Rapporteur Comments on the Bioremediation Session

Roger C. Prince

We have heard that bioremediation is an important and ethical approach to many environmental problems. Perhaps the best thing is that if successful, it is a permanent solution to the environmental problem. Environmental contaminants are of particular concern when they are bioavailable and are doing something to the environment. Almost by definition, bioremediation is likely to remedy this; successful bioremediation removes the biologically available material. Most of the competing technologies are not as final as this because they usually only move the problem. They may concentrate or reuse it, but the typical response is to pick it up and put it somewhere else. Even the more rigorous physical approaches such as thermal desorption and washing do not focus on the bioavailable material, and reducing the total contamination may not be as effective as bioremediation at removing this material. Bioremediation has the advantage that when the microbes have done what they can do to organic compounds, the organic compounds are usually essentially completely eliminated. That is not always true, but at least it is the major process that goes on in the bioremediation of organic compounds. Bioremediation is also relatively inexpensive, which means that the people who have to do it rather like it, and it does have at least some public support as an environmentally appropriate technology.

Corporate Research Laboratory, Exxon/Mobil Research & Engineering Co., Annandale, NJ



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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP Rapporteur Comments on the Bioremediation Session Roger C. Prince We have heard that bioremediation is an important and ethical approach to many environmental problems. Perhaps the best thing is that if successful, it is a permanent solution to the environmental problem. Environmental contaminants are of particular concern when they are bioavailable and are doing something to the environment. Almost by definition, bioremediation is likely to remedy this; successful bioremediation removes the biologically available material. Most of the competing technologies are not as final as this because they usually only move the problem. They may concentrate or reuse it, but the typical response is to pick it up and put it somewhere else. Even the more rigorous physical approaches such as thermal desorption and washing do not focus on the bioavailable material, and reducing the total contamination may not be as effective as bioremediation at removing this material. Bioremediation has the advantage that when the microbes have done what they can do to organic compounds, the organic compounds are usually essentially completely eliminated. That is not always true, but at least it is the major process that goes on in the bioremediation of organic compounds. Bioremediation is also relatively inexpensive, which means that the people who have to do it rather like it, and it does have at least some public support as an environmentally appropriate technology. Corporate Research Laboratory, Exxon/Mobil Research & Engineering Co., Annandale, NJ

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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP The US Environmental Protection Agency (EPA) has greatly supported bioremediation and has pushed its use in a variety of situations. Exxon probably would not have been allowed to use bioremediation in Alaska (Prince and Bragg 1997) without the EPA pushing strongly for it to be tried (EPA 1989), and I think their efforts have led to general public support for the technology. When we think about marine spills, it is important to recognize that the US coastline is divided into jurisdictions with statutory groups that decide how they would handle spills (http://www.nrt.org). Bioremediation is typically included as a final polishing step for open shorelines, and it is unlikely to be the “frontline” approach except in remote locations. Most shorelines are too publicly essential for something as slow as current bioremediation to work. Bioremediation is much more likely to be useful in places where time is not absolutely of the essence and where other processes such as physical removal of the oil with bulldozers are very difficult or too dangerous for work crews. It is also important that any clean-up strategy have a net environmental benefit (Baker 1995), which bioremediation can readily achieve because it is so noninvasive. As we have heard from all of the speakers, there are many good reasons that bioremediation is valuable, both on land (NRC 1993; Prince 1998) and in the marine environment (Lee and deMora 1999; Lin and others 1999; Prince and others 1997, 1999b; Swannell and others 1999). A major issue for those of us who are, as it were, practitioners is to continue successful applications when necessary. One of the biggest issues we face is maintaining both public and regulatory support, and a major issue is that bioremediation tends to be slow. There is thus a real need to give responders and the general public some confidence that a bioremediation strategy is having the expected results. We need to be able to show that the approach is encouraging a real biological process that will lead to biodegradation and removal of the contaminant. There is a pressing need for interim measures of success, and several of us are working on this issue. We are working on portable instrumentation and tool kits that allow us to monitor the success of fertilizer application, and the initial stimulation of microbial activity (Prince and others 1999a), but there is an obvious opportunity for developing sensitive molecular probes that will assess microbial responses directly. Dr. Lee addressed toxicity endpoints. We are somewhat saddled in the terrestrial environment with clean-up standards that set some sort of concentration level, typically a goal of x parts per million of a particular contaminant. An alternative, and perhaps more meaningful, endpoint would be a goal of some minimal level of toxicity in two or three appro-

