Environmental Aspects of Marine Biotechnology: Overview of the 1999 Workshop

INTRODUCTION

The U.S. coastal population is growing rapidly, so a healthy marine environment is ever more vital for the well-being of Americans. The 1999 workshop identified several areas where there are serious needs and exciting opportunities for biotechnology to improve our understanding of the marine environment to better ensure its protection (National Research Council, 2000). These areas include the bioremediation of oil and other spills, the health of coral reefs and other marine environments, and potential threats to human health caused by toxic blooms and microbial contamination. The intervening years have increased concern for the health of the marine environment, but they have also provided optimism that progress is possible. In particular, recent advances in microbiological and in toxicological testing discussed at the 2001 workshop could transform research in those areas and bring real improvements in our ability to understand and maintain the environment and protect human health.

BIOREMEDIATION

Large amounts of oil are extracted from the sea floor and even larger volumes are shipped. Unfortunately, remediation is sometimes required for accumulated daily small spills, and occasional major spills. Given the staggering scale of oil usage, which is estimated at 3.5 billion gallons (1.2 ×



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Marine Biotechnology in the Twenty-First Century: Problems, Promise, and Products Environmental Aspects of Marine Biotechnology: Overview of the 1999 Workshop INTRODUCTION The U.S. coastal population is growing rapidly, so a healthy marine environment is ever more vital for the well-being of Americans. The 1999 workshop identified several areas where there are serious needs and exciting opportunities for biotechnology to improve our understanding of the marine environment to better ensure its protection (National Research Council, 2000). These areas include the bioremediation of oil and other spills, the health of coral reefs and other marine environments, and potential threats to human health caused by toxic blooms and microbial contamination. The intervening years have increased concern for the health of the marine environment, but they have also provided optimism that progress is possible. In particular, recent advances in microbiological and in toxicological testing discussed at the 2001 workshop could transform research in those areas and bring real improvements in our ability to understand and maintain the environment and protect human health. BIOREMEDIATION Large amounts of oil are extracted from the sea floor and even larger volumes are shipped. Unfortunately, remediation is sometimes required for accumulated daily small spills, and occasional major spills. Given the staggering scale of oil usage, which is estimated at 3.5 billion gallons (1.2 ×

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Marine Biotechnology in the Twenty-First Century: Problems, Promise, and Products 1010 l) per day (Anonymous, 2001), even the spillage of a tiny fraction (estimated at <0.0035% in 1997 (Etkin, 1999)) means that more than 120 million gallons are spilled into the world’s oceans each year. Fortunately, despite the increasing volume of transported oil, the amount spilled from catastrophic accidents has been generally decreasing (Etkin, 1999). Nevertheless, there is intense public pressure for the infrequent major spills to be cleaned up in an environmentally appropriate manner as quickly as possible. Bioremediation offers a clean-up technology that works to speed natural degradation processes (Lee and deMora, 1999), and it has already achieved notable success following the spill from the Exxon Valdez in Alaska (Prince and Bragg, 1997). Extension of this approach to marshes, harbors, and dredged sediment will further facilitate the remediation process. Modern genomic and culturing tools, described at the second workshop, will revolutionize our understanding of, and hence our ability to manipulate and restore, marsh environments and dredged material. Both are fragile substrates where careless human intervention can cause more harm than good. Physical treatments of marshes can cause more damage than the initial spill (Canadian Coast Guard, 1995) and anaerobic dredge spoil may release heavy metals if allowed to become aerobic without appropriate containment (National Research Council, 1997). Bioremediation can potentially offer cost-effective and environmentally appropriate treatments for these troublesome situations. Sustained effort will be required in both basic science, to understand the microbial metabolic potential that we may be able to exploit, and in field applications. For example, recent mesocosm experiments (Dowty et al., 2001) and field studies at the San Jacinto test site in Texas (Simon et al., 1999) showed promising leads in developing bioremediation. Integrating the new genomics and proteomics tools and environmental remediation experiments, perhaps by encouraging collaborative research, is an obvious way of stimulating rapid progress in this important area of biotechnology. Reliable bioremediation strategies for marshes and dredged materials would be an important contribution toward maintaining ecosystem health in the face of continued exploitation of our coastline. ENVIRONMENTAL HEALTH The ever-growing coastal population is placing an increasing burden on the natural processes of the coastal environment. Fisheries are declining (Jackson et al., 2001), and there is increasing concern about sewage con-

