Skip to main content
SpringerLink
Log in

Decolorization of azo dyes by Geobacter metallireducens

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Geobacter metallireducens was found to be capable of decolorizing several azo dyes with different structures to various extents. Pyruvate, ethanol, acetate, propionate, and benzoate could support 66.3 ± 2.6−93.7 ± 2.1 % decolorization of 0.1 mM acid red 27 (AR27) in 40 h. The dependence of the specific decolorization rate on AR27 concentration (25 to 800 μM) followed Michaelis–Menten kinetics (K m = 186.9 ± 1.4 μΜ, V max = 0.65 ± 0.02 μmol mg protein−1 h−1). Enhanced AR27 decolorization was observed with the increase of cell concentrations ranging from 7.5 to 45 mgL−1. AR27 decolorization by G. metallireducens was retarded by the presence of goethite, which competed electrons with AR27 and was reduced to Fe(II). The addition of low concentrations of humic acid (1−100 mgL−1) or 2-hydroxy–1,4-naphthoquinone (0.5−50 μM) could improve the decolorization performance of G. metallireducens. High-performance liquid chromatography analysis suggested reductive pathway to be responsible for decolorization. This was the first study on azo dye decolorization by Geobacter strain and might improve our understanding of natural attenuation and bioremediation of environments polluted by azo dyes.

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

Similar content being viewed by others

References

  • Anderson RT, Vrionis HA, Ortiz-Bernad I, Resch CT, Peacock A, Dayvault R, Marutzky S, Metzler DR, Karp K, Lowe M, White DC, Long PE, Lovley DR (2003) Stimulating the in situ activity of Geobacter species to remove uranium from the groundwater of a uranium-contaminated aquifer. Appl Environ Microbiol 69:5884–5891

    Article  PubMed  CAS  Google Scholar 

  • Bazylinski DA, Dean AJ, Schuler D, Phillips EJP, Lovley DR (2000) N2-dependent growth and nitrogenase activity in the metal-metabolizing bacteria, Geobacter and Magnetospirillum species. Environ Microbiol 2:266–273

    Article  PubMed  CAS  Google Scholar 

  • Bond DR, Holmes DE, Tender LM, Lovley DR (2002) Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295:483–485

    Article  PubMed  CAS  Google Scholar 

  • Boukhalfa H, Icopini GA, Reilly SD, Neu MP (2007) Plutonium (IV) reduction by the meal-reducing bacteria Geobacter metallireducens G15 and Shewanella oneidensis MR1. Appl Environ Microbiol 73:5897–5903

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Brigé A, Motte B, Borloo J, Buysschaert G, Devreese B, van Beeumen JJ (2008) Bacterial decolorization of textile dyes is an extracellular process requiring a multicomponent electron transfer pathway. Microbiol Biotechnol 1:40–52

    Google Scholar 

  • Brown MA, DeVito SC (1993) Predicting azo dye toxicity. Crit Rev Environ Sci Technol 23:249–324

    Article  CAS  Google Scholar 

  • Cai P, Xiao X, He Y, Li W, Chu J, Wu C, He M, Zhang Z, Sheng G, Lam MHW, Xu F, Yu H (2011) Anaerobic biodecolorization mechanism of methyl orange by Shewanella oneidensis MR-1. Appl Microbiol Biotechnol. doi:10.1007/s00253-011-3508-8

  • Cervantes FJ, Vu-Thi-Thu L, Lettinga G, Field JA (2004) Quinone-respiration improves dechlorination of carbon tetrachloride by anaerobic sludge. Appl Microbiol Biotechnol 64:702–711

    Article  PubMed  CAS  Google Scholar 

  • Chen X, Sun G, Xu M (2010) Role of iron in azoreduction by resting cells of Shewanella decolorationis S12. J Appl Microbiol 110:580–586

    Article  PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Dos Santos AB, Cervantes FJ, Van Lier JB (2007) Review paper on current technologies for decolourization of textile wastewaters: perspectives for anaerobic biotechnology. Bioresour Technol 98:2369–2385

    Article  PubMed  Google Scholar 

  • Dubrow SF, Boardman GD, Michelsen DL (1996) Chemical pretreatment and aerobic–anaerobic degradation of textile dye wastewater. In: Reife A and Freeman HS (eds) Environmental chemistry of dyes and pigments. Wiley Interscience, San Diego, CA. pp 75–102

  • Fredrickson JK, Romine MF, Beliaev AS, Auchtung JM, Driscoll ME, Gardner TS, Nealson KH, Osterman AL, Pinchuk G, Reed JL, Rodionov DA, Rodrigues JLM, Saffarini DA, Serres MH, Spormann AM, Zhulin IB, Tiedje JM (2008) Towards environmental systems biology of Shewanella. Nat Rev Microbiol 6:592–603

    Article  PubMed  CAS  Google Scholar 

  • Hong Y, Guo J, Xu Z, Xu M, Sun G (2007a) Humic substances act as electron acceptor and redox mediator for microbial dissimilatory azoreduction by Shewanella decolorationis S12. J Microbiol Biotechnol 17:428–437

