Abstract
Cupriavidus metallidurans CH34 and related strains are adapted to metal contaminated environments. A strong resistance to environmental stressors and adaptation make it ideal strains for survival in decreasing biodiversity conditions and for bioaugmentation purposes in environmental applications. The soil bacterium C. metallidurans is able to grow chemolithoautotrophically on hydrogen and carbon dioxide allowing a strong resilience under conditions lacking organic matter. The biofilm growth on soil particles allows coping with starvation or bad conditions of pH, temperature and pollutants. Its genomic capacity of two megaplasmids encoding several heavy metal resistance operons allowed growth in heavy metal contaminated habitats. In addition its specific siderophores seem to play a role in heavy metal sequestration besides their role in the management of bioavailable iron. Efflux ATPases and RND systems pump the metal cations to the membrane surface where polysaccharides serve as heavy metal binding and nucleation sites for crystallisation of metal carbonates. These polysaccharides contribute also to flotation under specific conditions in a soil-heavy metals–bacteria suspension mixture. An inoculated moving bed sand filter was constructed to treat heavy metal contaminated water and to remove the metals in the form of biomass mixed with metal carbonates. A membrane based contactor allowed to use the bacteria as well in a versatile wastewater treatment system and to grow homogeneously formed heavy metal carbonates. Its behaviour toward heavy metal binding and flotation was combined in a biometal sludge reactor to extract and separate heavy metals from metal contaminated soils. Finally its metal-induced heavy metal resistance allowed constructing whole cell heavy metal biosensors which, after contact with contaminated soil, waste, solids, minerals and ashes, were induced in function of the bioavailable concentration (Cd, Zn, Cu, Cr, Co, Ni, Tl, Pb and Hg) in the solids and allowed to investigate the speciation of immobilization of those metals.
This is a preview of subscription content, access via your institution.









Abbreviations
- CDM:
-
Cellular dry matter
- RND:
-
Metal resistance, nodulation and cell division
- MERESAFIN:
-
Metal removal by sand filter inoculation
- BICMER:
-
Bacteria immobilized composite membrane reactor
- TCE:
-
3-Chlorobenzoate, trichloroethylene
- PAH:
-
Polyaromatic hydrocarbons
- Cop D:
-
Copper resistance protein D
References
Bulich AA, Isenberg DL (1981) Use of the luminescent bacterial system for the rapid assessment of aquatic toxicity. ISA Trans 20:29–33
Coenye T, Spilker T, Reik R, Vandamme P, Lipuma JJ (2005) Use of PCR analyses to define the distribution of Ralstonia species recovered from patients with cystic fibrosis. J Clin Microbiol 43:3463–3466
Collard JM, Corbisier P, Diels L, Dong Q, Jeanthon C, Mergeay M, Taghavi S, van der Lelie D, Wilmotte A, Wuertz S (1994) Plasmids for heavy metal resistance in Alcaligenes eutrophus CH34: mechanisms and applications. FEMS Microbiol Rev 14:405–414
Corbisier P, Thiry E, Diels L (1996) Bacterial biosensors for the toxicity assessment of solid wastes. Environ Tox Water Qual 11:171–177
Corbisier P, van der Lelie D, Borremans B, Provoost A, de Lorenzo V, Brown NL, Lloyd JR, Hobman JL, Csöregi E, Johansson G, Mattiason B (1999) Whole cell-protein-based biosensors for the detection of bioavailable heavy metals in environmental samples. Anal Clin Acta 387:235–244
Corbisier P, Diels L, Illangasekare T, Reible D, Reinhard M, Vangronsveld J (2002) Mobility and availability of contaminants. In: Reible D, Demnerova K (eds) Innovative appraoches to the on-site assessment, remediation of contaminated sites. Kluwer, The Netherlands, pp 31–65
Diels L (1997) Heavy metal bioremediation of soil. In: Sheehan D (ed) Methods in biotechnology, vol 2: bioremediation protocols. Humana press, Totowa, pp 283–295
Diels L, Mergeay M (1990) DNA probe mediated detection of resistant bacteria from soils highly polluted by heavy metals. Appl Environ Microbiol 56:1485–1491
Diels L, Sadouk A, Mergeay M (1989) Large plasmids governing multiple resistances to heavy metals: a genetic approach. Toxicol Environ Chem 23:79–89
Diels L, Carpels M, Geuzens P, Mergeay M, Rymen T (1992) Method and device for cleaning soil polluted by at least one heavy metal. European Patent 92,203,049.9
