Abstract
Forty percent of hazardous waste sites in the United States are co-contaminated with organic and metal pollutants. Data from both aerobic and anaerobic systems demonstrate that biodegradation of the organic component can be reduced by metal toxicity. Metal bioavailability, determined primarily by medium composition/soil type and pH, governs the extent to which metals affect biodegradation. Failure to consider bioavailability rather than total metal likely accounts for much of the enormous variability among reports of inhibitory concentrations of metals. Metals appear to affect organic biodegradation through impacting both the physiology and ecology of organic degrading microorganisms. Recent approaches to increasing organic biodegradation in the presence of metals involve reduction of metal bioavailability and include the use of metal-resistant bacteria, treatment additives, and clay minerals. The addition of divalent cations and adjustment of pH are additional strategies currently under investigation.
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- ABELSON P. H., ALDOUS E. Ion antagonisms in microorganisms; interference of normal magnesium metabolism by nickel, cobalt, cadmium, zinc, and manganese. J Bacteriol. 1950 Oct;60(4):401–413. doi: 10.1128/jb.60.4.401-413.1950. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Al-Tahhan R. A., Sandrin T. R., Bodour A. A., Maier R. M. Rhamnolipid-induced removal of lipopolysaccharide from Pseudomonas aeruginosa: effect on cell surface properties and interaction with hydrophobic substrates. Appl Environ Microbiol. 2000 Aug;66(8):3262–3268. doi: 10.1128/aem.66.8.3262-3268.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Amor L., Kennes C., Veiga M. C. Kinetics of inhibition in the biodegradation of monoaromatic hydrocarbons in presence of heavy metals. Bioresour Technol. 2001 Jun;78(2):181–185. doi: 10.1016/s0960-8524(00)00182-6. [DOI] [PubMed] [Google Scholar]
- Angle J. S., Chaney R. L. Cadmium Resistance Screening in Nitrilotriacetate-Buffered Minimal Media. Appl Environ Microbiol. 1989 Aug;55(8):2101–2104. doi: 10.1128/aem.55.8.2101-2104.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Babich H., Devanas M. A., Stotzky G. The mediation of mutagenicity and clastogenicity of heavy metals by physicochemical factors. Environ Res. 1985 Aug;37(2):253–286. doi: 10.1016/0013-9351(85)90107-0. [DOI] [PubMed] [Google Scholar]
- Babich H., Stotzky G. Effect of cadmium on fungi and on interactions between fungi and bacteria in soil: influence of clay minerals and pH. Appl Environ Microbiol. 1977 May;33(5):1059–1066. doi: 10.1128/aem.33.5.1059-1066.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Babich H., Stotzky G. Further studies on environmental factors that modify the toxicity of nickel to microbes. Regul Toxicol Pharmacol. 1983 Mar;3(1):82–99. doi: 10.1016/0273-2300(83)90053-3. [DOI] [PubMed] [Google Scholar]
- Birch L., Brandl H. A rapid method for the determination of metal toxicity to the biodegradation of water insoluble polymers. Anal Bioanal Chem. 1996 Mar;354(5-6):760–762. doi: 10.1007/s0021663540760. [DOI] [PubMed] [Google Scholar]
- Braide V. B. Calcium EDTA toxicity: renal excretion of endogenous trace metals and the effect of repletion on collagen degradation in the rat. Gen Pharmacol. 1984;15(1):37–41. doi: 10.1016/0306-3623(84)90077-6. [DOI] [PubMed] [Google Scholar]
- Capone D. G., Reese D. D., Kiene R. P. Effects of metals on methanogenesis, sulfate reduction, carbon dioxide evolution, and microbial biomass in anoxic salt marsh sediments. Appl Environ Microbiol. 1983 May;45(5):1586–1591. doi: 10.1128/aem.45.5.1586-1591.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Collins Y. E., Stotzky G. Heavy metals alter the electrokinetic properties of bacteria, yeasts, and clay minerals. Appl Environ Microbiol. 1992 May;58(5):1592–1600. doi: 10.1128/aem.58.5.1592-1600.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Forsberg C. W. Effects of heavy metals and other trace elements on the fermentative activity of the rumen microflora and growth of functionally important rumen bacteria. Can J Microbiol. 1978 Mar;24(3):298–306. doi: 10.1139/m78-050. [DOI] [PubMed] [Google Scholar]
