Skip to main content
Log in

Degradation of BTX by dissimilatory iron-reducing cultures

  • Original Paper
  • Published:
Biodegradation Aims and scope Submit manuscript

Abstract

The ability of indigenous bacteria to anaerobically degrade monoaromatic hydrocarbons has received attention as a potential strategy to remediate polluted aquifers. Despite the fact that iron-reducing conditions are often dominating in contaminated sediment, most of the studies have focussed on degradation of this class of pollutants with other terminal acceptors. In this work, we enriched bacteria from an iron-reducing aquifer in which a plume of pollution has developed over several decades and we show that benzene, toluene, meta- and para-xylene (BTX) could be degraded by the enriched cultures containing intrinsic iron-reducing microorganisms. To our knowledge, this is the first time that para-xylene degradation by dissimilatory iron-reducing bacteria has been reported in sediment free enrichment cultures. BTX degradation rates in enrichment cultures progressively increased in time and were found in good agreement with theoretical values calculated assuming complete BTX oxidation with Fe(II) as final electron acceptor. In addition, using labelled (13C1) benzene and toluene we could unambiguously identify intermediates of their respective degradation pathways. We provide evidence for benzene degradation via phenol formation under iron-reducing conditions, whereas toluene and meta-xylene were transformed into the corresponding benzylsuccinates.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anderson RT et al (1998) Anaerobic benzene oxidation in the Fe(III) reduction zone of petroleum-contaminated aquifers. Environ Sci Technol 32:1222–1229

    Article  CAS  Google Scholar 

  • Beller HR et al (1995) Byproducts of anaerobic alkylbenzene metabolism useful as indicators of in situ bioremediation. Environ Sci Technol 29:2864–2870

    Article  CAS  Google Scholar 

  • Beller HR et al (1996) Isolation and characterization of a novel toluene-degrading, sulfate- reducing bacterium. Appl Environ Microbiol 62:1188–1196

    CAS  Google Scholar 

  • Beller HR et al (1997a) Anaerobic activation of toluene and o-xylene by addition to fumarate in denitrifying strain T. J Bacteriol 179:670–676

    CAS  Google Scholar 

  • Beller HR et al (1997b) Benzylsuccinate formation as a means of anaerobic toluene aActivation by sulfate-reducing strain PRTOL1. Appl Environ Microbiol 63:3729–3731

    CAS  Google Scholar 

  • Beller HR (2000) Metabolic indicators for detecting in situ anaerobic alkylbenzene degradation. Biodegradation 11:125–139

    Article  CAS  Google Scholar 

  • Beller HR et al (2000) Anaerobic toluene activation by benzylsuccinate synthase in a highly enriched methanogenic culture. Appl Environ Microbiol 66:5503–5505

    Article  CAS  Google Scholar 

  • Biegert T et al (1996) Evidence that anaerobic oxidation of toluene in the denitrifying bacterium Thauera aromatica is initiated by formation of benzylsuccinate from toluene and fumarate. Eur J Biochem 238:661–668

    Article  CAS  Google Scholar 

  • Bonneville S et al (2004) Microbial reduction of iron(III) oxyhydroxides: effects of mineral solubility and availability. Chem Geol 212:255–268

    Article  CAS  Google Scholar 

  • Botton S et al (2006) Degradation of BTEX compounds under iron-reducing conditions in contaminated aquifer microcosms. Environ Toxicol Chem 25(10) 2630–2638

    Google Scholar 

  • Caldwell ME et al (2000) Detection of phenol and benzoate as intermediates of anaerobic benzene biodegradation under different terminal electron-accepting conditions. Environ Sci Technol 34:1216–1220

    Article  CAS  Google Scholar 

  • Chakraborty R et al (2004) Anaerobic degradation of monoaromatic hydrocarbons. Appl Microbiol Biotechol 64:437–446

    Article  CAS  Google Scholar 

  • Chakraborty R et al (2005) Hydroxylation and carboxylation—two crucial steps of anaerobic benzene degradation by dechloromonas strain RCB. Appl Environ Microbiol 9:5427–5432

    Article  CAS  Google Scholar 

  • Coates JD et al (2001) Geobacter hydrogenophilus, Geobacter chapellei and Geobacter grbiciae, three new, strictly anaerobic, dissimilatory Fe(III)-reducers. Int J Syst Evol Microbiol 51:581–588

    CAS  Google Scholar 

  • Edwards E et al (1992) Anaerobic degradation of toluene and xylene by aquifer microorganisms under sulfate-reducing conditions. Appl Environ Microbiol 58:794–800

    CAS  Google Scholar 

  • Edwards E et al (1994) Anaerobic degradation of toluene and o-xylene by a methanogenic consortium. Appl Environ Microbiol 60:313–322

    CAS  Google Scholar 

  • Fries M et al (1994) Isolation, characterization, and distribution of denitrifying toluene degraders from a variety of habitats. Appl Environ Microbiol 60:2802–2810

    CAS  Google Scholar 

  • Haner A et al (1995) Degradation of p-xylene by a denitrifying enrichment culture. Appl Environ Microbiol 61:3185–3188

    CAS  Google Scholar 

  • Harms G et al (1999) Anaerobic oxidation of o-xylene, m-xylene, and homologous alkylbenzenes by new types of sulfate-reducing bacteria. Appl Environ Microbiol 65:999–1004

