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Biotransformation of Halogenated Nonylphenols with Sphingobium Xenophagum Bayram and a Nonylphenol-Degrading Soil-Enrichment Culture

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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.

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References

  • Ahel M, Giger W, Koch M (1994) Behaviour of alkylphenol polyethoxylate surfactants in the aquatic environment. I. Occurrence and transformation in sewage treatment. Water Res 28:1131–1142

    Article  CAS  Google Scholar 

  • Ball HA, Reinhard M (1985) Discharge of halogenated octylphenol polyethoxylate residues in a chlorinated secondary effluent. In: Jolley RL et al (eds) Water chlorination: chemistry, environmental impact, and health effects, vol 5. Lewis, Chelsea, pp 1505–1514

    Google Scholar 

  • Ball HA, Reinhard M, McCarty PL (1989) Biotransformation of halogenated and nonhalogenated octylphenol polyethoxylate residues under aerobic and anaerobic conditions. Environ Sci Technol 23:951–961

    Article  CAS  Google Scholar 

  • Corvini PFX, Hollender JJiR, Schumacher S, Prell J, Hommes G, Priefer U et al (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

    Article  CAS  Google Scholar 

  • Corvini PFX, Schäffer A, Schlosser D (2006b) Microbial degradation of nonylphenol and other alkylphenols—our evolving view. Appl Environ Microbiol 72:223–243

    CAS  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

    Article  CAS  Google Scholar 

  • Di Corcia A, Cavallo R, Crescenzi C, Nazzari M (2000) Occurrence and abundance of dicarboxylated metabolites of nonylphenol polyethoxylate surfactants in treated sewages. Environ Sci Technol 34:3914–3919

    Article  CAS  Google Scholar 

  • Díaz A, Ventura F, Galceran MT (2002) Development of a solid phase micro extraction method for the determination of short-ethoxychain nonylphenols and their brominated analogues in raw and treated water. J Chromatogr A 963:159–167

    Article  Google Scholar 

  • Eganhouse RP, Pontolillo J, Gaines RB, Frysinger GS, Gabriel FLP, Kohler HPE et al (2009) Isomer-specific determination of 4-nonylphenols using comprehensive two-dimensional gas chromatography/time-of-flight mass spectrometry. Environ Sci Technol 43:9306–9313

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ferguson PL, Iden CR, Brownawell BJ (2001) Distribution and fate of neutral alkylphenol ethoxylate metabolites in a wastewater impacted urban estuary. Environ Sci Technol 35:2428–2435

    Article  CAS  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  Google Scholar 

  • Fujita Y, Reinhard M (1997) Identification of metabolites from the biological transformation of the nonionic surfactant residue octylphenoxyacetic acid and its brominated analog. Environ Sci Technol 31:1518–1524

    Article  CAS  Google Scholar 

  • Fujita M, Ike M, Mori K, Kaku H, Sakaguchi Y, Asano M et al (2000) Behaviour of nonylphenolethoxylates in sewage treatment plants in Japan-biotransformation and toxicity. Water Sci Technol 42:23–30

    CAS  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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gabriel FLP, Cyris M, Jonkers N, Giger W, Guenther K, Kohler HP (2007) Elucidation of the ipso-substitution mechanism for side-chain cleavage of α-quaternary 4-nonylphenols and 4-t-butoxyphenol in Sphingobium xenophagum Bayram. Appl Environ Microbiol 73:3320–3326

    Article  CAS  Google Scholar 

  • Gabriel FLP, Routledge EJ, Heidlberger A, Rentsch D, Guenther K, Giger W et al (2008) Isomer-specific degradation and endocrine disrupting activity of nonylphenols. Environ Sci Technol 42:6399–6408

    Article  CAS  Google Scholar 

  • García-Reyero N, Requena V, Petrovic M, Fischer B (2004) Estrogenic potential of halogenated derivatives of nonylphenol ethoxylates and carboxylates. Environ Toxicol Chem 23:705–711

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hill EM, Smith MD (2006) Identification and steroid receptor activity of products formed from the bromination of technical nonylphenol. Chemosphere 64:1761–1768

    Article  CAS  Google Scholar 

  • Ieda T, Horii Y, Petrick G, Yamashita N, Ochiai N, Kannan K (2005) analysis of nonylphenol isomers in a technical mixture and in water by comprehensive two-dimensional gas chromatography–mass spectrometry. Environ Sci Technol 39:7202–7207

    Article  CAS  Google Scholar 

  • Jobling S, Sheahan D, Osborne JA, Matthiessen P, Sumpter JP (1996) Inhibition of testicular growth in rainbow trout (Oncorhynchus mykiss) exposed to estrogenic alkylphenolic chemicals. Environ Toxicol Chem 15:194–202

    CAS  Google Scholar 

  • Maguire RJ (1999) Review of the persistence of nonylphenol and nonylphenol ethoxylates in aquatic environments. Water Qual Res J Can 34:37–78

