Skip to main content

Advertisement

SpringerLink
Log in

Pilot plant for bioremediation of mercury-containing industrial wastewater

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Mercury is an extremely toxic pollutant that is currently being emitted mainly by low level industrial sources. It is distributed globally through the atmosphere, from where it precipitates onto the surface of the Earth, enters aquatic organisms, accumulates in fish and finally affects the health of human populations. Microbes have evolved a mechanism for mercury detoxification [mercury resistance operon (mer)] based on intracellular reduction of Hg2+ to non-toxic Hg0 by the mercuric reductase enzyme and subsequent diffusional loss of Hg0 from the cell. It was shown that Hg0 produced by microbial detoxification can be retained quantitatively in packed bed bioreactors, in which biofilms of mercury-resistant bacteria are grown on porous carrier material. This review describes operation of this system on a technical, fully automated, scale, and its operation at a chloralkali electrolysis factory. It was shown to work with high efficiency under fluctuating mercury concentrations and to be robust against transiently toxic conditions. The gradient of mercury concentration in the technical scale system exerted a strong selective pressure on the microbial community, which resulted in a succession of mercury-resistant strains at high mercury concentrations and an increase in phylogenetic and functional diversity at low mercury concentrations. Clean-up of mercury-containing wastewater by mercury-resistant microbes is a simple, environmentally friendly and cost-effective alternative to current treatment technologies.

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.
Fig. 6.

Similar content being viewed by others

References

  • Amin-Zaki L, Elhassani S, Majeed MA, Clarkson RW, Doherty R, Greenwood MR, Giovanoli-Jakubczak R (1976) Perinatal methylmercury poisoning in Iraq. Am J Dis Child 130:1070–1076

    CAS  PubMed  Google Scholar 

  • Bae W, Chen W, Mulchandani A, Mehra RK (2000) Enhanced bioaccumulation of heavy metals by bacterial cells displaying synthetic phytochelatins. Biotechnol Bioeng 70:518–524

    Article  CAS  PubMed  Google Scholar 

  • Bae W, Mehra RK, Mulchandani A, Chen W (2001) Genetic engineering of Escherichia coli for enhanced uptake and bioaccumulation of mercury. Appl Environ Microbiol 67:5335–5338

    Article  CAS  PubMed  Google Scholar 

  • Bae W, Mulchandani A, Chen W (2002) Cell surface display of synthetic phytochelatins using ice nucleation protein for enhanced heavy metal bioaccumulation. J Inorg Biochem 88:223–227

    Article  CAS  PubMed  Google Scholar 

  • Bang SS, Pazirandeh M (1999) Physical properties and heavy metal uptake of encapsulated Escherichia coli expressing a metal binding gene (NCP). J Microencapsul 16:489–499

    Article  CAS  PubMed  Google Scholar 

  • Barkay T (2000) Mercury cycle. Encyclopedia of microbiology 3:171–181

    CAS  Google Scholar 

  • Barkay T, Schaefer J (2001) Metal and radionuclide bioremediation: issues, considerations and potentials. Curr Opin Microbiol 4:318–323

    CAS  PubMed  Google Scholar 

  • Becker FU (1996) Stofftransportraten und Reaktionsgeschwindigkeit der Hg-Biotransformation in Mehrphasenreaktoren. PhD Dissertation, Technical University of Braunschweig.

  • Benoit JM, Gilmour CC, Mason RP (2001a) Aspects of bioavailability of mercury for methylation in pure cultures of Desulfobulbus propionicus (1pr3). Appl Environ Microbiol 67:51–58

    Article  CAS  PubMed  Google Scholar 

  • Benoit JM, Gilmour CC, Mason RP (2001b) The influence of sulfide on solid-phase mercury bioavailability for methylation by pure cultures of Desulfobulbus propionicus (1pr3). Environ Sci Technol 35:127–132

    CAS  PubMed  Google Scholar 

  • Bizily SP, Rugh CL, Summers AO, Meagher RB (1999) Phytoremediation of methylmercury pollution: merB expression in Arabidopsis thaliana confers resistance to organomercurials. Proc Natl Acad Sci USA 96:6808–6813