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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP priate routine tests (Mueller and others 1999; Potter and others 1999; Saterbak and others 1999). The EPA is also addressing monitoring the disappearance of genotoxicity with successful bioremediation at terrestrial sites (Brooks and others 1998; Hughes and others 1998), and there are obvious potential extensions of this work to marine sediments (Ho and others 1999). The US Geological Survey (USGS) is developing a toxicity identification evaluation protocol for sediments (Lebo and others 1999), with the goal of using it for monitoring remediation. Thus, although there is some work in this area, there is a real need for more research on this issue. One new approach is to use semipermeable membrane devices loaded with oils that mimic fish tissue; these can be exposed at the contaminated site, and subsequently analyzed for contaminants, in a more reproducible way than exposing living animals on-site (Macrae and Hall 1998; Parrott and others 1999; Utvik and Johnsen 1999). Developing modern molecular genetic tools for assaying toxicity may also revolutionize this area and have profound influences on how and when remediation activities should be conducted. There is also a very pressing need to deal with the mixed contaminants found in dredged materials from harbors and estuaries (NRC 1997). Dr. Young described anaerobic processes that might target such contaminants. A biological technology for cleaning contaminated sediments would be very useful, but it must accommodate the fact that the anaerobic conditions that are slowing down the degradation of some contaminants (e.g., hydrocarbons) are also immobilizing others (e.g., metals). The complete degradation of extensively halogenated compounds such as polychlorinated biphenyls (Bedard and others 1998; Wu and others 1999) requires initial anaerobic reductive dehalogenation followed by aerobic degradation. If one made currently anaerobic-contaminated sediments aerobic, one might well speed up the degradation of some organic contaminants, but at the potential expense of mobilizing currently immobilized metals and slowing reductive degradation processes. The issue of handling such mixed contamination requires much more research, and modern molecular tools may have an important role to play once the fundamental microbiological processes are understood. The area of anaerobic degradation of organic pollutants is so new that it is quite likely that basic research in this area will open new avenues for bioprocessing. There are, also, some surprises when considering the spectrum of applications of bioremediation. In Europe there is now concern over the large volumes of vegetable oils that are shipped by sea (Mudge 1995). On several beaches, for example, mats of vegetable oil have polymerized on the beach. One might have thought that vegetable oil would be readily biodegradable and a very easy target for bioremediation. However, un-

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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP der some circumstances, it is proving to be a long-lived contaminant. Thus, there are many areas in bioremediation as a response for marine spills where we are still being surprised. Bioremediation is basically aiming to stimulate natural processes. Someone asked yesterday, “So, you mean if you just waited, it would happen anyway?” and the answer is essentially, “Yes.” With our current knowledge of bioremediation, we are only speeding up the natural process; and if we are lucky, we stimulate it up to five-fold. The other side of this issue is that there are some situations where the natural rate of biodegradation of a contaminant is fast enough that there is no pressing need to stimulate it. There is quite a bit of research in this area, because of course such an approach might be even cheaper than bioremediation. Relying on natural attenuation is being accepted as an appropriate response for some terrestrial spills (Chapelle 1999; Lahvis and others 1999; Lu and others 1999; McNab and Dooher 1998; Stapleton and Sayler 1998), usually with the proviso that the site be monitored to ensure that the contaminant is indeed degrading and not migrating. There are obvious opportunities for using modern molecular probes in studying and quantifying the phenomena associated with natural attenuation, and work for terrestrial applications is well under way (Stapleton and Sayler 1998). As we heard in Dr. Portier's presentation, it is often more important to clean up the source of chronic contamination than to clean the contaminated site. If the point source is removed, natural attenuation may well remedy the contaminated area that was being affected by the source. So, a part of what we heard was the need to continue and steadily improve the successful applications of bioremediation. However, another important avenue for research and development is to move bioremediation to the next level of effectiveness and speed. There is a general optimism in the field that we ought to be able to do radically better in stimulating natural processes without causing any significant harm—We need to find ways of getting things to happen much faster. In the laboratory, one can get many contaminants to disappear with dramatically rapid rate constants, but we are not within two orders of magnitude of these rates in the field. We have to understand better what it is that is limiting the biodegradation of some of our contaminants. The presentations principally dealt with organic compounds, and the great thing about organic compounds is that eventually they are converted to CO2 and water and to all intents and purposes disappear. Inorganic contaminants can only be moved or collected; and although there are several technologies for handling inorganic contaminants in wastewater (Krishnan and others 1993), including several biological ones (Keasling and others 1998; Kefala and others 1999), there are not yet any

