Strategies To Mitigate Deleterious Effects Of Metals On microorganisms

Several techniques have been proposed for mitigating the toxicity of metals in the environment. These strategies for enhancing microbial processes, such as litter decomposition, methanogenesis, acidogenesis, nitrogen transformation, and biodegradation of organics, include using metal-resistant bacteria,84 treatment additives,141 clay minerals,112 and chelating agents.122 The manipulation of

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FIGURE 11.1 Effect of pH on microbial gene expression responses to cadmium. Examples of a stress response gene (yciM), a transport-related gene (ynfM), an oxidoreductase gene (ydiS), and a hypothetical gene (ECs2202) are provided (a). Effect of pH on (CdOH+) (b) and (CdOHCl) (c) in M9 medium containing cadmium (5.4 |M) as predicted by MINEQL+ geochemical modeling software. (Parts (b) and (c) from Worden, C. et al., FEMS Microbiol Lett, 293, 58-64, 2009. With permission.)

physiochemical factors (i.e., divalent cation concentrations and pH) has also been explored as an approach to diminish metal toxicity.99 The effect of pH on metal toxicity has been perhaps the most well studied of these physiochemical factors.

Few studies have investigated the use of metal-resistant bacteria in enhancing microbial processes, such as organic contaminant biodegradation in cocontaminated environments.142 In soil microcosms contaminated with both 2,4-dichlorophenoxyacetic acid (2,4-D) (0.5 mg/g) and cadmium (0.06 mg/g), cadmium-sensitive Alcaligenes eutrophus JMP134 was only able to degrade 2,4-D in the presence of cadmium-resistant isolates, such as Pseudomonas sp., Bacillus sp., and Arthrobacter sp.24 Cadmium was accumulated by metal-resistant microorganisms, thereby reducing cadmium bioavailability and toxicity in the environment. More recently, a strain of Pseudomonas chlororaphis exhibited the ability to degrade naphthalene in the presence of 100 nickel and cobalt.142 This strain contained a cnr-like operon that provided resistance through the efflux of metal from the cell. Many other microbes appear capable of removing heavy metals from cocon-taminated systems prior to bioremediation efforts. For example, Stenotrophomonas sp. CD02 was able to grow in complex media containing 4 mM cadmium and removed up to 80% of the dissolved metal ions after reaching stationary growth.143

Treatment additives, chelating agents, and clay minerals can be added to a system to bind to metals and reduce metal mobility. Treatment additives, such as carbonates, phosphates, and hydroxides, form insoluble precipitates with metals, thus decreasing their bioavailability. Jonioh et al.141

examined the effect of adding calcium carbonate on lead toxicity to microorganisms isolated from a contaminated environment. Additional carbonate (ranging from 1% to 10%) was found to reduce lead toxicity. The additive increased the soil pH and formed an insoluble precipitate with the lead, decreasing the overall lead bioavailability. White and Knowles91 added excess phosphate in order to bind and remove cobalt and zinc, thus preventing metal complexation with the carbon source, nitrilotriacetic acid.

Chelating agents have been employed to reduce metal toxicity toward microorganisms used for biodegradation. EDTA has been involved in reducing the toxicity of nickel to an actinomycete144 and of copper to bacteria and algae;145 however, EDTA also has a strong affinity for essential metals, it is toxic to some microorganisms, and therefore may have limited applications for bioremediation.146 Malakul et al.122 used a less toxic, commercially available chelating resin (Chelex 100) to reduce cadmium toxicity during naphthalene biodegradation. Additional carbon sources could also be considered as metal chelators.147 The addition of succinate (0.5% wt/vol) reduced nickel uptake in Pseudomonas aeruginosa (0.5-fold). Adding other carbon sources could become problematic in biodegradation studies because the microorganism could preferentially utilize the additional carbon source over the organic pollutant.

Clay minerals have been shown to reduce metal bioavailability and toxicity to a variety of organisms (112-115). Babich and Stotzky112 reduced the toxicity of cadmium to a fungus (Aspergillus niger), a bacterium (Bacillus megaterium), and an actinomycete (N. corallina) by adding kaolinite (1-20%) or montmorillonite (1-5%) to an agar medium containing cadmium. Bentonite and vermicu-lite (3%) reduced the toxicity of cadmium to Streptomyces bottropensis.114 Similarly, in solution studies, Kamel114 reported that 3% bentonite and vermiculite reduced the toxicity of 1.33 mM cadmium to Streptomyces bottropensis. Increased clay concentrations resulted in greater protection.

Metal toxicity is also affected by physiochemical factors, such as pH and the concentration of divalent cations. Adding divalent cations, such as zinc, has been reported to mitigate toxicity produced by other metals. For example, the addition of 60 |M zinc reduced toxicity in Pseudomonas putida caused by 3 mM cadmium.148 Zinc had no effect on cells grown in the absence of cadmium. Little is understood surrounding the mechanism of protection; however, cadmium uptake was observed to be dependent on zinc concentration.149 Zinc was found to be a competitive inhibitor of cadmium uptake.

pH is perhaps the most well studied of the physiochemical factors affecting metal toxicity (as indicated by the numerous studies mentioned in the previous section). Although it has been widely reported that lowering pH decreases metal toxicity,123 135 136 140 there are only a few studies that have applied this observation to biodegradation. Sandrin and Maier85 observed the effect of pH on cadmium toxicity (334 |M) during naphthalene biodegradation by a Burkholderia sp. At pH 4 and 5, similar growth on naphthalene was observed in the presence and absence of cadmium; however, at pH 6 and 7, little growth occurred. A similar effect of pH on nickel toxicity was observed for Burkholderia cepacia PR1301.131 Growth was not affected at pH 5 when nickel (3.41 mM) was present, but was completely inhibited at pH 7 in the presence of the same concentration of nickel.

A more detailed understanding of the effects of additives and physiochemical factors on metal toxicity should provide insight into efficient strategies for mitigating metal toxicity in the environment. These approaches are important both for reducing the inhibition of general microbial processes in soil, including litter decomposition, methanogenesis, acidogenesis, and nitrogen transformation, and for enhancing biodegradation at waste sites cocontaminated with metal and organic pollutants.

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