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Quinone-respiration improves dechlorination of carbon tetrachloride by anaerobic sludge

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Abstract

The impact of humic acids and the humic model compound, anthraquinone-2,6-disulfonate (AQDS), on the biodegradation of carbon tetrachloride (CT) by anaerobic granular sludge was studied. Addition of both humic acids and AQDS at sub-stoichiometric levels increased the first-order rate of conversion of CT up to 6-fold, leading to an increased production of inorganic chloride, which accounted for 40–50% of the CT initially added. Considerably less dechlorination occurred in sludge incubations lacking humic substances. By comparison, very limited dechlorination occurred in sterile controls with autoclaved sludge. Accumulation of chloroform (1–10%) and dichloromethane (traces) also accounted for the CT converted. The accumulation of a chlorinated ethene, perchloroethylene (up to 9% of added CT), is also reported for the first time as an end-product of CT degradation. A humus-respiring enrichment culture (composed primarily of a Geobacter sp.) derived from the granular sludge also dechlorinated CT, yielding products similar to the AQDS-supplemented granular sludge consortium. The dechlorination of CT by the Geobacter enrichment was dependent on the presence of AQDS or humic acids, which were reduced during the assays. The reduced form of AQDS, anthrahydroquinone-2,6-disulfonate, was shown to cause the chemical reduction of CT when incubated in sterile medium. The results taken as a whole indicate that the formation of reduced humic substances by quinone-respiring microorganisms can contribute to the reductive dechlorination of CT.

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References

  • Agteren MH van, Keuning S (1998) Handbook on biodegradation and biological treatment of hazardous organic compounds. Kluwer, Dordrecht

  • Bradley PM, Chapelle FH, Lovley DR (1998) Humic acids as electron acceptors for anaerobic microbial oxidation of vinyl chloride and dichloroethene. Appl Environ Microbiol 64:3102–3105

    CAS  PubMed  Google Scholar 

  • Budzikiewicz H (2003) Heteroaromatic monothiocarboxylic acids from Pseudomonas spp. Biodegradation 14:65–72

    Article  CAS  PubMed  Google Scholar 

  • Cervantes FJ, Velde S van der, Lettinga G, Field JA (2000a) Quinones as terminal electron acceptors for anaerobic microbial oxidation of phenolic compounds. Biodegradation 11:313–321

    Article  CAS  PubMed  Google Scholar 

  • Cervantes FJ, Velde S van der, Lettinga G, Field JA (2000b) Competition between methanogenesis and quinone respiration for ecologically important substrates in anaerobic consortia. FEMS Microbiol Ecol 34:161–171

    Article  CAS  PubMed  Google Scholar 

  • Cervantes FJ, Dijksma W, Duong-Dac T, Ivanova A, Lettinga G, Field JA (2001a) Anaerobic mineralization of toluene by enriched sediments with quinones and humus as terminal electron acceptors. Appl Environ Microbiol 67:4471–4478

    Article  CAS  PubMed  Google Scholar 

  • Cervantes FJ, Van der Zee FP, Lettinga G, Field JA (2001b) Enhanced decolourisation of acid orange 7 in a continuous UASB reactor with quinones as redox mediators. Water Sci Technol 44:123–128

    CAS  Google Scholar 

  • Cervantes FJ, Duong-Dac T, Ivanova AE, Roest K, Akkermans ADL, Lettinga G, Field JA (2003) Selective enrichment of Geobacter sulfurreducens from anaerobic granular sludge with quinones as terminal electron acceptors. Biotechnol Lett 25:39–45

    Article  CAS  PubMed  Google Scholar 

  • Coates JD, Ellis DJ, Roden E, Gaw K, Blunt-Harris EL, Lovley DR (1998) Recovery of humics-reducing bacteria from a diversity of sedimentary environments. Appl Environ Microbiol 64:1504–1509

    CAS  PubMed  Google Scholar 

  • Collins R, Picardal F (1999) Enhanced anaerobic transformation of carbon tetrachloride by soil organic matter. Environ Toxicol Chem 18:2703–2710

    CAS  Google Scholar 

  • Criddle CS, McCarty PL (1991) Electrolytic model system for reductive dehalogenation in aqueous environments. Environ Sci Technol 25:973–978

    CAS  Google Scholar 

  • Curtis GP, Reinhard M (1994) Reductive dehalogenation of hexachloroethane, carbon tetrachloride, and bromoform by anthrahydroquinone disulfonate and humic acid. Environ Sci Technol 28:2393–2401

    CAS  Google Scholar 

  • De Best JH, Salminen E, Doddema HJ, Janssen DB, Harder W (1998) Transformation of carbon tetrachloride under sulfate reducing conditions. Biodegradation 8:429–436