    Article  PubMed  Google Scholar 

  • Bizily SP, Rugh CL, Meagher RB (2000) Phytodetoxification of hazardous organomercurials by genetically engineered plants. Nat Biotechnol 18:213–217

    Article  PubMed  Google Scholar 

  • Braune B, Muir D, DeMarch B, Gamberg M, Poole K, Currie R, Dodd M, Duschenko W, Eamer J, Elkin B, Evans M, Grundy S, Hebert C, Johnstone R, Kidd K, Koenig B, Lockhart L, Marshall H, Reimer K, Sanderson J, Shutt L (1999) Spatial and temporal trends of contaminants in Canadian Arctic freshwater and terrestrial ecosystems: a review. Sci Total Environ 230:145–207

    Article  CAS  PubMed  Google Scholar 

  • Brim H, McFarlan SC, Fredrickson JK, Minton KW, Zhai M, Wackett LP, Daly MJ (2000) Engineering Deinococcus radiodurans for metal remediation in radioactive mixed waste environments. Nat Biotechnol 18:85–90

    Article  CAS  PubMed  Google Scholar 

  • Brunke M, Deckwer WD, Frischmuth A, Horn JM, Lunsdorf H, Rhode M, Rohricht M, Timmis KN, Weppen P (1993) Microbial retention of mercury from waste streams in a laboratory column containing merA gene bacteria. FEMS Microbiol Rev 11:145–152

    Article  CAS  PubMed  Google Scholar 

  • Canstein H von, Li Y, Timmis KN, Deckwer WD, Wagner-Döbler I (1999) Removal of mercury from chloralkali electrolysis wastewater by a mercury-resistant Pseudomonas putida strain. Appl Environ Microbiol 65:5279–5284

    PubMed  Google Scholar 

  • Canstein H von, Li Y, Wagner-Döbler I (2001a) Long-term performance of bioreactors cleaning mercury-contaminated wastewater and their response to temperature and mercury stress and mechanical perturbation. Biotechnol Bioeng 74:212–219

    Article  PubMed  Google Scholar 

  • Canstein H von, Li Y, Wagner-Döbler I (2001b) Long-term stability of mercury reducing microbial biofilm communities analysed by 16S-23S rDNA interspacer region polymorphism. Microb Ecol 42:624–634

    Article  PubMed  Google Scholar 

  • Canstein H von, Li Y, Leonhauser J, Haase E, Felske A, Deckwer WD, Wagner-Döbler I (2002a) Spatially oscillating activity and microbial succession of mercury-reducing biofilms in a technical-scale bioremediation system. Appl Environ Microbiol 68:1938–1946

    Article  PubMed  Google Scholar 

  • Canstein H von, Kelly S, Li Y, Timmis KN, Wagner-Döbler I (2002b) Species diversity improves the efficiency of mercury-reducing biofilms under changing environmental conditions. Appl Environ Microbiol 68:2829–2837

    Article  PubMed  Google Scholar 

  • Chang JS, Law WS (1998) Development of microbial mercury detoxification processes using mercury-hyperresistant strain of Pseudomonas aeruginosa PU21. Biotechnol Bioeng 57:462–470

    Article  CAS  PubMed  Google Scholar 

  • Chang JS, Chao YP, Law WS (1998) Repeated fed-batch operations for microbial detoxification of mercury using wild-type and recombinant mercury-resistant bacteria. J Biotechnol 64:219–230

    Article  CAS  PubMed  Google Scholar 

  • Chen SL, Wilson DB (1997a) Construction and characterization of Escherichia coli genetically engineered for bioremediation of Hg2+-contaminated environments. Appl Environ Microbiol 63:2442–2445

    CAS  PubMed  Google Scholar 

  • Chen SL, Wilson DB (1997b) Genetic engineering of bacteria and their potential for Hg2+ bioremediation. Biodegradation 8:97–103

    Article  CAS  PubMed  Google Scholar 

  • Chen SL, Kim EK, Shuler ML, Wilson DB (1998) Hg2+ removal by genetically engineered Escherichia coli in a hollow fiber bioreactor. Biotechnol Prog 14:667–671

    Article  CAS  PubMed  Google Scholar 

  • Clarkson TW (1992) Mercury: major issues in environmental health. Environ Health Perspect 100:31–38