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Marine Biotechnology in the Twenty-First Century: Problems, Promise, and Products tamination of recreational beaches (Griffin et al., 2001), fertilizer runoff (Frink et al., 1999), toxic dinoflagellates (Burkholder and Glasgow, 2001), and diseases of coral reefs (Richardson, 1998) and other organisms (Harvell et al., 1999). These are not minor concerns. Outbreaks of harmful algal blooms, such as the toxic Pfiesteria in North Carolina and then the Chesapeake Bay in the late 1990s, caused near hysteria in the press (Magnien, 2001). In spite of substantial efforts, controversy still exists over what causes these outbreaks, although excess inorganic nutrients in the water seem to play a role (National Science and Technology Council, 2000). Such outbreaks have substantial costs both to individuals, such as fishermen, and to communities (Anderson et al., 2000). Preventing these acute events in a cost-effective manner would have many benefits. If they cannot be totally prevented, it would be appropriate to develop control strategies to minimize their longevity. One possibility is that harmful algal blooms are controlled by trace elements in the water (Anderson and Garrison, 1997). Manipulating these elements might be a cost-effective tool, but this possibility needs additional investigation before it can be seriously addressed. Alternatively, it might be possible to biocontrol some organisms by adding specific pathogens when a bloom has become established. For example, a virus has been isolated that is apparently capable of controlling the brown-tide microalga Aureococcus (Milligan and Cosper, 1994). Healthy marine environments, especially coral reefs, have substantial economic benefits for local communities (e.g., Hundloe, 1990). Tourism, possibly one of the world’s largest industries, often relies on a healthy coral ecosystem to attract customers. Yet healthy marine environments seem to be declining around all our coasts. At times, this is clearly due to damage from development, perhaps because of increased nutrients or increased silt in the water. In other cases, the decline is attributed to disease, although very few of the diseases of marine organisms have been correlated with a specific pathogen (Richardson et al., 1997; Richardson, 1998; Harvell et al., 1999). Thus, at present it is difficult to be sure how widespread these diseases are, whether putative causative organisms are indeed responsible for disease, or whether the organisms exploit certain environmental conditions at different times or in different places. Marine biotechnology, and particularly the development of new techniques in genomics and proteomics, offers the potential for exquisitely sensitive diagnostic tests to clearly identify the initial outbreaks of toxic organisms, discover their distribution in estuaries and oceans, and perhaps help to identify biocontrol agents. Similarly, these techniques could reliably

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Marine Biotechnology in the Twenty-First Century: Problems, Promise, and Products detect the causative agents of many of the diseases that are afflicting coral reefs and other environments (Figure 1). In turn, it might be possible to diagnose some of the conditions that predispose ecological systems to outbreaks of toxic organisms and diseases and thereby protect vital estuarine and marine resources. There is also a need for active restoration of compromised ecosystems, such as degraded coral reefs. It may be necessary to raise the replacement organisms by aquaculture to provide the necessary material for restoration. Unfortunately, the few attempts at restoration that have been undertaken to date, such as the work with stony corals, have not been very successful. Reproduction and larval metamorphosis in many shellfish are controlled by specific environmental chemicals, such as prostaglandins. Sometimes inexpensive mimics can be used to trigger desired events (e.g., hydrogen peroxide as a replacement for specific prostaglandins). Perhaps these findings can be extended to other invertebrates, but development of techniques for large-scale production of diverse organisms for restoration will take a sustained and targeted research program. HUMAN HEALTH One of the primary concerns in public health is the risk that humans using the marine environment will encounter microbial pathogens, especially from human excreta (Griffin et al., 2001). Unfortunately, the diversity of potentially harmful microorganisms is so great that routine monitoring for pollution relies on the search for “indicator organisms.” Historically, these indicators have been used because they are conservative, they occur with high concentrations of pathogens, and they cannot replicate in the environment (Griffin et al., 2001). All current tests involve culturing, including those for total and fecal coliforms, Escherichia coli, enterococci, and Clostridium perfringens. These have served humans well, but they are by no means perfect; tests take time to culture and analyze and do not assess indigenous nonsewage organisms, such as Vibrio vulnificus, which can cause severe disease and even death in immuno-compromised persons. Modern molecular tools offer the promise of essentially instant tests, perhaps akin to the antibody tests for common ailments now available in physician’s offices. Alternatively, PCR-amplification tests could be developed for particularly troublesome organisms. Real-time tests would revolutionize health-risk monitoring of recreational beaches (Grimes, 1999; Rose and Grimes, 2001).

