol during incubation of a Sphingomonas sp. strain with the xeno-estrogenic octylphenol. Biodegradation 11:1–19

    Google Scholar 

  • Tanner A, Hopper DJ (2000) Conversion of 4-hydroxyacetophenone into 4-phenyl acetate by a flavin adenine dinucleotidecontaining Baeyer–Villiger-type monooxygenase. J Bacteriol 182:6565–6569

    CAS  PubMed  PubMed Central  Google Scholar 

  • Telscher MJ, Schuller U, Schmidt B, Schaffer A (2005) Occurrence of a nitro metabolite of a defined nonylphenol isomer in soil/sewage sludge mixtures. Environ Sci Technol 39:7896–7900

    CAS  PubMed  Google Scholar 

  • Thibaut R, Debrauwer L, Rao D, Cravedi J (1998) Characterization of biliary metabolites of 4-n-nonylphenol in rainbow trout (Oncorhynchus mykiss). Xenobiotika 28:745–757

    CAS  Google Scholar 

  • Thibaut R, Debrauwer L, Rao D, Cravedi JP (1999) Urinary metabolites of 4-n-nonylphenol in rainbow trout (Oncorhynchus mykiss). Sci Total Environ 233:193–200

    CAS  PubMed  Google Scholar 

  • Thibaut R, Debrauwer L, Perdu E, Goksoyr A, Cravedi JP, Arukwe A (2002a) Regio-specific hydroxylation of nonylphenol and the involvement of CYP2K- and CYP2M-like iso-enzymes in Atlantic salmon (Salmo salar). Aquat Toxicol 56:177–190

    CAS  PubMed  Google Scholar 

  • Thibaut R, Monod G, Cravedi JP (2002b) Residues of 14C-4-n-nonylphenol in mosquitofish (Gambusia holbrooki) oocytes and embryos during dietary exposure of mature females to this xenohormone. Mar Environ Res 54:685–689

    CAS  PubMed  Google Scholar 

  • Thiele B, Heinke V, Kleist E, Guenther K (2004) Contribution to the structural elucidation of 10 isomers of technical p-nonylphenol. Environ Sci Technol 38:3405–3411

    CAS  PubMed  Google Scholar 

  • Thurston CF (1994) The structure and function of fungal laccases. Microbiology 140:19–26

    CAS  Google Scholar 

  • Topp E, Starratt A (2000) Rapid mineralization of the endocrine-disrupting chemical 4-nonylphenol in soil. Environ Toxicol Chem 19:313–318

    CAS  Google Scholar 

  • Tschech A, Fuchs G (1987) Anaerobic degradation of phenol by pure cultures of newly isolated denitrifying pseudomonads. Arch Microbiol 148:213–217

    CAS  PubMed  Google Scholar 

  • Tsutsumi Y, Haneda T, Nishida T (2001) Removal of estrogenic activities of bisphenol A and nonylphenol by oxidative enzymes from lignin-degrading basidiomycetes. Chemosphere 42:271–276

    CAS  PubMed  Google Scholar 

  • Ushiba Y, Takahara Y, Ohta H (2003) Sphingobium amiense sp. Nov., a novel nonylphenol-degrading bacterium isolated from a river sediment. Int J Syst Evol Microbiol 53:2045–2048

    CAS  PubMed  Google Scholar 

  • Vallini G, Frassinetti S, Scorzetti G (1997) Candida aquaetextoris sp. Nov., a new species of yeast occurring in sludge from a textile industry wastewater treatment plant in Tuscany, Italy. Int J Syst Bacteriol 47:336–340

    CAS  PubMed  Google Scholar 

  • Vallini G, Frassinetti S, D’Andrea F, Catelani G, Agnolucci M (2001) Biodegradation of 4-(1-nonyl)phenol by axenic cultures of the yeast Candida aquaetextoris: identification of microbial breakdown products and proposal of a possible metabolic pathway. Int Biodeterior Biodegrad 47:133–140

    CAS  Google Scholar 

  • van Beilen JB, Funhoff EG (2005) Expanding the alkane oxygenase toolbox: new enzymes and applications. Curr Opin Biotechnol 16:308–314

    PubMed  Google Scholar 

  • van Beilen JB, Li Z, Duetz WA, Smits THM, Witholt B (2003) Diversity of alkane hydroxylase systems in the environment. Oil Gas Sci Technol 58:427–440

    Google Scholar 

  • van den Heuvel RHH, Fraaije MW, Laane C van Berkel WJH (1998) Regio- and stereospecific conversion of 4-alkylphenols by the covalent flavoprotein vanillyl-alcohol oxidase. J Bacteriol 180:5646–5651

    PubMed  PubMed Central  Google Scholar 

  • van den Heuvel RHH, Fraaije MW, Ferrer M, Mattevi A, van Berkel WJH (2000) Inversion of the stereospecificity of vanillyl-alcohol oxidase. Proc Natl Acad Sci U S A 97:9455–9460

