Impact of metals on the biodegradation of organic pollutants

Environmental Health Perspectives, June 15, 2003 by Todd R. Sandrin, Raina M. Maier

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 day minerals. The addition of divalent cations and adjustment of pH are additional strategies currently under investigation. Key words: bioavailability, biodegradation, bioremediation, hazardous waste, heavy metals, inhibition, metal toxicity, pollutants. Environ Health Perspect 111:1093-1101 (2003). doi:10.1289/ehp.5840 available via http://dx.doi.org/[Online 4 March 2003]

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Remediation of sites co-contaminated with organic and metal pollutants is a complex problem, as the two components often must be treated differently, yet 40% of the hazardous waste sites currently on the National Priority List of the U.S. Environmental Protection Agency (U.S. EPA) are co-contaminated (Sandrin et al. 2000). Metals most frequently found at U.S. EPA Superfund sites include arsenic, barium, cadmium, chromium, lead, mercury, nickel, and zinc. Common organic co-contaminants include petroleum, chlorinated solvents, pesticides, and herbicides. Biodegradation to innocuous end products (C[O.sub.2], cell mass, water) is considered to be an environmentally sound and cost-effective process for removing organic contaminants (National Research Council 1994). In contrast, the nonbiodegradable metal component must either be removed or stabilized within the site. Removal involves a combination of steps that may include mobilization, separation and collection, off-site transport, and disposal. Stabilization of metals requires that the site be permanently changed in some way. Most drastic is vitrification, wherein contaminated soil is heated to form a glasslike substance (Staley 1995). Alternatively, the site may be capped or paved to prevent water from entering the site and transporting metal contaminants, or site conditions may be imposed (e.g., anaerobiosis) that reduce the potential for metal mobilization and transport (Liu et al. 2001; Zoumis et al. 2001). In either case, metal removal or metal stabilization, treatment of the organic component by biodegradation is likely to be the first step in remediation of co-contaminated sites (Roane et al. 1996).

It is well documented that the presence of metals can inhibit a broad range of microbial processes including methane metabolism, growth, nitrogen and sulfur conversions, dehalogenation, and reductive processes in general. An exhaustive review of the impacts of metals on many of these processes is available (Baath 1989). However, the effects of metal toxicity on organic pollutant biodegradation in contaminated water and soil environments have not been adequately defined quantitatively or qualitatively. This is because metals may be present in a variety of different physical and chemical forms, namely, as separate-phase solids, soil-adsorbed species, colloidal solutions, soluble complexed species, or ionic solutes. Related complications stem from the fact that the physical and chemical state of metals is affected by environmental conditions such as pH and ionic strength of the water phase as well as soil properties that include ion exchange capacity, clay type and content, and organic matter content.

In this review we discuss metal inhibition and toxicity in the context of the biodegradation of co-contaminant organic chemicals for which treatment is deemed necessary. Specifically, we address: a) the importance of the physical-chemical state of metals in relation to metal bioavailability and inhibition of microbial activity, b) the impact of metals on aerobic and anaerobic biodegradation processes, c) relationships between metal concentration and metal impacts on biodegradation, and d) how metal toxicity can be mitigated to allow effective biodegradation of targeted organic pollutants.

Metal Toxicity and Bioavailability

Metals exert their toxic effects on microorganisms through one or more mechanisms. An excellent review is available that describes modes of metal toxicity and the mechanisms by which microorganisms resist such toxicity (Nies 1999). Toxic metal cations may substitute for physiologically essential cations within an enzyme (e.g., [Cd.sup.2 ] may substitute for [Zn.sup.2 ]), rendering the enzyme nonfunctional. Similarly, metal oxyanions, such as arsenate, may be used in place of structurally similar, essential nonmetal oxyanions, such as phosphate. In addition, metals impose oxidative stress on microorganisms (Kachur et al. 1998).