François M. M. Morel
Biological processes in seawater are dependent on the supply of a number of chemical elements that serve as nutrients and affected by others that may act as toxicants. Besides the major algal nutrients (nitrogen, phosphorus, and silicon), marine organisms require trace elements—chiefly trace metals such as manganese, iron, cobalt, nickel, copper, and zinc—for growth. We now know, for example, that the iron supply limits phytoplankton productivity of some regions of the oceans. Conversely, the seawater concentration of a metal such as copper is nearly toxic to a number of marine microorganisms and may control, for example, the distribution of important photosynthetic species such as Prochlorococcus in the water column. Thus it is clear that in principle, we may be able to manipulate the concentration of trace metals in seawater to affect a desired change such as enhancing some natural degradation process, shifting the dominant flora and fauna, or increasing the productivity—all of which may be considered aspects of bioremediation lato sensu.
Because the concentration of trace metals like iron and copper are very low in seawater—picomoles to nanomoles per liter at the surface —they are particularly apt to be increased inadvertently or purposefully by humans. Certainly we have increased the concentrations of metals in many bays and estuaries in the same way that we have increased nitrogen or phosphorus concentrations. But we have also increased substantially
Princeton Environmental Institute, Department of Geosciences, Princeton University, Princeton, NJ
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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP Use of Trace Metals in: Marine Bioremediation: A Need for Fundamental Knowledge François M. M. Morel Biological processes in seawater are dependent on the supply of a number of chemical elements that serve as nutrients and affected by others that may act as toxicants. Besides the major algal nutrients (nitrogen, phosphorus, and silicon), marine organisms require trace elements—chiefly trace metals such as manganese, iron, cobalt, nickel, copper, and zinc—for growth. We now know, for example, that the iron supply limits phytoplankton productivity of some regions of the oceans. Conversely, the seawater concentration of a metal such as copper is nearly toxic to a number of marine microorganisms and may control, for example, the distribution of important photosynthetic species such as Prochlorococcus in the water column. Thus it is clear that in principle, we may be able to manipulate the concentration of trace metals in seawater to affect a desired change such as enhancing some natural degradation process, shifting the dominant flora and fauna, or increasing the productivity—all of which may be considered aspects of bioremediation lato sensu. Because the concentration of trace metals like iron and copper are very low in seawater—picomoles to nanomoles per liter at the surface —they are particularly apt to be increased inadvertently or purposefully by humans. Certainly we have increased the concentrations of metals in many bays and estuaries in the same way that we have increased nitrogen or phosphorus concentrations. But we have also increased substantially Princeton Environmental Institute, Department of Geosciences, Princeton University, Princeton, NJ
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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP the supply of many trace elements to the entire North Atlantic and North Pacific Oceans through atmospheric pollution. On that scale of ocean basins, the effect of our nitrogen and phosphorus inputs is almost inconsequential. As a result, we can conceive of fertilizing whole regions of the oceans with iron, whereas fertilizing them with nitrogen and phosphorus would be unfeasible. Thus, the subject of bioremediation using metals has a regional (if not quite global) dimension as well as a local one. I focus here exclusively on the use of metals in bioremediation and do not discuss the issue of remediation of metal pollution. Although it is true that metal pollution may be a problem in some marine systems (perhaps even on an ocean-basin scale), the natural biogeochemical processes that cycle trace metals in the marine environment are sufficiently rapid that stopping the pollution is generally all that is required for remediation. In some cases, of course, dredging of metal-laden sediments may be beneficial or necessary. Here I examine the question of the use of trace metals in marine bioremediation using examples that span the whole range of spatial and temporal scales. My concern is with the establishment of a knowledge base that would make such bioremediation technically feasible as well as socially and environmentally responsible. I particularly focus on the need for fundamental understanding of marine processes, from the molecular to the ecological scale, and the development of molecular and synoptic tools appropriate to oceanographic research. Perhaps the most obvious application of bioremediation technology in the marine realm is for the cleanup of oil spills. Stimulating the growth and metabolism of microorganisms that degrade hydrocarbons is certainly feasible on the scale of an oil spill and also one of the few practical options available to us—once prevention and containment have failed. In some instances, additions of nitrogen and phosphorus have been shown to be effective in accelerating the biodegradation of the oil, at least on shore. The relative proportions of these major nutrients to the available organic food source are well known, and it is a relatively simple matter to estimate how much should be added. Not so for trace elements. Many trace elements are necessary for the growth of oil-degrading bacteria, and some, such as iron or copper, are essential cofactors in the very enzymes that catalyze hydrocarbon degradation. Thus, trace metal additions may well be useful, but we have little quantitative knowledge of how much of any particular trace metal is required. In fact it is possible that the metal content of the oil sometimes results in a concentration of some metal in seawater that is too high. For any trace metal, there is only a relatively narrow range of concentrations that is optimal for the growth of marine microorganisms. Below this range, a trace metal is limiting; above it is toxic.