    PubMed  CAS  Google Scholar 

  • Hong Y, Xu M, Guo J, Xu Z, Chen X, Sun G (2007b) Respiration and growth of Shewanella decolorationis S12 with an azo compound as sole electron acceptor. Appl Environ Microbiol 73:64–72

    Article  PubMed  CAS  Google Scholar 

  • Hori T, Muller A, Igarashi Y, Conrad R, Friedrich MW (2010) Identification of iron-reducing microorganisms in anoxic rice paddy soil by 13C-acetate probing. ISME J 4:267–278

    Article  PubMed  CAS  Google Scholar 

  • Jahn MK, Haderlein SB, Meckenstock RU (2006) Reduction of Prussian Blue by the two iron-reducing microorganisms Geobacter metallireducens and Shewanella alga. Environ Microbiol 8:362–367

    Article  PubMed  CAS  Google Scholar 

  • Khalid A, Arshad M, Crowley DE (2008) Decolorization of azo dyes by Shewanella sp. under saline conditions. Appl Microbiol Biotechnol 79:1053–1059

    Article  PubMed  CAS  Google Scholar 

  • Kwon MJ, Finneran KT (2006) Microbially mediated biodegradation of hexahydro-1,3,5-trinitro-1,3,5-triazine by extracellular electron shuttling compounds. Appl Environ Microbiol 72:5933–5941

    Article  PubMed  CAS  Google Scholar 

  • Kwon MJ, Finneran KT (2008a) Biotransformation products and mineralization potential for hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) in abiotic versus biological degradation pathways with anthraquinone-2,6-disulfonate (AQDS) and Geobacter metallireducens. Biodegradation 19:705–715

    Article  PubMed  CAS  Google Scholar 

  • Kwon MJ, Finneran KT (2008b) Hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) and octahydro-1,3,5,7-tetranitro-1,3,5,7-tetrazocine (HMX) biodegradation kinetics amongst several Fe(III)-reducing bacteria. Soil Sed Contam 17:189–203

    CAS  Google Scholar 

  • Lin B, Westerhoff HV, Röling WFM (2009) How Geobacteraceae may dominate subsurface biodegradation: physiology of Geobacter metallireducens in slow-growth habitat-stimulating retentostats. Environ Microbiol 11:2425–2433

    Article  PubMed  CAS  Google Scholar 

  • Liu G, Wang J, Lu H, Jin R, Zhou J, Zhang L (2009a) Effects of reduction products of ortho-hydroxyl substituted azo dyes on biodecolorization of azo dyes. J Hazard Mater 171:222–229

    Article  PubMed  CAS  Google Scholar 

  • Liu G, Zhou J, Meng X, Fu QS, Wang J, Jin R, Lv H (2012) Decolorization of azo dyes by marine Shewanella strains under saline conditions. Appl Microbiol Biotechnol. doi:10.1007/s00253-012-4216-8

  • Liu G, Zhou J, Wang J, Wang X, Jin R, Lv H (2011) Decolorization of azo dyes by Shewanella oneidensis MR-1 in the presence of humic acids. Appl Microbiol Biotechnol 91:417–424

    Article  PubMed  CAS  Google Scholar 

  • Liu G, Zhou J, Wang J, Zhou M, Lu H, Jin R (2009b) Acceleration of azo dye decolorization by using quinone reductase activity of azoreductase and quinone redox mediator. Bioresour Technol 100:2791–2795

    Article  PubMed  CAS  Google Scholar 

  • Lloyd JR, Macaskie LE (1996) A novel PhosphorImager-based technique for monitoring the microbial reduction of technetium. Appl Environ Microbiol 62:578–582

    PubMed  CAS  Google Scholar 

  • Lovley DR, Coates JD, Blunt-Harris EL, Phillips EJP, Woodward JC (1996) Humic substances as electron acceptors for microbial respiration. Nature 382:445–448

    Article  CAS  Google Scholar 

  • Lovley DR, Fraga JL, Blunt-Harris EL, Hayes LA, Phillips EJP, Coates JD (1998) Humic substances as a mediator for microbially catalyzed metal reduction. Acta Hydrochim Hydrobiol 26:152–157

    Article  CAS  Google Scholar 

  • Lovley DR, Giovannoni SJ, White DC, Champine JE, Phillips EJP, Gorby YA, Goodwin S (1993) Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch Microbiol 159:336–344

    Article  PubMed  CAS  Google Scholar 

  • Lovley DR, Philips EJP (1988) Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microbiol 54:1472–1480

    PubMed  CAS  Google Scholar 

  • Lovley DR, Phillips EJP, Gorby YA, Landa ER (1991) Microbial reduction of uranium. Nature 350:413–416

    Article  CAS  Google Scholar 

  • Lovley DR, Ueki T, Zhang T, Malvankar NS, Shrestha PM, Flanagan KA, Aklujkar M, Butler JE, Giloteaux L, Rotaru AE, Holmes DE, Franks AE, Orellana R, Risso C, Nevin KP (2011) Geobacter: the microbe electric’s physiology, ecology, and practical applications. Adv Microb Physiol 59:1–100