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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP proven biotechnologies for dealing with metals and metalloids in sediments, shorelines, and marshes. One potential new approach is phytoremediation—the use of plants to remedy environmental problems (Salt and others 1995). Although there is interest in using plants to stimulate oil biodegradation (Carman and others 1998), most work appears to be focused on using plants to accumulate metals and metalloids (Raskin and others 1994). Thus, in summary, we heard that bioremediation in the marine environment is an important option for dealing with spills and a potential option for dealing with contaminated sediments. Progress in developing these technologies will come from a number of fronts, and modern molecular approaches must be integrated into this ongoing work. Terrestrial applications of bioremediation have received more attention than marine ones because of the far greater need, and gene-probe and molecular taxonomy approaches are beginning to move from the laboratory to the field. Some of these will be directly transferable to the marine environment, but there will undoubtedly be a need to develop saline-specific techniques. The next few years promise to be an exciting time for such developments. REFERENCES Baker JM. 1995 Net environmental benefit analysis for oil spill response. In: Proceedings of the 1995 International Oil Spill Conference. Washington, DC: American Petroleum Institute. p 611-614. Bedard DL, VanDort H, Deweerd KA. 1998 Brominated biphenyls prime extensive microbial reductive dehalogenation of aroclor 1260 in Housatonic River sediment. Appl Environ Microbiol 64:1786-1795. Brooks LR, Hughes TJ, Claxton LD, Austern B, Brenner R, Kremer F. 1998 Bioassay-directed fractionation and chemical identification of mutagens in bioremediated soils. Environ Health Perspect 106(Suppl 6):1435-1440. Carman EP, Crossman TL, Gatliff E.G. 1998 Phytoremediation of no. 2 fuel oil-contaminated soil. J Soil Contam 7:455-466. Chapelle FH. 1999 Bioremediation of petroleum hydrocarbon-contaminated ground water: The perspectives of history and hydrology. Ground Water 37:122-132. EPA [Environmental Protection Agency]. 1989 Alaskan oil spill bioremediation project. EPA/600/8-89/073. Ho K, Patton L, Latimer JS, Pruell RJ, Pelletier M, McKinney R, Jayaraman S. 1999 The chemistry and toxicity of sediment affected by oil from the North Cape spilled into Rhode Island Sound. Marine Poll Bull 38:314-323.(See also “The US National Response Team,” <http://www.nrt.org>.) Hughes TJ, Claxton LD, Brooks L, Warren S, Brenner R, Kremer F. 1998 Genotoxicity of bioremediated soils from the Reilly tar site, St. Louis Park, Minnesota. Environ Health Perspect 106(Suppl 6):1427-1433.