    Google Scholar 

  • Daly MJ (2000) Engineering radiation-resistant bacteria for environmental biotechnology. Curr Opin Biotechnol 11:280–285

    Article  CAS  PubMed  Google Scholar 

  • Danhamer H (1995) Ermittlung und Modellierung der Kinetik der Biotransformation von Hg2+ zu Hg0 durch Pseudomonas putida KT2442::mer-73. Diploma Thesis, Technical University of Braunschweig

  • Ebinghaus R, Kock HH, Temme C, Einax JW, Lowe AG, Richter A, Burrows JP, Schroeder WH (2002) Antarctic springtime depletion of atmospheric mercury. Environ Sci Technol 36:1238–1244

    Google Scholar 

  • Eccles H (1999) Treatment of metal-contaminated wastes: why select a biological process? Trends Biotechnol 17:462–465

    Google Scholar 

  • EPA (1997) Locating and estimating air emissions from sources of mercury and mercury compounds. EPA-454/R-97–012. US Environmental Protection Agency, Research Triangle Park, N.C.

  • EPA (2000) Mercury research strategy. EPA/600/R-00/073. US Environmental Protection Agency, Cincinnati, Ohio

  • European Commission (2000) Reference document on best available techniques in the chlor-alkali manufacturing industry. Integrated pollution prevention and control (IPPC). European Commission, Directorate General, Joint Research Centre, Institute for Prospective Technologcal Studies Seville, Technologies for Sustainable Development, and European IPPC Bureau. World Trade Center, Seville, Spain

  • Felske A, Pauling BV, von Canstein HF, Li Y, Lauber J, Buer J, Wagner-Döbler I (2001) Detection of small sequence differences using competitive PCR: molecular monitoring of genetically improved, mercury reducing bacteria. Biotechniques 30:142–148

    CAS  PubMed  Google Scholar 

  • Frischmuth A, Weppen P, Deckwer WD (1991) Quecksilberentfernung aus wässrigen Medien durch aktive mikrobielle Prozesse. Bioengineering 7:38

    CAS  Google Scholar 

  • Fry JC, Gadd G, Herbert RA, Jones CW, Watson-Craik IA (ed) (1992) Microbial control of pollution. Proceedings of the 48th symposium of the Society for General Microbiology held at the University of Cardiff, March 1992. Cambridge University Press

  • Gadd GM (2000) Bioremedial potential of microbial mechanisms of metal mobilization and immobilization. Curr Opin Biotechnol 11:271–279

    CAS  PubMed  Google Scholar 

  • Horn JM, Brunke M, Deckwer WD, Timmis KN (1994) Pseudomonas putida strains which constitutively overexpress mercury resistance for biodetoxification of organomercurial pollutants. Appl Environ Microbiol 60:357–362

    CAS  Google Scholar 

  • Ji G, Silver S (1995) Bacterial resistance mechanisms for heavy metals of environmental concern. J Ind Microbiol 14:61–75

    CAS  PubMed  Google Scholar 

  • Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76

    CAS  PubMed  Google Scholar 

  • Lorenzo V de, Kuenen G (1999) Scientific basis for the bioremediation of the toxic spill of the Aznalcollar mine: combining bacteria and plants to address and intractable kind of pollution. Environ Microbiol 1:275–278

    Article  PubMed  Google Scholar 

  • Lovley DR (ed) (2000) Environmental microbe-metal interactions. ASM Press, Washington, D.C.

  • Macdonald RW, Barrie LA, Bidleman TF, Diamond ML, Gregor DJ, Semkin RG, Strachan WM, Li YF, Wania F, Alaee M, Alexeeva LB, Backus SM, Bailey R, Bewers JM, Gobeil C, Halsall CJ, Harner T, Hoff JT, Jantunen LM, Lockhart WL, Mackay D, Muir DC, Pudykiewicz J, Reimer KJ, Smith JN, Stern GA (2000) Contaminants in the Canadian Arctic: 5 years of progress in understanding sources, occurrence and pathways. Sci Total Environ 254:93–234

    Article  CAS  PubMed  Google Scholar 

  • Means JL, Hinchee RE (1994) Emerging technology for bioremediation of metals. Lewis, Boca Raton, Fla.