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Marine Biotechnology in the Twenty-First Century: Problems, Promise, and Products FIGURE 1 Coral diseases (top) black band and (bottom) plague type II contributing to the decline of coral reefs in U.S. waters. Courtesy of L. Richardson.

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Marine Biotechnology in the Twenty-First Century: Problems, Promise, and Products A different hazard to human health is exemplified by toxic dinoflagellates that seem to cause cognitive disturbances from exposure to aerosols of water that contained the organism (Grattan et al., 2001). Although understanding the chemical nature and pharmacology of this toxin may provide a useful experimental tool for neuroscientists, a more pressing need is to protect human health by developing assays for the toxin. All of these areas are characterized by a real potential for rapid increases in understanding if modern molecular tools of biotechnology can be effectively integrated into more classical environmental disciplines. This integration will require interdisciplinary science and substantial funding, but the rewards should amply repay the investment. Recommendations to Enhance Environmental Applications of Marine Biotechnology Explore the possibility that molecular tools will aid in understanding the environmental impact of oil and other contaminant spills in the marine environment. Molecular tools may also be used to track the progress of remediation efforts and may provide guidance for deciding when a remediation effort has ceased to provide clear environmental benefits. Bring genomic and other modern molecular techniques to bear on the nature and progress of diseases of marine organisms. Investments must be made to understand and develop methods for culturing marine pathogens. Similar tools will be essential for understanding coral-reef diversity as restoration proceeds. Develop genomic and other modern molecular techniques to monitor potentially toxic species, such as dinoflagellates, and human pathogens in the marine environment, so that potential outbreaks of disease can be predicted and eventually prevented. In all these areas, it is essential that field and laboratory investigations go hand in hand and that the best of classical and modern molecular techniques be combined. That will happen only if interdisciplinary science is fostered and encouraged. REFERENCES Anderson, D. M., and D. J. Garrison, Eds. 1997. The ecology and oceanography of harmful algal blooms. Limnology and Oceanography 42:1009-1305.