    Google Scholar 

  • De Best JH, Hunneman P, Doddema HJ, Janssen DB, Harder W (1999) Transformation of carbon tetrachloride in an anaerobic packed-bed reactor without addition of another electron donor. Biodegradation 10:287–295

    Article  PubMed  Google Scholar 

  • Eekert MHA van, Schröder TJ, Stams AJM, Schraa G, Field JA (1998) Degradation and fate of carbon tetrachloride in unadapted methanogenic granular sludge. Appl Environ Microbiol 64:2350–2356

    PubMed  Google Scholar 

  • Eekert MHA van, Stams AJM, Field JA, Schraa G (1999) Gratuitous dechlorination of chloroethanes by methanogenic granular sludge. Appl Microbiol Biotechnol 51:46–52

    Article  Google Scholar 

  • Egli CR, Scholtz R, Cook AM, Leisinger T (1987) Anaerobic dechlorination of tetrachloromethane and 1,2-dichloroethane to degradable products by pure cultures of Desulfitobacterium sp. and Methanobacterium sp. FEMS Microbiol Lett 43:257–261

    Google Scholar 

  • Field JA, Cervantes FJ, Van der Zee FP, Lettinga G (2000) Role of quinones in the biodegradation of priority pollutants: a review. Water Sci Technol 42:215–222

    CAS  Google Scholar 

  • Frankin RJ (2001) Full-scale experiences with anaerobic treatment of industrial wastewaters. Water Sci Technol 44:1–6

    CAS  Google Scholar 

  • Gantzer CJ, Wackett LP (1991) Reductive dechlorination catalyzed by bacterial transition-metal coenzymes. Environ Sci Technol 25:715–722

    CAS  Google Scholar 

  • Gerlach R, Cunningham AB, Caccavo JF (2000) Dissimilatory iron-reducing bacteria can influence the reduction of carbon tetrachloride by iron metal. Environ Sci Technol 34:2461–2464

    Article  CAS  Google Scholar 

  • Hashsham SA, Freedman DL (1999) Enhanced biotransformation of carbon tetrachloride by Acetobacterium woodii upon addition of hydroxocobalamin and fructose. Appl Environ Microbiol 65:4537–4542

    Google Scholar 

  • Kappler A, Haderlein SB (2003) Natural organic matter as reductant for chlorinated aliphatic pollutants. Environ Sci Technol 37:2714–2719

    Article  CAS  PubMed  Google Scholar 

  • Koons BW, Baeseman JL, Novak PJ (2001) Investigation of cell exudates active in carbon tetrachloride and chloroform degradation. Biotechnol Bioeng 74:12–17

    Article  CAS  PubMed  Google Scholar 

  • Kriegman-King MR, Reinhard M (1994) Transformation of carbon tetrachloride by pyrite in aqueous solution. Environ Sci Technol 28:692–700

    CAS  Google Scholar 

  • Krone UE, Laufer K, Thauer RK (1989) Coenzyme F430 as a possible catalyst for the reductive dehalogenation of chlorinated C1 hydrocarbons in methanogenic bacteria. Biochemistry 28:10061–10065

    PubMed  Google Scholar 

  • Kudlich M, Keck A, Klein J, Stolz A (1997) Localization of the enzyme system involved in anaerobic reduction of azo dyes by Sphingomonas sp. strain BN6 and effect of artificial redox mediators on the rate of azo dye reduction. Appl Environ Microbiol 63:3691–3694

    CAS  Google Scholar 

  • Laszlo JA (2000) Regeneration of azo-dye-saturated cellulosic anion exchange resin by Burkholderia cepacia anaerobic dye reduction. Environ Sci Technol 34:167–172

    Article  CAS  Google Scholar 

  • Lee CH, Lewis TA, Paszczynski A, Crawford RL (1999) Identification of an extracellular catalyst of carbon tetrachloride dehalogenation from Pseudomonas stutzeri strain KC as pyridine-2,6-bis(thiocarboxylate). Biochem Biophys Res Commun 261:562–566

    Article  CAS  PubMed  Google Scholar 

  • Lettinga G, Velsen AFM van, Hobma SW, Zeeuw W de, Klapwijk A (1980) Use of the upflow sludge blanket (USB) reactor concept for biological wastewater treatment, especially for anaerobic treatment. Biotechnol Bioeng 22:699–734

    CAS  Google Scholar 

  • Lewis TA, Paszczynski A, Gordon-Wylie SW, Jeedigunta S, Lee CH, Crawford RL (2001) Carbon tetrachloride dechlorination by the bacterial transition metal chelator pyridine-2,6-bis(thiocarboxylic acid). Environ Sci Technol 35:552–559