    PubMed Central  Google Scholar 

  • Van Ginkel CG (1996) Complete degradation of xenobiotic surfactants by consortia of aerobic microorganisms. Biodegradation 7:151–164

    CAS  PubMed  Google Scholar 

  • Vares T, Niemenmaa O, Hatakka A (1994) Secretion of ligninolytic enzymes and mineralization of 14C-ring-labelled synthetic lignin by three Phlebia tremellosa strains. Appl Environ Microbiol 60:569–575

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vinken R, Schmidt B, Schäffer A (2002) Synthesis of tertiary 14C-labelled nonylphenol isomers. J Label Compd Radiopharm 45:1253–1263

    CAS  Google Scholar 

  • Vinken R, Höllrigl-Rosta A, Schmidt B, Schäffer A, Corvini PFX (2004) Bioavailability of a nonylphenol isomer in dependence on the association to dissolved humic substances. Water Sci Technol 50:285–291

    Google Scholar 

  • Watanabe K, Futamata H, Harayama S (2002) Understanding the diversity in catabolic potential of microorganisms for the development of bioremediation strategies. Antonie Van Leeuwenhoek 81:655–663

    CAS  PubMed  Google Scholar 

  • Webster J (1992) Anamorph–teleomorph relationships. In: Bärlocher F (ed) The ecology of aquatic hyphomycetes. Springer, Berlin Heidelberg New York, pp 99–117

    Google Scholar 

  • Wheeler TF, Heim JR, LaTorre MR, Janes B (1997) Mass spectral characterization of p-nonylphenol isomers using high-resolution capillary GC-MS. J Chromatogr Sci 35:19–30

    CAS  Google Scholar 

  • Whited GM, Gibson DT (1991) Toluene-4-monooxygenase, as three-component enzyme system that catalyzes the oxidation of toluene to p-cresol in Pseudomonas mendocina KR1. J Bacteriol 173:3010–3016

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wright JD (1993) Fungal degradation of benzoic acid and related compounds. World J Microbiol Biotechnol 9:9–16

    CAS  PubMed  Google Scholar 

  • Xu F (1996) Oxidation of phenols, anilines, and benzenethiols by fungal laccases: correlation between activity and redox potentials as well as halide inhibition. Biochemistry 35:7608–7614

    CAS  PubMed  Google Scholar 

  • Yadav JS, Loper JC (2000) Cloning and characterization of the cytochrome P450 oxidoreductase gene from the zygomycete fungus Cunninghamella. Biochem Biophys Res Commun 268:345–353

    CAS  PubMed  Google Scholar 

  • Yamada K, Akiba Y, Shibuya T, Kashiwada A, Matsuda K, Hirata M (2005) Water purification through bioconversion of phenol compounds by tyrosinase and chemical adsorption by chitosan beads. Biotechnol Prog 21:823–829

    CAS  PubMed  Google Scholar 

  • Ying GG, Williams B, Kookana R (2002) Environmental fate of alkylphenols and alkylphenol ethoxylates—a review. Environ Int 28:215–226

    CAS  PubMed  Google Scholar 

  • Ying GG, Kookana RS, Dillon P (2003) Sorption and degradation of selected five endocrine disrupting chemicals in aquifer material. Water Res 37:3785–3791

    CAS  PubMed  Google Scholar 

  • Yuan SY, CH Yu, Chang BV (2004) Biodegradation of nonylphenol in river sediment. Environ Pollut 127:425–430

    CAS  PubMed  Google Scholar 

  • Zalko D, Costagliola R, Dorio C, Rathahao E, Cravedi JP (2003) In vivo metabolic fate of the xeno-estrogen 4-n-nonylphenol in Wistar rats. Drug Metab Dispos 31:168–178

    CAS  PubMed  Google Scholar 

Download references

Acknowledgement

We greatly acknowledge K. Smith (UFZ Centre for Environmental Research Leipzig-Halle) for help with the English language.

Author information

Authors and Affiliations

  1. Department of Environmental Research, RWTH Aachen University, 52074, Aachen, Germany

    P. F. X. Corvini & A. Schäffer

  2. Fraunhofer Institute for Molecularbiology and Applied Ecology, 57392, Schmallenberg, Germany

    A. Schäffer

  3. Department of Environmental Microbiology, UFZ Centre for Environmental Research Leipzig-Halle, Permoserstr. 15, 04318, Leipzig, Germany

    D. Schlosser

Authors
  1. P. F. X. Corvini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Schäffer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. Schlosser
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. Schlosser.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Corvini, P.F.X., Schäffer, A. & Schlosser, D. Microbial degradation of nonylphenol and other alkylphenols—our evolving view. Appl Microbiol Biotechnol 72, 223–243 (2006). https://doi.org/10.1007/s00253-006-0476-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-006-0476-5

Keywords

Search

Navigation