Diels L, Van Roy S, Mergeay M, Doyen W, Taghavi S, Leysen R (1993) Immobilization of bacteria in composite membranes and development of tubular membrane reactors for heavy metal recuperation. In Third international conference on effective membrane processes—New perspectives, Paterson R (ed), BHR Group Conference Series, Publication no. 3, 275–293
Diels L, Dong Q, van der Lelie D, Baeyens W, Mergeay M (1995a) The czc operon of Alcaligenes eutrophus CH34: from resistance mechanism to the removal of heavy metals. J Industr Microbiol 124:142–153
Diels L, Van Roy S, Somers K, Willems I, Doyen W, Mergeay M, Springael D, Leysen R (1995b) The use of bacteria immobilized in tubular membrane reactors for heavy metal recovery and degradation of chlorinated aromatics. J Memb Sci 100:249–258
Diels L, Van Roy S, Dong Q, Dresselaers T, Hennen A, Ryngaert A, Peys K, Springael D (1996a) Molecular approaches in biofilm studies of membrane reactors. Med Fac Landbouww Univ Gent 61/4b:1917–1924
Diels L, Van Roy S, Leysen R, Mergeay M (1996b) Heavy metal bioprecipitation by Alcaligenes Eutrophus CH34 immobilized in a membrane bioreactor. Intern Biodet Biodegr 37:239
Diels L, De Smet M, Hooyberghs L, Corbisier P (1999) Heavy metals bioremediation of soil. Molec Biotech 12:149–158
Diels L, Spaans PH, Van Roy S, Hooyberghs L, Wouters H, Walter E, Winters J, Macaskie L, Finlay J, Pernfuss B, Woebking H, Pümpel T (2003) Heavy metals removal by sand filters inoculated with metal sorbing and precipitating bacteria. Hydrometallurgy 71:235–241
Dong Q, Mergeay M (1994) Czc/cnr efflux: a three-component chemiosmotic antiport pathway with a 12-transmembrane-helix protein. Mol Microbiol 14:185–187
Gilis A, Khan AM, Cornelis P, Meyer JM, Mergeay M, van der Lelie D (1996) Siderophore-mediated iron uptake in Alcaligenes eutrophus CH34 and identification of aleB encoding the ferric-alcaligin E receptor. J Bacteriol 178:5499–5507
Höfte M, Dong Q, Kourambos S, Krishnapillai V, Sherratt D, Mergeay M (1994) The sss gene product, which affects pyoverdin production in Pseudomonas aeruginosa 7NSK2, is a site-specific recombinase. Mol Microbiol 14:1011–1020
Kefala MI, Zouboulis AI, Matis KA (1999) Biosorption of cadmium ions by Actinomycetes and separation by flotation. Environ Pollut 104:283–293
Leysen R, Doyen W(1987) European patent specification for Zirfon membranes. EP0241995 (B1)
Liu YG, Huang N (1998) Efficient amplification of insert end sequences from bacterial artificial chromosome clones by thermal asymmetric interlaced PCR. Plant Mol Biol Rep 16:175–181
Magrisso S, Erel Y, Belkin S (2008) Microbial reporters of metal bioavailability. Microb Biotechnol 1:320–330
Mergeay M (1991) Towards an understanding of the genetics of bacterial metal resistance. Trends Biotechnol 9:17–24
Mergeay M (2000) Bacteria adapted to industrial biotopes: the metal resistant Ralstonia. In: GSaR Hengge-Aronis (ed) Bacterial stress responses. ASM Press, Washington D.C., pp 403–414
Mergeay M, Houba C, Gerits J (1978) Extrachromosomal inheritance controlling resistances to Cd++, Zn++, and Co++ ions: evidence from curing in a Pseudomonas. Arch Intern Physiol Bioch 86:440–441
Mergeay M, Nies D, Schlegel G, Gerits J, Van Gijsegem F (1985) Alcaligenes eutrophus CH34, a facultative chemolithotroph displaying plasmid bound resistance to heavy metals. J Bacteriol 162:328–334
Mergeay M, Sadouk A, Diels L, Faelen M, Gerits J, Denecke J, Powell B (1987) High level spontaneous mutagenesis revealed by survival at non-optimal temperature in Alcaligenes eutrophus CH34. Arch Inter Physiol Bioch 95:35–36
Mergeay M, Monchy S, Vallaeys T, Auquier V, Benotmane A, Bertin P, Taghavi S, Dunn J, van der Lelie D, Wattiez R (2003) Ralstonia metallidurans, a bacterium specifically adapted to toxic metals: towards a catalogue of metal-responsive genes. FEMS Microb Rev 27:385–410
Mergeay M, Monchy S, Janssen P, Van Houdt R, Leys N (2009) Megaplasmids in Cupriavidus genus and metal resistance. In: Schwartz E (ed) Microbial megaplasmids. Springer, Berlin, p 320 ISBN: 978-3-540-85466-1
Monchy S, Benotmane MA, Wattiez R, van Aelst S, Auquier V, Borremans B, Mergeay M, Taghavi S, van der Lelie D, Vallaeys T (2006) Transcriptomic and proteomic analyses of the pMOL30-encoded copper resistance in Cupriavidus metallidurans strain CH34. Microbiology 152:1765–1776