    CAS  Google Scholar 

  • Montgomery-Brown J, Reinhard M (2003) Occurrence and behavior of alkylphenol polyethoxylates in the environment. Environ Eng Sci 20:471–486

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Montgomery-Brown J, Li Y, Ding WH, Mong GM, Campbell JA, Reinhard M (2008) NP1EC degradation pathways under oxic and microxic conditions. Environ Sci Technol 42:2879–2885

    Article  Google Scholar 

  • Pal R, Bhasin VK, Lal R et al (2006) Proposal to reclassify [Sphingomonas] xenophaga Stolz 2000, [Sphingomonas] taejonensis Lee et al. 2001 as Sphingobium xenophagum comb. nov. and Sphingopyxis taejonensis comb. nov., respectively. Int J Syst Evol Microbiol 56:667–670

    Article  CAS  Google Scholar 

  • Pham Manh H, Shinji T, Michihiko I, Yayoi K, Kousuke K, Pham Hung V et al (2003) Simultaneous determination of degradation products of nonylphenol polyethoxylates and their halogenated derivatives by solid-phase extraction and gas chromatography-tandem mass spectrometry after trimethylsilylation. J Chromatogr A 1020:161–171

    Article  Google Scholar 

  • Petrovic M, Diaz A, Ventura F, Barcelo D (2001) Simultaneous determination of halogenated derivatives of alkylphenol ethoxylates and their metabolites in sludges, river sediments, surface, drinking and waste waters by liquid chromatography-mass spectrometry. Anal Chem 73:5886–5895

    Article  CAS  Google Scholar 

  • Petrovic M, Barcelo D, Diaz A, Ventura F (2003) Low nanogram per litre determination of halogenated nonylphenols, nonylphenol carboxylates and their non-halogenated precursors in water and sludge by liquid chromatography electrospray tandem mass spectrometry. J Am Soc Mass Spectrom 14:516–527

    Article  CAS  Google Scholar 

  • Preuss TG, Gehrhardt J, Schirmer K, Coors A, Rubach M, Russ A et al (2006) Nonylphenol isomers differ in estrogenic activity. Environ Sci Technol 40:5147–5153

    Article  CAS  Google Scholar 

  • Reinhard M, Goodman N, Mortelmans KE (1982) Occurrence of brominated alkylphenol polyethoxy carboxylates in mutagenic wastewater concentration. Environ Sci Technol 16:351–362

    Article  CAS  Google Scholar 

  • Renner R (1997) European bans on surfactant trigger transatlantic debate. Environ Sci Technol 31:316A–320A

    Article  CAS  Google Scholar 

  • Shioji H, Tsunoi S, Kobayashi Y, Shigemori T, Ike M, Fujita M, Miyaji Y et al (2006) Estrogenic activity of branched 4-nonylphenol isomers examined by yeast two-hybrid assay. J Health Sci 52:132–141

    Article  CAS  Google Scholar 

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

    Article  CAS  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

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Thiele B, Gunther K, Schwuger MJ (1997) Alkylphenol ethoxylates: trace analysis and environmental behavior. Chem Rev 97:3247–3272

    Article  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 

  • United States Environmental Protection Agency (2007) Estimation Programs Interface (EPI) SuiteTM for Microsoft® Windows, version 3.20. USEPA, Washington, DC

    Google Scholar 

  • Ventura F, Figueras A, Caixach J, Espadaler I, Romero J, Guardiola J et al (1988) Characterisation of polyethoxylated surfactants and their brominated derivatives formed at the water treatment plant of Barcelona by GC/MS and FAB mass-spectrometry. Water Res 22:1211–1217

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Ying GG, Williams B, Kookana RS (2002) Environmental fate of alkylphenols and alkylphenol ethoxylates—a review. Environ Int 18:215–226

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Funding was provided by the USEPA and the American Water Works Association Research Foundation through a grant to the National Center for Sustainable Water Supply at Arizona State University (Tempe, AZ), Nanyang Technological University (Singapore), Water Reuse Foundation, California Department of Water Resources, Santa Clara Valley Water District, and National Science Foundation of China (Grants No. 50578114 and 50878165). The authors thank Frédéric Gabriel and Hans Peter Kohler for providing S. xenophagum Bayram. Opinions, findings, conclusions, and recommendations in this publication are those of the authors and do not necessarily reflect the views of the sponsoring agencies.

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Correspondence to Martin Reinhard.

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Li, Y., Montgomery-Brown, J. & Reinhard, M. Biotransformation of Halogenated Nonylphenols with Sphingobium Xenophagum Bayram and a Nonylphenol-Degrading Soil-Enrichment Culture. Arch Environ Contam Toxicol 60, 212–219 (2011). https://doi.org/10.1007/s00244-010-9576-4

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