  • Misra TK (1992) Bacterial resistances to inorganic mercury salts and organomercurials. Plasmid 27:4–16

    CAS  PubMed  Google Scholar 

  • Moller S, Sternberg C, Andersen JB, Christensen BB, Ramos JL, Givskov M, Molin S (1998) In situ gene expression in mixed-culture biofilms: evidence of metabolic interactions between community members. Appl Environ Microbiol 64:721–732

    CAS  PubMed  Google Scholar 

  • Muir D, Braune B, DeMarch B, Norstrom R, Wagemann R, Lockhart L, Hargrave B, Bright D, Addison R, Payne J, Reimer K (1999) Spatial and temporal trends and effects of contaminants in the Canadian Arctic marine ecosystem: a review. Sci Total Environ 230:83–144

    Article  CAS  PubMed  Google Scholar 

  • Mulder CPH, Uliassi DD, Doak DF (2001) Physical stress and diversity-productivity relationships: the role of positive interactions. Proc Natl Acad Sci USA 98:6704–6708

    Article  CAS  PubMed  Google Scholar 

  • Nielsen AT, Tolker-Nielsen T, Barken KB, Molin S (2000) Role of commensal relationships on the spatial structure of a surface-attached microbial consortium. Environ Microbiol 2:59–68

    Article  CAS  PubMed  Google Scholar 

  • Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51:730–750

    Article  CAS  PubMed  Google Scholar 

  • Osborn AM, Bruce KD, Strike P, Ritchie DA (1997) Distribution, diversity and evolution of the bacterial mercury resistance (mer) operon. FEMS Microbiol Rev 19:239–262

    Article  CAS  PubMed  Google Scholar 

  • Pazirandeh M, Wells BM, Ryan RL (1998) Development of bacterium-based heavy metal biosorbents: enhanced uptake of cadmium and mercury by Escherichia coli expressing a metal binding motif. Appl Environ Microbiol 64:4068–4072

    CAS  PubMed  Google Scholar 

  • Pümpel T, Paknikar K (2001) Bioremediation technologies for metal-containing wastewaters using metabolically active microorganisms. In: Laskin AI, Bennett JW, Gadd G (eds), vol. 48. Academic Press, San Diego, pp 135–171

  • Röhricht M (1993) Mikrobielle Verfahren zur Entfernung von Schwermetallen aus wässrigen Lösungen im Vergleich zu Ionenaustauschern. PhD Thesis, Technical University of Braunschweig

  • Rugh CL, Wilde HD, Stack NM, Thompson DM, Summers AO, Meagher RB (1996) Mercuric ion reduction and resistance in transgenic Arabidopsis thaliana plants expressing a modified bacterial merA gene. Proc Natl Acad Sci USA 93:3182–3187

    Article  CAS  PubMed  Google Scholar 

  • Rugh CL, Senecoff JF, Meagher RB, Merkle SA (1998) Development of transgenic yellow poplar for mercury phytoremediation. Nat Biotechnol 16:925–928

    CAS  PubMed  Google Scholar 

  • Saouter E, Turner R, Barkay T (1994) Microbial reduction of ionic mercury for the removal of mercury from contaminated environments. Ann N Y Acad Sci 721:423–427

    CAS  PubMed  Google Scholar 

  • Sayler GS, Ripp S (2002) Field applications of genetically engineered microorganisms for bioremediation processes. Curr Opin Biotechnol 11:286–289

    Article  Google Scholar 

  • Schaefer JK, Letowski J, Barkay T (2002) mer-Mediated resistance and volatilization of Hg(II) under anaerobic conditions. Geomicrobiology 19:87–102

    CAS  Google Scholar 

  • Schiering N, Kabsch W, Moore MJ, Distefano MD, Walsh CT, Pai EF (1991) Structure of the detoxification catalyst mercuric ion reductase from Bacillus sp. strain RC607. Nature 352:168–172

    CAS  PubMed  Google Scholar 

  • Schrope M (2001) US to take temperature of mercury threat. Nature 409:124

    Article  CAS  Google Scholar 

  • Sigel A, Sigel H (eds) (1997) Metal ions in biological systems. mercury and its effects on environment and biology, vol 34. Dekker, New York