- Franklin NM, Stauber JL, Markich SJ, Lim RP. pH-dependent toxicity of copper and uranium to a tropical freshwater alga (Chlorella sp.). Aquat Toxicol. 2000 Mar 1;48(2-3):275–289. doi: 10.1016/s0166-445x(99)00042-9. [DOI] [PubMed] [Google Scholar]
- GUNN S. A., GOULD T. C., ANDERSON W. A. CADMIUM-INDUCED INTERSTITIAL CELL TUMORS IN RATS AND MICE AND THEIR PREVENTION BY ZINC. J Natl Cancer Inst. 1963 Oct;31:745–759. [PubMed] [Google Scholar]
- Gabbiani G., Gregory A., Baic D. Cadmium-induced selective lesions of sensory ganglia. J Neuropathol Exp Neurol. 1967 Jul;26(3):498–506. doi: 10.1097/00005072-196707000-00010. [DOI] [PubMed] [Google Scholar]
- Goldberg S. S., Cordeiro M. N., Silva Pereira A. A., Mares-Guia M. L. Release of lipopolysaccharide (LPS) from cell surface of Trypanosoma cruzi by EDTA. Int J Parasitol. 1983 Feb;13(1):11–18. doi: 10.1016/s0020-7519(83)80062-9. [DOI] [PubMed] [Google Scholar]
- Ibim S. E., Trotman J., Musey P. I., Semafuko W. E. Depletion of essential elements by calcium disodium EDTA treatment in the dog. Toxicology. 1992;73(2):229–237. doi: 10.1016/0300-483x(92)90105-n. [DOI] [PubMed] [Google Scholar]
- Ivanov A. Iu, Fomchenkov V. M., Khasanova L. A., Gavriushkin A. V. Toksicheskoe deistvie gidroksilirovannykh ionov tiazhelykh metallov natsitoplazmaticheskuiu membranu bakterial'nykh kletok. Mikrobiologiia. 1997 Sep-Oct;66(5):588–594. [PubMed] [Google Scholar]
- Ji G., Silver S. Bacterial resistance mechanisms for heavy metals of environmental concern. J Ind Microbiol. 1995 Feb;14(2):61–75. doi: 10.1007/BF01569887. [DOI] [PubMed] [Google Scholar]
- Kachur A. V., Koch C. J., Biaglow J. E. Mechanism of copper-catalyzed oxidation of glutathione. Free Radic Res. 1998 Mar;28(3):259–269. doi: 10.3109/10715769809069278. [DOI] [PubMed] [Google Scholar]
- Kamashwaran S. R., Crawford D. L. Anaerobic biodegradation of pentachlorophenol in mixtures containing cadmium by two physiologically distinct microbial enrichment cultures. J Ind Microbiol Biotechnol. 2001 Jul;27(1):11–17. doi: 10.1038/sj.jim.7000153. [DOI] [PubMed] [Google Scholar]
- Knight B. P., McGrath S. P., Chaudri A. M. Biomass carbon measurements and substrate utilization patterns of microbial populations from soils amended with cadmium, copper, or zinc. Appl Environ Microbiol. 1997 Jan;63(1):39–43. doi: 10.1128/aem.63.1.39-43.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Korkeala H., Pekkanen T. J. The effect of pH and potassium phosphate buffer on the toxicity of cadmium for bacteria. Acta Vet Scand. 1978;19(1):93–101. doi: 10.1186/BF03547645. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kuo C., Genthner B. Effect of added heavy metal ions on biotransformation and biodegradation of 2-chlorophenol and 3-chlorobenzoate in anaerobic bacterial consortia. Appl Environ Microbiol. 1996 Jul;62(7):2317–2323. doi: 10.1128/aem.62.7.2317-2323.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Laddaga R. A., Silver S. Cadmium uptake in Escherichia coli K-12. J Bacteriol. 1985 Jun;162(3):1100–1105. doi: 10.1128/jb.162.3.1100-1105.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leive L. Release of lipopolysaccharide by EDTA treatment of E. coli. Biochem Biophys Res Commun. 1965 Nov 22;21(4):290–296. doi: 10.1016/0006-291x(65)90191-9. [DOI] [PubMed] [Google Scholar]
- Liu C., Jay J. A., Ford T. E. Evaluation of environmental effects on metal transport from capped contaminated sediment under conditions of submarine groundwater discharge. Environ Sci Technol. 2001 Nov 15;35(22):4549–4555. doi: 10.1021/es001763p. [DOI] [PubMed] [Google Scholar]
