A novel metabolic pathway for degradation of 4-nonylphenol environmental contaminants by Sphingomonas xenophaga Bayram: ipso-Hydroxylation and intramolecular rearrangement

University of Duisburg-Essen, Essen, North Rhine-Westphalia, Germany
Journal of Biological Chemistry (Impact Factor: 4.57). 05/2005; 280(16):15526-33. DOI: 10.1074/jbc.M413446200
Source: PubMed


Several nonylphenol isomers with alpha-quaternary carbon atoms serve as growth substrates for Sphingomonas xenophaga Bayram, whereas isomers containing hydrogen atoms at the alpha-carbon do not. Three metabolites of 4-(1-methyloctyl)-phenol were isolated in mg quantities from cultures of strain Bayram supplemented with the growth substrate isomer 4-(1-ethyl-1,4-dimethyl-pentyl)-phenol. They were unequivocally identified as 4-hydroxy-4-(1-methyl-octyl)-cyclohexa-2,5-dienone, 4-hydroxy-4-(1-methyl-octyl)-cyclohex-2-enone, and 2-(1-methyl-octyl)-benzene-1,4-diol by high pressure liquid chromatography-mass spectrometry and nuclear magnetic resonance spectroscopy. Furthermore, two metabolites originating from 4-n-nonylphenol were identified as 4-hydroxy-4-nonyl-cyclohexa-2,5-dienone and 4-hydroxy-4-nonyl-cyclohex-2-enone by high pressure liquid chromatography-mass spectrometry. We conclude that nonylphenols were initially hydroxylated at the ipso-position forming 4-alkyl-4-hydroxy-cyclohexa-2,5-dienones. Dienones originating from growth substrate nonylphenol isomers underwent a rearrangement that involved a 1,2-C,O shift of the alkyl moiety as a cation to the oxygen atom of the geminal hydroxy group yielding 4-alkoxyphenols, from which the alkyl moieties can be easily detached as alcohols by known mechanisms. Dienones originating from nongrowth substrates did not undergo such a rearrangement because the missing alkyl substituents at the alpha-carbon atom prevented stabilization of the putative alpha-carbocation. Instead they accumulated and subsequently underwent side reactions, such as 1,2-C,C shifts and dihydrogenations. The ipso-hydroxylation and the proposed 1,2-C,O shift constitute key steps in a novel pathway that enables bacteria to detach alpha-branched alkyl moieties of alkylphenols for utilization of the aromatic part as a carbon and energy source.