  • Smith T, Pitts K, McGarvey JA, Summers AO (1998) Bacterial oxidation of mercury metal vapor, Hg(0). Appl Environ Microbiol 64:1328–1332

    CAS  PubMed  Google Scholar 

  • Souza MP de, Huang CP, Chee N, Terry N (1999) Rhizosphere bacteria enhance the accumulation of selenium and mercury in wetland plants. Planta 209:259–263

    Article  PubMed  Google Scholar 

  • Strasdeit H, von Döllen A, Saak W, Wilhelm M (2000) Intrazellulärer Abbau von Diorganoquecksilber-Verbindungen durch biologische Thiole—Einblicke aus Modellreaktionen. Angew Chem 112:803-805

    Article  Google Scholar 

  • Summers AO, Silver S (1972) Mercury resistance in a plasmid-bearing strain of Escherichia coli. J Bacteriol 112:1228–1236

    CAS  PubMed  Google Scholar 

  • Summers AO, Silver S (1978) Microbial transformations of metals. Annu Rev Microbiol 32:637–672

    CAS  PubMed  Google Scholar 

  • Valls M, Atrian S, de Lorenzo V, Fernandez LA (2000) Engineering a mouse metallothionein on the cell surface of Ralstonia eutropha CH34 for immobilization of heavy metals in soil. Nat Biotechnol 18:661–665

    Article  CAS  PubMed  Google Scholar 

  • Wackett LP, Bruce NC (2002) Environmental biotechnology: towards sustainability. Curr Opin Biotechnol 11:229–231

    Article  Google Scholar 

  • Wagner-Döbler I, von Canstein HF, Li Y, Timmis KN, Deckwer WD (2000a) Removal of mercury from chemical wastewater by microorganisms in technical scale. Environ Sci Technol 34:4628–4634

    Article  Google Scholar 

  • Wagner-Döbler I, Lunsdorf H, Lubbehusen T, von Canstein HF, Li Y (2000b) Structure and species composition of mercury-reducing biofilms. Appl Environ Microbiol 66:4559–4563

    Article  PubMed  Google Scholar 

  • Wagner-Döbler I, von Canstein HF, Li Y, Leonhauser J, Deckwer WD (2002) Prozeßintegrierte Quecksilberentfernung aus Abwässern der Chloralkali-Elektrolyse durch Mikroorganismen. Chem Ing Technol 74:504–508

    Article  Google Scholar 

  • Weast RC (1984) CRC handbook of chemistry and physics. CRC Press, Boca Raton, Fla.

  • White C, Sharman AK, Gadd GM (1998) An integrated microbial process for the bioremediation of soil contaminated with toxic metals. Nat Biotechnol 16:572–575

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

I want to thank my students for their motivation, good spirits, careful work, persistence and for many stimulating discussions. Without them, nothing would have happened, and everything would have been much less fun. Wolf-Dieter Deckwer was the engineering backbone, heart and brain of the scale-up from lab scale to technical scale. The operation of the pilot plant would not have been possible without the support of the management at ECI Ibbenbüren (Dieter Saß), Preussag Wassertechnik (Rüdiger Böckle) and Spolchemie (Jindrich Maslo). I would like to especially thank the people at the factories, whose daily maintenance work made our microbes function well: Hans Hardemann and Karen Bartel at ECI Ibbenbüren, Karel Cipra and Jaroslav Dycka at Spolchemie. They were guided and assisted by Johannes Leonhäuser from GBF, a fine example of an engineer who is not only perfect with computers, but does not mind to stick his head deep into a dirty tank. Many thanks also to Kenneth Timmis, who initially saw the potential of this process and firmly stuck to it. And thanks to the European Community who supported our work with three projects (QLRT-1999-01213; BIO4-98-0168; LIFE97 ENV/D/000463).

Author information

Authors and Affiliations

  1. National Research Institute for Biotechnology, Mascheroder Weg 1, 38124, Braunschweig, Germany

    I. Wagner-Döbler

Authors
  1. I. Wagner-Döbler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to I. Wagner-Döbler.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wagner-Döbler, I. Pilot plant for bioremediation of mercury-containing industrial wastewater. Appl Microbiol Biotechnol 62, 124–133 (2003). https://doi.org/10.1007/s00253-003-1322-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-003-1322-7

Keywords

Search

Navigation