- Malakul P, Srinivasan KR, Wang HY. Metal toxicity reduction in naphthalene biodegradation by use of metal-chelating adsorbents . Appl Environ Microbiol. 1998 Nov;64(11):4610–4613. doi: 10.1128/aem.64.11.4610-4613.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nies D. H. Resistance to cadmium, cobalt, zinc, and nickel in microbes. Plasmid. 1992 Jan;27(1):17–28. doi: 10.1016/0147-619x(92)90003-s. [DOI] [PubMed] [Google Scholar]
- Nies D. H., Silver S. Ion efflux systems involved in bacterial metal resistances. J Ind Microbiol. 1995 Feb;14(2):186–199. doi: 10.1007/BF01569902. [DOI] [PubMed] [Google Scholar]
- Ogundele M. O. Cytotoxicity of EDTA used in biological samples: effect on some human breast-milk studies. J Appl Toxicol. 1999 Nov-Dec;19(6):395–400. doi: 10.1002/(sici)1099-1263(199911/12)19:6<395::aid-jat590>3.0.co;2-5. [DOI] [PubMed] [Google Scholar]
- Rai L. C., Gaur J. P., Kumar H. D. Protective effects of certain environmental factors on the toxicity of zinc, mercury, and methylmercury to Chlorella vulgaris. Environ Res. 1981 Aug;25(2):250–259. doi: 10.1016/0013-9351(81)90026-8. [DOI] [PubMed] [Google Scholar]
- Roane T. M., Josephson K. L., Pepper I. L. Dual-bioaugmentation strategy to enhance remediation of cocontaminated soil. Appl Environ Microbiol. 2001 Jul;67(7):3208–3215. doi: 10.1128/AEM.67.7.3208-3215.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rogers J. E., Li S. W. Effect of metals and other inorganic ions on soil microbial activity: soil dehydrogenase assay as a simple toxicity test. Bull Environ Contam Toxicol. 1985 Jun;34(6):858–865. doi: 10.1007/BF01609817. [DOI] [PubMed] [Google Scholar]
- Rosner J. L., Aumercier M. Potentiation by salicylate and salicyl alcohol of cadmium toxicity and accumulation in Escherichia coli. Antimicrob Agents Chemother. 1990 Dec;34(12):2402–2406. doi: 10.1128/aac.34.12.2402. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Said W. A., Lewis D. L. Quantitative assessment of the effects of metals on microbial degradation of organic chemicals. Appl Environ Microbiol. 1991 May;57(5):1498–1503. doi: 10.1128/aem.57.5.1498-1503.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sandrin T. R., Chech A. M., Maier R. M. A rhamnolipid biosurfactant reduces cadmium toxicity during naphthalene biodegradation. Appl Environ Microbiol. 2000 Oct;66(10):4585–4588. doi: 10.1128/aem.66.10.4585-4588.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sandrint Todd R., Maier Raina M. Effect of pH on cadmium toxicity, speciation, and accumulation during naphthalene biodegradation. Environ Toxicol Chem. 2002 Oct;21(10):2075–2079. [PubMed] [Google Scholar]
- Selifonova O., Burlage R., Barkay T. Bioluminescent sensors for detection of bioavailable Hg(II) in the environment. Appl Environ Microbiol. 1993 Sep;59(9):3083–3090. doi: 10.1128/aem.59.9.3083-3090.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Silver S. Bacterial resistances to toxic metal ions--a review. Gene. 1996 Nov 7;179(1):9–19. doi: 10.1016/s0378-1119(96)00323-x. [DOI] [PubMed] [Google Scholar]
- Silver S., Phung L. T. Bacterial heavy metal resistance: new surprises. Annu Rev Microbiol. 1996;50:753–789. doi: 10.1146/annurev.micro.50.1.753. [DOI] [PubMed] [Google Scholar]
- Springael D., Diels L., Hooyberghs L., Kreps S., Mergeay M. Construction and characterization of heavy metal-resistant haloaromatic-degrading Alcaligenes eutrophus strains. Appl Environ Microbiol. 1993 Jan;59(1):334–339. doi: 10.1128/aem.59.1.334-339.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sterritt R. M., Lester J. N. Interactions of heavy metals with bacteria. Sci Total Environ. 1980 Jan;14(1):5–17. doi: 10.1016/0048-9697(80)90122-9. [DOI] [PubMed] [Google Scholar]
- Traina S. J., Laperche V. Contaminant bioavailability in soils, sediments, and aquatic environments. Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):3365–3371. doi: 10.1073/pnas.96.7.3365. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zoumis T., Schmidt A., Grigorova L., Calmano W. Contaminants in sediments: remobilisation and demobilisation. Sci Total Environ. 2001 Feb 5;266(1-3):195–202. doi: 10.1016/s0048-9697(00)00740-3. [DOI] [PubMed] [Google Scholar]