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For example, halogenated chemicals are rare in nature, and the natural substrates for enzymes involved in reductive dehalogenation are completely unknown Mohn and Tiedje, The corollary of this situation is that bond types or structures not known in nature are often not metabolized. Since these new substrates are a potential energy resource, they exert selective pressure for organism variants to use them.

To acquire basically new enzymatic traits through natural evolution is thought to take a very long time, probably hundreds or thousands of years. If one wants to biodegrade these nonnatural chemicals in our lifetime to cleanup hazardous waste, the task will likely involve protein and gene engineering, a process not financially feasible in the foreseeable future.

Ecological systems are driven by the resources available and the competition for them among the community members. For pollutant degradation, the major question is whether the pollutant is an energy resource—will an organism grow on the chemical as a substrate? If so, there is strong selective pressure for the degrading population to outgrow others, thereby amplifying the rate of degradation.

It is useful to group chemicals into two classes of biodegradability: 1 those that support the growth of microbial populations and 2 those that are cometabolized in other words, they do not support growth but are partly metabolized, usually through only a step or two of the complete metabolic pathway. Organisms that carry out cometabolism are not naturally selected and, therefore, are much more difficult to manage in nature.

For this reason the distinction of these two classes is important. When pollutants are growth substrates, major advantages accrue: 1 the catalyst grows logarithmically with no external input of resources; 2 the proper growth, activity, and distribution of the microbial population which is very difficult to manage under other circumstances is an inherent outcome of natural selection for the primary energy substrate; and 3 growth substrates are almost always completely oxidized to carbon dioxide, leaving no toxic intermediates.

Less than complete pollutant destruction by natural selection is usually due to limitation by some other resource, most commonly the electron acceptor. Because of these advantages, chemicals that are growth substrates have not and should not become widespread pollution problems. This is because the limitations on natural selection disappear as the chemical becomes more widely distributed. Examples of chemicals that are growth substrates are benzene, toluene, xylenes, naphthalene, chlorophenols, acetone, nitrilotriacetic acid, and 2,4-D.

Whenever a pollutant is a growth substrate, bioremediation should be seriously considered. Even if the waste contains mixtures of chemicals, some of which are growth substrates and others not, bioremediation may still be advantageous because it can reduce other remediation costs, such as the amount of activated carbon needed. Cometabolism usually results from relaxed specificity of an enzyme. No sequential metabolic pathway or energy coupling to adenosine triphosphate production typically occurs.

Therefore, natural selection cannot be achieved through this secondary pollutant substrate. Sometimes the primary and secondary substrates are competitive inhibitors, which may require more sophisticated management, such as pulse feeding or precise concentration control. Cometabolic processes typically accumulate intermediates, some of which may be toxic. Cometabolic reactions seem to be the only ones that show activity on many of the recalcitrant chlorinated solvents, such as perchloroethylene PCE , trichloroethylene TCE , carbon tetrachloride, and chloroform.

Laboratory testing and field testing are beginning to show that it may be possible to successfully manage a cometabolic process in situ.

Nonetheless, the experimentation, field testing, and monitoring will all need to be more extensive than for pollutants that are growth substrates. I suggest that the following key questions, in the indicated order of priority, are a basic guide to successful bioremediation:. The first question is whether the chemical is biodegradable, because bioremediation cannot be accomplished if no organism exists that can degrade the chemical. Biodegradability must be established if it is not already well-documented in the literature. Subquestions are whether the chemical is a growth substrate, for the reasons discussed above, and whether the biodegrading organism exists at the site.

A focus on the biodegradability of the pollutant is also important because it suggests the time until application and the research needed for application, as shown in Figure 1. In the figure, biodegradability is indicated by the frequency of the biodegrading populations within the total soil community. The higher frequency implies several benefits to bioremediation, including greater diversity among the populations of degraders, less chance of encountering patches devoid of organisms, and a rather global distribution of this biodegradative property at most sites, which allows extrapolation of information among sites.

If organisms are widespread, they cannot be limiting to biodegradation. Hence, environmental factors are then the focus for ensuring or enhancing bioremediation. The time until field application of a bioremediation technology can also be predicted by the biodegradability scale of Figure 1. When natural degrading organisms are widespread, application is more immediate because conditions may be met naturally or, if not, technology exists for removing some of the environmental limitations.