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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP Keasling JD, VanDien SJ, Pramanik J. 1998 Engineering polyphosphate metabolism in Escherichia coli: Implications for bioremediation of inorganic contaminants. Biotechnol Bioengineer 58:231-239. Kefala MI, Zouboulis AI, Matis KA. 1999 Biosorption of cadmium ions by actinomycetes and separation by flotation Environ Poll 104:283-293. Krishnan ER, Utrecht PW, Patkar AN, Davis JS, Pour SG, Foerst ME. 1993 Recovery of metals from sludges and wastewaters. Park Ridge, NJ. Noyes Data Corporation. Lahvis MA, Baehr AL, Baker RJ. 1999 Quantification of aerobic biodegradation and volatilization rates of gasoline hydrocarbons near the water table under natural attenuation conditions. Water Resources Res 35:753-765. Lebo JA, Huckins JN, Petty JD, Ho KT. 1999 Removal of organic contaminant toxicity from sediments—Early work toward development of a toxicity identification evaluation (TIE) method. Chemosphere 39:389-406. Lee K, deMora S. 1999 In situ bioremediation strategies for oiled shoreline environments Environ Technol 20:783-794. Lin, Q, Mendelssohn IA, Henry CB, Robert, PO, Walsh MM, Overton EB, Portier, RJ. 1999 Effects of bioremediation agents on oil degradation in mineral and sandy salt marsh sediments. Environ Technol 20:825-837. Lu GP, Clement TP, Zheng CM, Wiedemeier TH. 1999 Natural attenuation of BTEX compounds: Model development and field-scale application. Ground Water 37:707-717. Macrae JD, Hall KJ. 1998 Comparison of methods used to determine the availability of polycyclic aromatic hydrocarbons in marine sediment. Environ Sci Technol 32:3809-3815. McNab WW, Dooher BP. 1998 Uncertainty analyses of fuel hydrocarbon biodegradation signatures in ground water by probabilistic modeling. Ground Water 36:691-698. Mudge SM. 1995 Deleterious effects from accidental spillages of vegetable oils. Spill Sci Technol Bull 2:187-191. Mueller DC, Bonner JS, McDonald SJ, Autenrieth RL. 1999 Acute toxicity of estuarine wetland sediments contaminated by petroleum Environ Technol 20:875-882. NRC [National Research Council]. 1997 Contaminated Sediments in Ports and Waterways: Cleanup Strategies and Technologies. Washington, DC. National Academy Press. NRC [National Research Council]. 1993 In Situ Bioremediation: When Does It Work? Washington, DC: National Academy Press. Parrott JL, Backus SM, Borgmann AI, Swyripa M. 1999 The use of semipermeable membrane devices to concentrate chemicals in oil refinery effluent on the Mackenzie River. Arctic 52:125-138. Potter CL, Glaser JA, Chang LW, Meier JR, Dosani MA, Herrmann RF. 1999 Degradation of polynuclear aromatic hydrocarbons under bench-scale compost conditions. Environ Sci Technol 33:1717-1725.

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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP Prince RC. 1998 Bioremediation. In: Kirk-Othmer Encyclopedia of Chemical Technology, 4th ed, suppl. New York: John Wiley. p 48-89. Prince RC, Atlas RM, Zelibor JL Jr. 1997 Environmental applications of marine biotechnology. In: Altman A, ed. Agricultural Biotechnology. New York: Marcel Dekker. p 615-628. Prince RC, Bare RE, Garrett RM, Grossman MJ, Haith CE, Keim LG, Lee K, Holtom G, Lambert P, Sergy GA, Owens EH, Guénette CC. 1999a Bioremediation of a marine oil spill in the Arctic. In: In Situ Bioremediation of Petroleum Hydrocarbon and Other Organic Compounds. Alleman BC Leeson A, eds. Columbus, OH: Battelle Press. p 227-232. Prince RC, Bragg JR. 1997 Shoreline bioremediation following the Exxon Valdez oil spill in Alaska. Bioremed J 1:97-104. Prince RC, Varadaraj R, Fiocco RJ, Lessard RR. 1999b Bioremediation as an oil spill response tool. Environ Technol 20:891-896. Raskin I, Nanda Kumar PBA, Dushenkov S, Salt DE. 1994 Bioconcentration of heavy metals by plants. Curr Opinion Biotechnol 5:285-290. Salt DE, Blaylock M, Nanda Kumar PBA, Dushenkov V, Ensley BD, Chet I, Raskin I. 1995 Phytoremediation: A novel strategy for the removal of toxic metals from the environment using plants. Biotechnology 13:468-474. Saterbak A, Toy RJ, Wong DCL, McMain BJ, Williams MP, Dorn PB, Brzuzy LP, Chai EY, Salanitro JP. 1999 Ecotoxicological and analytical assessment of hydrocarbon-contaminated soils and application to ecological risk assessment. Environ Toxicol Chem 18:1591-1607. Stapleton RD, Sayler GS. 1998 Assessment of the microbiological potential for the natural attenuation of petroleum hydrocarbons in a shallow aquifer system. Microbial Ecol 36:349-361. Swannell RPJ, Mitchell D, Lethbridge G, Jones D, Heath D, Hagley M, Jones M, Petch S, Milne R, Croxford R, Lee K. 1999 A field demonstration of the efficacy of bioremediation to treat oiled shorelines following the Sea Empress incident. Environ Technol 20:863-873. Utvik TIR, Johnsen S. 1999 Bioavailability of polycyclic aromatic hydrocarbons in the North Sea. Environ Sci Technol 33:1963-1969. Wu QZ, Bedard DL, Wiegel J. 1999 2,6-Dibromobiphenyl primes extensive dechlorination of aroclor 1260 in contaminated sediment at 8-30 degrees C by stimulating growth of PCB-dehalogenating microorganisms. Environ Sci Technol 33:595-602.

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