    CAS  Google Scholar 

  • Hess A et al (1997) In situ analysis of denitrifying toluene- and m-xylene-degrading bacteria in a diesel fuel-contaminated laboratory aquifer column. Appl Environ Microbiol 63:2136–2141

    CAS  Google Scholar 

  • Jahn MK et al (2005) Anaerobic degradation of benzene, toluene, ethylbenzene, and o-xylene in sediment-free iron-reducing enrichment cultures. Appl Environ Microbiol 71:3355–3358

    Article  CAS  Google Scholar 

  • Kane SR et al (2002) Biochemical and genetic evidence of benzylsuccinate synthase in toluene-degrading, ferric iron-reducing Geobacter metallireducens. Biodegradation 13:149–154

    Article  CAS  Google Scholar 

  • Kazumi J et al (1997) Anaerobic degradation of benzene in diverse anoxic environments. Environ Sci Technol 31:813–818

    Article  CAS  Google Scholar 

  • Lovley DR et al (1986) Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Appl Environ Microbiol 51:683–689

    CAS  Google Scholar 

  • Lovley DR et al (1987) Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl Environ Microbiol 53:1536–1540

    CAS  Google Scholar 

  • Lovley DR et al (1990) Anaerobic oxidation of toluene, phenol and p-creosol by the dissimilatory iron reducing organism, GS-15. Appl Environ Microbiol 56:1858–1864

    CAS  Google Scholar 

  • Lovley D et al (1996) Rapid anaerobic benzene oxidation with a variety of chelated Fe(III) forms. Appl Environ Microbiol 62:288–291

    CAS  Google Scholar 

  • Lovley DR et al (1998) Humic substances as a mediator for microbially catalyzed metal reduction. Acta hydrochimica et hydrobiologica 26:152–157

    Article  CAS  Google Scholar 

  • Lovley DR et al (1999) Role of humic-bound iron as an electron transfer agent in dissimilatory Fe(III) reduction. Appl Environ Microbiol 65:4252– 4254

    CAS  Google Scholar 

  • Lovley DR et al (2004) Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microbial Physiol 49:219–286

    CAS  Google Scholar 

  • Meckenstock RU et al (2004) Inhibition of anaerobic microbial o-xylene degradation by toluene in sulphdogenic sediment columns and pure cultures. FEMS Microbiol Ecol 47:381–386

    Article  CAS  Google Scholar 

  • Morasch B et al (2001) The use of a solid adsorber resin for enrichment of bacteria with toxic substrates and to identify metabolites: degradation of naphthalene, o-, and m-xylene by sulfate-reducing bacteria. J Microbiol Meth 44:183–191

    Article  CAS  Google Scholar 

  • Phelps CD et al (1999) Anaerobic biodegradation of BTEX and gasoline in various aquatic sediments. Biodegradation 10:15–25

    Article  CAS  Google Scholar 

  • Phelps CD et al (2001) Use of stable isotopes to identify benzoate as a metabolite of benzene degradation in a sulphidogenic consortium. Environ Microbiol 3:600–603

    Article  CAS  Google Scholar 

  • Rabus R et al (1995) Anaerobic degradation of ethylbenzene and other aromatic hydrocarbons by new denitrifying bacteria. Arch Microb 163:96–103

    CAS  Google Scholar 

  • Röling WFM et al (2001) Relationships between microbial community structure and hydrochemistry in a landfill leachate-polluted aquifer. Appl Environ Microbiol 67:4619–4629

    Article  Google Scholar 

  • Rooney-Varga JN et al (1999) Microbial communities associated with anaerobic benzene degradation in a petroleum-contaminated aquifer. Appl Environ Microbiol 65:3056–3063

    CAS  Google Scholar 

  • Snoeyenbos-West OL et al (2000) Enrichment of Geobacter species in response to stimulation of Fe(III) reduction in sandy aquifer sediments. Microbial Ecol 39:153–167

    Article  CAS  Google Scholar 

  • Ulrich AC et al (2005) Metabolites detected during biodegradation of 13C6-benzene in nitrate-reducing and methanogenic enrichment cultures. Environ Sci Technol 39:6681–6691

    Article  CAS  Google Scholar 

  • van Breukelen BM et al (2003) Biogeochemistry and isotope geochemistry of a landfill leachate plume. J Contam Hydrol 65:245–268

    Article  CAS  Google Scholar 

  • Viollier E et al (2000) The ferrozine method revisited: Fe(II)/Fe(III) determination in natural waters. Appl Geochem 15:785–790

    Article  CAS  Google Scholar 

  • Young LY et al (2005) Metabolic biomarkers for monitoring in situ anaerobic hydrocarbon degradation. Environ Health Persp 113:62–67

    Article  CAS  Google Scholar 

  • Zheng Z et al (2002) Intrinsic biodegradation of toluene coupled to the microbial reduction of ferric iron: laboratory column experiments. Environ Geol 42:649–656

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We acknowledge the Netherlands Organization for Scientific Research (NWO) for funding in the framework of TRIAS project 835.80.007, Resilience of the groundwater ecosystem in reaction to anthropogenic disturbances.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sabrina Botton.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Botton, S., Parsons, J.R. Degradation of BTX by dissimilatory iron-reducing cultures. Biodegradation 18, 371–381 (2007). https://doi.org/10.1007/s10532-006-9071-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10532-006-9071-9

Keywords

Navigation