    Article  PubMed  CAS  Google Scholar 

  • McCormick ML, Adriaens P (2004) Carbon tetrachloride transformation on the surface of nanoscale biogenic magnetite particles. Environ Sci Technol 38:1045–1053

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Meng X, Liu G, Zhou J, Fu QS, Wang G (2012) Azo dye decolorization by Shewanella aquimarina under saline conditions. Bioresour Technol 114:95–101

    Article  PubMed  CAS  Google Scholar 

  • Ortiz-Bernad I, Anderson RT, Vrionis HA, Lovley DR (2004) Vanadium respiration by Geobacter metallireducens: novel strategy for in situ removal of vanadium from groundwater. Appl Environ Microbiol 70:3091–3095

    Article  PubMed  CAS  Google Scholar 

  • Pearce CI, Christie R, Boothman C, von Canstein H, Guthrie JT, Lloyd JR (2006) Reactive azo dye reduction by Shewanella strain J18 143. Biotechnol Bioeng 95:692–703

    Article  PubMed  CAS  Google Scholar 

  • Pearce CI, Lloyd JR, Guthrie JT (2003) The removal of colour from textile wastewater using whole bacterial cells: a review. Dyes Pigm 58:179–196

    Article  CAS  Google Scholar 

  • Rau J, Knackmus HJ, Stolz A (2002) Effects of different quinoid redox mediators on the anaerobic reduction of azo dyes by bacteria. Environ Sci Technol 36:1497–1504

    Article  PubMed  CAS  Google Scholar 

  • Roden EE, Scheibe TD (2005) Conceptual and numerical model of uranium(VI) reductive immobilization in fractured subsurface sediments. Chemosphere 59:617–628

    Article  PubMed  CAS  Google Scholar 

  • Saratale RG, Saratale GD, Chang JS, Govindwar SP (2011) Bacterial decolorization and degradation of azo dyes: a review. J Taiwan Inst Chem Engrs 42:138–157

    Article  CAS  Google Scholar 

  • Stolz A (2001) Basic and applied aspects in the microbial degradation of azo dyes. Appl Microbiol Biotechnol 56:69–80

    Article  PubMed  CAS  Google Scholar 

  • Tremblay PL, Aklujkar M, Leang C, Nevin KP, Lovley DR (2011) A genetic system for Geobacter metallireducens: role of the flagellin and pilin in the reduction of Fe(III) oxide. Environ Microbiol Rep 4:82–88

    Article  PubMed  Google Scholar 

  • Van der Zee FP, Cervantes FJ (2009) Impact and application of electron shuttles on the redox (bio)transformation of contaminants: a review. Biotechnol Adv 27:256–277

    Article  PubMed  Google Scholar 

  • Van Trump JI, Sun Y, Coates JD (2006) Microbial interactions with humic substances. Adv Appl Microbiol 60:55–96

    Article  PubMed  Google Scholar 

  • Wang X, Cheng X, Sun D (2008) Autocatalysis in reactive black 5 biodecolorization by Rhodopseudomonas palustris W1. Appl Microbiol Biotechnol 80:907–915

    Article  PubMed  CAS  Google Scholar 

  • Wolf M, Kappler A, Jiang J, Meckenstock RU (2009) Effects of humic substances and quinones at low concentrations on ferrihydrite reduction by Geobacter metallireducens. Environ Sci Technol 43:5679–5685

    Article  PubMed  CAS  Google Scholar 

  • Xu H, Heinze TM, Chen S, Cerniglia CE, Chen H (2007) Anaerobic metabolism of 1-amino-2-naphthol-based azo dyes (Sudan dyes) by human intestinal microflora. Appl Environ Microbiol 73:7759–7762

    Article  PubMed  CAS  Google Scholar 

  • Yang YY, Du LN, Wang G, Jia XM, Zhao YH (2011) The decolorisation and mechanism of Shewanella oneidensis MR-1 for methyl orange and acid yellow 199 under microaerophilic conditions. Water Sci Technol 63:956–963

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The work was financially supported by National Natural Science Foundation of China (No. 51008044, 50978040), Fundamental Research Funds for the Central Universities, and China Postdoctoral Science Foundation (201104596).

Author information

Authors and Affiliations

  1. Key Laboratory of Industrial Ecology and Environmental Engineering (Ministry of Education), School of Environmental Science and Dalian University of Technology, Dalian, 116024, Republic of China

    Guangfei Liu, Jiti Zhou, Congcong Chen, Jing Wang, Ruofei Jin & Hong Lv

Authors
  1. Guangfei Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiti Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Congcong Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ruofei Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hong Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jing Wang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 208 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, G., Zhou, J., Chen, C. et al. Decolorization of azo dyes by Geobacter metallireducens . Appl Microbiol Biotechnol 97, 7935–7942 (2013). https://doi.org/10.1007/s00253-012-4545-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-012-4545-7

Keywords

Search

Navigation