However, when organisms do not exist or are rare, the time until application is more distant because successful addition or distribution of organisms is difficult to achieve, especially in the subsurface Harvey et al. It is even more difficult to genetically engineer a new catalytic property; this approach is far from any practical application to bioremediation.

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The second question—is the environment habitable? First, does the environment contain toxic chemicals that make it difficult or impossible for microbes to live? Many polluted sites contain mixtures of chemicals and metals, some at high concentrations, that may pickle the environment so that bioremediation is not feasible. The second issue is the availability of sufficient life-sustaining growth factors, such as nutrients, particularly nitrogen and phosphorus; appropriate electron acceptors; and perhaps other growth factors that might be contained in soil organic matter.

Nutrient supply can be evaluated by considering whether the proper carbon-nitrogen-phosphorus C:N:P ratio is likely to be met by the soil environment.

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Microbial growth in most subsoils is not limited by nitrogen and phosphorus as long as the new carbon being provided is not in amounts greater than tens of parts per million. This is often the case with pollutant chemicals. Since nitrogen and phosphorus are inexpensive, however, they are often added as insurance. Too often in bioremediation there is a solution in need of a problem. Thus, effort or money is spent to modify something that is not ratelimiting.

To avoid this waste, the rate-limiting parameter must first be defined.

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In doing so, it is worthwhile to consider the ecosystem in its entirety and to recognize the three key components: sub-. Factors that reflect this interrelationship and that can limit biodegradation are shown in parentheses in Figure 2. If biodegradability and habitability have been established, the most common limiting parameter is oxygen, since it has relatively low solubility in water and is in high demand as an oxidant for all biological respiration.

Thus, schemes for injection of oxygen or hydrogen peroxide into soil or aquifers are common. Such treatments overcome a rate limitation if the site is anaerobic. Alternative electron acceptors are possible, and nitrate is particularly attractive because of its high electron-accepting capacity in water, its leachability in soils, its low toxicity, and its low cost.

Research on denitrification-driven bioremediation is in its infancy, however. The frequency of this type of biodegrading population in soil is not known, but it almost certainly is lower than for oxygen-respiring organisms. Other treatments to meet physiological requirements include addition of nutrients, adjustment of pH, and removal of toxicants by leaching, precipitation, or some form of inactivation.

As stated above, nutrient addition is common, probably because it is easy and cheap and may occasionally provide some benefit, not because it has been a well-documented requirement for many sites. A second important limitation on biodegradation is the availability of the chemical to the organisms, or bioavailability.

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Bioavailability is limited when the pollutant is dissolved in organic matter or trapped in micropores in the soil matrix. Substantial work is under way to attempt to understand and enhance the bioavailability of water-in-soluble chemicals. The ecological approach to this problem, however, would be to focus on ensuring that the local environment con-. A related issue, but on a slightly larger scale, is the movement of the chemical or organism so that the two come into contact.

Mobility is not a limitation for water-soluble chemicals, which move through soil easily, but it is a severe problem for very insoluble chemicals. In this case, movement of organisms is all that is feasible if physical mixing is not possible. Returning to the ecological approach, the key point in determining whether bioremediation is successful is to establish whether the conditions of natural selection can be expected to be met within the site vicinity.

The point is not to determine pollutant mass balances; it is not to ensure that all heterogeneity can be understood and accounted for; and it is not even to worry about local concentrations above regulatory targets if conditions of the surrounding environment ensure that natural selection will occur. This approach recognizes that energy from organic matter is the key limitation for microbial growth and that if the appropriate enzymes and required environmental conditions exist, there is no way to prevent complete biodegradation. Thus, the first criterion for successful bioremediation is documentation of the conditions for natural selection, namely: 1 is the chemical a growth substrate for microbes?

The ecological approach suggests that more emphasis should be placed on documenting adequate electron acceptor supply and less on measuring the actual pollutant. A second line of evidence for a successful bioremediation is whether the biological record suggests that natural selection has occurred. This evidence was well illustrated by Madsen et al.

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Types of evidence in the biological record include 1 increased rate of pollutant mineralization; 2 increased populations of microorganisms e. At contaminated sites, this kind of evidence in the biological record would be strongly indicative of successful intrinsic bioremediation and its persistence as long as the conditions for natural selection can be ensured. The author's research on biodegradation has been funded by the U. Begon, M. Harper, and C. Ecology: Individuals, Populations and Communities. Cambridge, Mass. Harvey, R.