    Article  CAS  PubMed  Google Scholar 

  • McCormick ML, Bouwer EJ, Adriaens P (2002) Carbon tetrachloride transformation in a model iron-reducing culture: relative kinetics of biotic and abiotic reactions. Environ Sci Technol 36:403–410

    Article  CAS  PubMed  Google Scholar 

  • Middeldorp PJM, Luijten MLGC, Van der Pas BA, Eekert MHA van, Kengen SWM, Schraa G, Stams AJM (1999) Anaerobic microbial reductive dehalogenation of chlorinated ethenes. Bioremediation J 3:151–169

    CAS  Google Scholar 

  • Nurmi JT, Tratnyek PG (2002) Electrochemical properties of natural organic matter (NOM), fractions of NOM, and model biogeochemical electron shuttles. Environ Sci Technol 36:617–624

    Article  CAS  PubMed  Google Scholar 

  • Perlinger JA, Angst W, Schwarzenbach RP (1996). Kinetics of the reduction of hexachloroethane by juglone in solutions containing hydrogen sulfide. Environ Sci Technol 30:3408–3417

    Article  CAS  Google Scholar 

  • Picardal FW, Arnold RG, Couch H, Little AM, Smith MA (1993) Involvement of cytochromes in the anaerobic biotransformation of tetrachloromethane by Shewanella putrefaciens 200. Appl Environ Microbiol 59:3763–3770

    Google Scholar 

  • Recknagel RO, Glende EA (1973) Carbon tetrachloride hepatotoxicity: an example of lethal cleavage. Crit Rev Toxicol 2:263–297

    Google Scholar 

  • Schwarzenbach RP, Stierli R, Lanz K, Zeyer J (1990) Quinone and iron porphyrin mediated reduction of nitroaromatic compounds in homogeneous aqueous solution. Environ Sci Technol 24:1566–1574

    CAS  Google Scholar 

  • Tratnyek PG, Scherer MM, Deng B, Hu S (2001) Effects of natural organic matter anthropogenic surfactants, and model quinones on the reduction of contaminants by zero-valent iron. Water Res 35:4435–4443

    Article  CAS  PubMed  Google Scholar 

  • Vogel TM, Criddle CS, McCarty PL (1987) Transformations of halogenated aliphatic compounds. Environ Sci Technol 21:722–736

    CAS  Google Scholar 

  • Wentz M (1995) The evolution of environmentally responsible fabricare technologies. Am Drycleaner 62:52–62

    Google Scholar 

  • Zee FP van der, Lettinga G, Field JA (2000) The role of (auto)catalysis in the mechanism of an azo dye reduction. Water Sci Technol 42:301–308

    Google Scholar 

  • Zee FP van der, Bouwman RHM, Strik DPBTB, Lettinga G, Field JA (2001) Application of redox mediators to accelerate the transformation of reactive azo dyes in anaerobic bioreactors. Biotechnol Bioeng 75:691–701

    Article  PubMed  Google Scholar 

  • Zou S, Stensel HD, Ferguson JF (2000) Carbon tetrachloride degradation: effect of microbial growth substrate and vitamin B12 content. Environ Sci Technol 34:1751–1757

    Article  CAS  Google Scholar 

Download references

Acknowledgement

This research was financially supported by the Council of Science and Technology of Mexico (Project SEP-CONACyT 40808).

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Authors and Affiliations

  1. Sub-department of Environmental Technology, Wageningen University, P.O. Box 8129, 6700 EV, Wageningen, The Netherlands

    F. J. Cervantes, L. Vu-Thi-Thu & G. Lettinga

  2. Department of Chemical and Environmental Engineering, University of Arizona, P.O. Box 210011, Tucson, AZ 85721-0011, USA

    J. A. Field

  3. Departamento de Ciencias del Agua y del Medio Ambiente, Instituto Tecnológico de Sonora, 5 de Febrero 818 Sur, 85000, Cd. Obregón, Sonora, Mexico

    F. J. Cervantes

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  1. F. J. Cervantes
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  2. L. Vu-Thi-Thu
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  3. G. Lettinga
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  4. J. A. Field
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Correspondence to F. J. Cervantes.

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Cervantes, F.J., Vu-Thi-Thu, L., Lettinga, G. et al. Quinone-respiration improves dechlorination of carbon tetrachloride by anaerobic sludge. Appl Microbiol Biotechnol 64, 702–711 (2004). https://doi.org/10.1007/s00253-004-1564-z

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  • DOI: https://doi.org/10.1007/s00253-004-1564-z

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