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Marine Biotechnology in the Twenty-First Century: Problems, Promise, and Products Anderson, D. M., P. Hoagland, Y. Kaoru, and A. White. 2000. Estimated Annual Economic Impacts from Harmful Algal Blooms (HABs) in the United States. Sea Grant, Woods Hole Oceanographic Institute: Technical Report. Woods Hole, Mass. Anonymous. 2001. Industry at a glance. World Oil 222:15. Burkholder, J. M., and H. B. Glasgow. 2001. History of toxic Pfiesteria in North Carolina Estuaries from 1991 to the present. BioScience 51:827-841. Canadian Coast Guard. 1995. Oil Spill Response Field Guide. Dowty, R. A., G. P. Shaffer, M. W. Hester, G. W. Childers, F. M. Campo, and M. C. Greene. 2001. Phytoremediation of small-scale oil spills in fresh marsh environments: a mesocosm simulation. Marine Environmental Research 52:195-211. Etkin, D. S. 1999. Historical overview of oil spills from all sources. In Proceedings of the 1999 International Oil Spill Conference. American Petroleum Institute, Washington, D.C. Frink, C. R., P. E. Waggoner, and J. H. Ausubel. 1999. Nitrogen fertilizer: retrospect and prospect. Proceedings of the National Academy of Sciences USA 96:1175–1180. Grattan, L. M., D. Oldach, and J. G. Morris. 2001. Human health risks of exposure to Pfiesteria piscicida. BioScience 51:853-857. Griffin, D. W., E. K. Lipp, M. R. McLaughlin, and J. B. Rose. 2001. Marine recreation and public health microbiology: quest for the ideal indicator. BioScience 51:817-825. Grimes, D. J. 1999. Water we count on. New Scientist 161:46. Harvell, C. D., K. Kim, J. M. Burkholder, R. R. Colwell, P. R. Epstein, D. J. Grimes, E. E. Hofmann, E. K. Lipp, A. D. M. E. Osterhaus, R. M. Overstreet, J. W. Porter, G. W. Smith, and G. R. Vasta. 1999. Emerging marine diseases—climate links and anthropogenic factors. Science 285:1505-1510. Hundloe, T. 1990. Measuring the value of the Great Barrier Reef. Parks Recreation 26:11-15. Jackson, B. C., M. X. Kirby, W. H. Berger, K. A. Bjorndal, L. W. Botsford, B. J. Bourque, R. H. Bradbury, R. Cooke, J. Erlandson, J. A. Estes, T. P. Hughes, S. Kidwell, C. B. Lange, H. S. Lenihan, J. M. Pandolfi, C. H. Peterson, R. S. Steneck, M. J. Tegner, and R. R. Warner. 2001. Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629-638. Lee, K., and S. deMora. 1999. In situ bioremediation strategies for oiled shoreline environments. Environmental Technology 20:783-794. Magnien, R. E. 2001. The dynamics of science, perception, and policy during the outbreak of Pfiesteria in the Chesapeake Bay . BioScience 51:843-852. Milligan, K. L. D., and E. M. Cosper. 1994. Isolation of virus capable of lysing the brown tide microalga, Aureococcus anophagefferens. Science 266:805-807. National Research Council. 1997. Contaminated Sediments in Ports and Waterways. Cleanup strategies and technologies. National Academy Press. Washington, D.C. National Research Council. 2000. Opportunities for Environmental Applications of Marine Biotechnology. National Academy Press. Washington, D.C. National Science and Technology Council, Committee on Environment and Natural Resources. 2000. Harmful Algal Blooms in US Waters. National Science and Technology Council, Committee on Environment and Natural Resources, National Assessment, Washington, D.C.

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Marine Biotechnology in the Twenty-First Century: Problems, Promise, and Products Prince, R. C., and J. R. Bragg. 1997. Shoreline bioremediation following the Exxon Valdez oil spill in Alaska. Journal of Bioremediation 1:97-104. Richardson, L. L., K. Kuta, S. Schnell, and R. G. Carlton. 1997. Ecology of the black band disease microbial consortium. Proceedings of the 8th International Coral Reef Symposium. 1:597-600 Richardson, L. L. 1998. Coral diseases: what is really known? Trends in Ecology and Evolution 13:438-443. Richardson, L. L., W. M. Goldberg, K. G. Kuta, R. B. Aronson, G. W. Smith, K. B. Ritchie, J. C. Halas, J. S. Feingold and S. M. Miller. 1998. Florida’s mystery coral-killer identified. Nature 392:557-558. Rose, J. B., and D. J. Grimes. 2001. Reevaluation of microbial water quality: powerful new tools for detection and risk assessment. A report from the American Academy of Microbiology. Washington, D.C. Simon, M. A., J. S. Bonner, T. J. McDonald, and R. L. Autenrieth. 1999. Bioaugmentation for the enhanced bioremediation of petroleum in a wetland. Polycyclic Aromatic Compounds 14:231-239.