Monchy S, Benotmane MA, Janssen P, Vallaeys T, Taghavi S, van der Lelie D, Mergeay M (2007) Plasmids pMOL28 and pMOL30 of Cupriavidus metallidurans are specialized in the maximal viable response to heavy metals. J Bacteriol 189:7417–7425
Peys K, Diels L, Leysen R, Vandecasteele C (1997) Development of a membrane biofilm reactor for the degradation of chlorinated aromatics. Water Sci Tech 36:205–214
Podda F, Zuddas P, Minacci A, Pepi M, Baldi F (2000) Heavy metal co-precipitation with hydrozincite [Zn(5)(CO(3))(2)(OH)(6)] from mine waters caused by photosynthetic microorganisms. Appl Environ Microbiol 11:5092–5098
Pümpel T, Ebner C, Pernfuss B, Schinner F, Diels L, Keszthelyi Z, Macaskie L, Tsezos M, Wouters H (2001) Removal of nickel from plating rinsing water by a moving-bed sandfilter inoculated with metal sorbing and precipitating bacteria. Hydrometallurgy 59:383–393
Ruttens A, Mench M, Colpaert JV, Boisson J, Carleer R, Vangronsveld K (2006) Phytostabilization of a metal contaminated sandy soil. I: Influence of compost and/or inorganic metal immobilizing soil amendments on phytotoxicity and plant availability of metals. Environ Poll 144:524–532
Saier MH, Tam R, Reizer A, Reizer J (1994) Two novel families of bacterial membrane proteins concerned nodulation, cell division and transport. Mol Microbiol 11:841–847
Sato Y, Nishihara H, Yoshida M, Watanabe M, Rondal JD, Concepcion RN, Ohta H (2006) Cupriavidus pinatubonensis sp. nov. and Cupriavidus laharis sp. nov., novel hydrogen-oxidizing, facultatively chemolithotrophic bacteria isolated from volcanic mudflow deposits from Mt. Pinatubo in the Philippines. Int J Syst Evol Microbiol 56:973–978
Schultze-Lam S, Harauz G, Beveridge TS (1992) Participation of cyanobacterial S layer in fine grain mineral formation. J Bacteriol 174:7971–7981
Shaw JJ, Settles LG, Kado CI (1988) Transposon Tn4431 mutagenesis of Xanthomonas campestris pv Campestris. Characterisation of a non-pathogenic mutant and cloning of a locus for pathogenicity. Mol Plant–Microbe Interact 1:39–45
Springael D, Peys K, Ryngaert A, Van Roy S, Hooyberghs L, Ravatn R, Heyndrickx M, van der Meer JR, Vandecasteele C, Mergeay M, Diels L (2002) Community shifts in a seeded 3-chlorobenzoate degrading membrane biofilm reactor: indications for involvement of in situ horizontal transfer of the clc-element from inoculum to contaminant bacteria. Environ Microbiol 4:70–80
Tesseir A, Campbell PGC, Bisson M (1979) Sequential extraction procedure for the speciation of particulate trace metals. Anal Chem 51:844–850
Tibazarwa C, Wuerz S, Mergeay M, Wyns L, van der Lelie D (2001) A microbial biosensor to predict bioavailable nickel in soil and its transfer to plants. Environ Pollut 113:19–26
Van Assche F, Clijsters H (1990) A biological test system for the evaluation of the phytotoxicity of metal contaminated soils. Environ Pollut 66:157–172
Van der Lelie D, Verschaeve L, Regniers L, Corbisier P (2000) Use of bacterial tests (the VITOTOX (R) genotoxicity test and the BIOMET heavy metal test) to analyze chemicals and environmental samples. In: Personne G, Janssen C (eds) New microbiotests for routine toxicity screening and biomonitoring. Kluwer Academic Publishers, New York, pp 197–207
Volesky B (2003) Biosorption process simulation tools. Hydrometallurgy 71:179−190
Woebking H, Diels L (2000) Abreicherung und Rückgewinnung von Eisen and Nichteisenmetallen aus industriellen Abwässeren unter Verwendung eines Bakterien geimpften Sandfilters. Berg- and Hüttenmännische Monatshefte 7:265–270
Wuertz S, Mergeay M (1997) The impact of heavy metals on soil microbial communities and their activities. In: van Elsas D, Wellington E, Trevors J (eds) Modern soil microbiology. Marcel Dekker Publisher, New York, pp 607–642
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Diels, L., Van Roy, S., Taghavi, S. et al. From industrial sites to environmental applications with Cupriavidus metallidurans . Antonie van Leeuwenhoek 96, 247–258 (2009). https://doi.org/10.1007/s10482-009-9361-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-009-9361-4
Keywords
- Anaerobic reactors
- Bioavailability
- Biosensors
- Cupriavidus metallidurans
- Heavy metals
- Heavy metal resistance
- Moving bed sand filter
- Soil remediation
- Water treatment