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    • "However, Nguyen et al. [89] found that most of the isolated alkylphenol-degrading bacteria are able to degrade long-chain alkylphenols via multicomponent phenol hydroxylase and the ortho-cleavage pathway. The ipso-hydroxylation pathway was responsible for the removal of the alkyl chain from NP by Sphingomonas strains [90–96], in which NP isomers were initially hydroxylated at the ipso-position forming dienones, and subsequently the nonyl chain shifts to the oxygen atom in the introduced hydroxyl group to form alkoxyphenols, from which the alkyl moieties can be easily detached as alcohols by known mechanisms [95,97]. "
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    ABSTRACT: Nonylphenol (NP) is an ultimate degradation product of nonylphenol polyethoxylates (NPE) that is primarily used in cleaning and industrial processes. Its widespread use has led to the wide existence of NP in various environmental matrices, such as water, sediment, air and soil. NP can be decreased by biodegradation through the action of microorganisms under aerobic or anaerobic conditions. Half-lives of biodegradation ranged from a few days to almost one hundred days. The degradation rate for NP was influenced by temperature, pH and additions of yeast extracts, surfactants, aluminum sulfate, acetate, pyruvate, lactate, manganese dioxide, ferric chloride, sodium chloride, hydrogen peroxide, heavy metals, and phthalic acid esters. Although NP is present at low concentrations in the environment, as an endocrine disruptor the risks of long-term exposure to low concentrations remain largely unknown. This paper reviews the occurrence of NP in the environment and its aerobic and anaerobic biodegradation in natural environments and sewage treatment plants, which is essential for assessing the potential risk associated with low level exposure to NP and other endocrine disruptors.
    International Journal of Molecular Sciences 12/2012; 13(1):491-505. DOI:10.3390/ijms13010491 · 2.86 Impact Factor
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    • "The degradation of technical nonylphenol mixtures in Sphingomonas sp. TTNP3 and Sphingobium xenophagum Bayram leads to the formation of minor amounts of 2-alkylated hydroquinones (Corvini et al. 2004a; Gabriel et al. 2005), potentially toxic metabolites that may pose oxidative stress on the organism. Even though Sphingomonas sp. "
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    ABSTRACT: Hydroquinone-1,2-dioxygenase, an enzyme involved in the degradation of alkylphenols in Sphingomonas sp. strain TTNP3 was purified to apparent homogeneity. The extradiol dioxygenase catalyzed the ring fission of hydroquinone to 4-hydroxymuconic semialdehyde and the degradation of chlorinated and several alkylated hydroquinones. The activity of 1 mg of the purified enzyme with unsubstituted hydroquinone was 6.1 μmol per minute, the apparent Km 2.2 μM. ICP-MS analysis revealed an iron content of 1.4 moles per mole enzyme. The enzyme lost activity upon exposure to oxygen, but could be reactivated by Fe(II) in presence of ascorbate. SDS-PAGE analysis of the purified enzyme yielded two bands of an apparent size of 38 kDa and 19 kDa, respectively. Data from MALDI-TOF analyses of peptides of the respective bands matched with the deduced amino acid sequences of two neighboring open reading frames found in genomic DNA of Sphingomonas sp strain TTNP3. The deduced amino acid sequences showed 62% and 47% identity to the large and small subunit of hydroquinone dioxygenase from Pseudomonas fluorescens strain ACB, respectively. This heterotetrameric enzyme is the first of its kind found in a strain of the genus Sphingomonas sensu latu.
    AMB Express 05/2011; 1(1):8. DOI:10.1186/2191-0855-1-8
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    • "Degradation of NP by Sphingomonas sp. TTNP3 and S. xenophagum Bayram (formerly reported as S. xenophaga Bayram [Pal et al. 2006]) is initiated by ipso-hydroxylation followed by cleavage of the benzylic carbon bond (Gabriel et al. 2005b, 2007; Corvini et al. 2006a), yielding rearrangement products and a mixture of branched nonyl alcohol isomers (NOH). A recent study of Gabriel et al. (2008) further indicated that NP isomers with bulky a-substitutions were relatively recalcitrant and that differential ipso-hydroxylation of NP mixtures may markedly affect the specific estrogenicity of the aged NP material. "
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    ABSTRACT: When discharged in chlorinated wastewater, alkylphenol ethoxylate metabolites (APEMs) are often discharged in halogenated form (XAPEMs, X = Cl, or Br). The potential environmental impact of XAPEM release was assessed by studying the biotransformation of halogenated nonylphenol by Sphingobium xenophagum Bayram and a soil-enrichment culture. S. xenophagum Bayram transformed chlorinated nonylphenol (ClNP) slowly and nearly completely to form nonyl alcohol; the monobrominated nonylphenol (BrNP) and dibrominated nonylphenol were transformed cometabolically with nonylphenol (NP) as the primary substrate. The presence of either ClNP or BrNP in the S. xenophagum Bayram cultures retarded the transformation of nonhalogenated NP. NP-degrading soil cultures transformed nonhalogenated NP to a mixture of nonyl alcohols but were not capable of transforming either ClNP or BrNP. The presence of either ClNP or BrNP retarded the transformation of nonhalogenated NP in the soil cultures, as was observed in S. xenophagum Bayram cultures. Predicting the environmental fate of alkylphenol ethoxylate residues requires considering APEM halogenation during effluent chlorination and inhibitory effects as well as the refractory nature of halogenated metabolites.
    Archives of Environmental Contamination and Toxicology 02/2011; 60(2):212-9. DOI:10.1007/s00244-010-9576-4 · 1.90 Impact Factor
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