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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP This dual role of trace metals as essential nutrients and as toxicants poses a major difficulty for designing practical protocols for bioremediation. This difficulty is much amplified by the complicated chemistry of trace metals in seawater. Most bioactive metals (e.g., Fe, Co, Ni, Cu, Zn, and Cd) are known to be complexed by strong organic ligands in surface seawater. Titrating these ligands with relatively small additions of metals can result in very large increases in inorganic metal concentrations and, consequently, in metal toxicity. In some cases, it is the addition of a chelator to decrease the inorganic concentration of some metals, rather than the addition of metals, that may be necessary to stimulate the growth of oil-degrading bacteria. To effect a practical bioremediation of oil spills by manipulating trace metal chemistry in seawater requires that we know not only what metals are required by the target organisms and how much, but also what the concentrations of the metals and of their chelators are in seawater and in the oil. One of the most common uses of trace metals for bioremediation is found in the control of noxious algal blooms in fresh waters. A widespread technique for controlling the proliferation of unwanted phytoplankton or macrophyte species in lakes and reservoirs is simply to add relatively large doses of copper sulfate. (The technique is of course also used in swimming pools to keep algal growth to a minimum.) Based on empirical data, the copper is added to a level that is toxic to the target species; that species is killed along with much of the microflora and fauna, and it settles to the sediments, taking with it some fraction of the toxic metal. The process is not always efficacious, of course, and sometimes requires repeated addition of copper sulfate. Sometimes it also has unwanted effects on macrofauna such as fish. It has been suggested that a similar approach could be used to control harmful algal blooms—such as those of toxic dinoflagellate species —in coastal waters (Anderson and Garrison 1997). This may perhaps be a particularly appropriate approach. It is generally thought that the relative concentrations of nutrients, including trace elements, and their availability to the biota may be a key factor in determining which species dominate the assemblage of phytoplankton in a given locale at a given time. This may well be true of noxious or toxic species, and it has been suggested that the apparently increasing frequency of harmful algal blooms may be related to changes in the relative availability of major nutrients and/or trace metals brought about by human activity. Thus, the control of the floral composition of coastal waters by manipulating, or rectifying, trace metal chemistry may indeed be feasible and perhaps be advisable. Besides the formidable practical problems posed by the much larger areas to be treated and the much more dynamic mixing regime of coastal
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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP waters compared with lakes, there are complex chemical and biological issues to contend with, however. A major reason to control noxious algal blooms in coastal waters is to protect the health or edibility of shellfish such as clams or oysters. Thus, a control technology must not only stop the growth of unwanted algal species, it must also preserve the growth of other species that serve as necessary food to the whole ecosystem, including economically important shellfish. The quasicomplete elimination of the aquatic flora that is practiced in small eutrophic lakes cannot be blindly used in coastal ecosystems. An effective metal treatment method requires that we understand thoroughly both the chemistry of trace metals in coastal waters and the role of these metals in the ecology of the phytoplankton. Because of the high concentration of organic compounds in coastal waters, the nature and extent of metal chelation by natural organic complexing agents is even less well understood than it is in open ocean waters. Furthermore, we are just beginning to understand the relationship between trace metals and the physiology of a few species of marine phytoplankton; we are still very far from understanding the ecological role of trace metals in marine systems. Much chemical, biochemical, physiological, and ecological work needs to be done before we can envisage designing and implementing a successful and safe technique for controlling algal blooms by modifying the trace metal chemistry of a coastal area. The relentless increase in atmospheric carbon dioxide concentration (pCO2) and its attendant effect on global warming is of concern to an increasing number of people. This concentration is currently 360 parts per million (ppm); it was 270 ppm 100 years ago, before the massive use of fossil fuel necessitated by the industrial revolution. Atmospheric carbon dioxide was even lower, less than 200 ppm, 15,000 years ago, at the height of the last glacial period. What biogeochemical processes made pCO2so low during glacial times, and can we take advantage of these processes to check the present increase in pCO2? According to one major hypothesis, the very low glacial pCO2 may have been caused by massive fertilization of large regions of the oceans, particularly the Southern Ocean around Antarctica (Price and Morel 1998). This fertilization would have resulted in a more effective uptake of CO2 by photosynthetic marine organisms and its sequestration in deep oceanic waters upon remineralization of the sinking particulate biomass. Iron, transported to the oceans from the continent (along with other trace metals) by the high winds that characterized glacial times, is the hypothesized fertilizer. Indeed, it has now been demonstrated that addition of iron promotes the growth of phytoplankton in some regions of the world's oceans, including the Southern Ocean. Some have suggested—sometimes in jest, sometimes in earnest (Chisholm and Morel 1991) —that we could now engineer the largest (pre-
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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP meditated) bioremediation project of all times by fertilizing the Southern Ocean with iron and sequestering the fossil fuel-derived CO2into the oceanic abyss. Besides the staggering technical problems posed by the scale of such a project, there are profound questions of scientific uncertainty (as well as troubling moral issues). Our present experience with iron fertilization experiments, which scale from beakers to a few square miles of oceans, gives us insight into the response of the system over only a few days. The added iron practically disappears from the system after such time and is incorporated into the biogeochemical processes that cycle iron and other trace metals in surface seawater. What, in fact, would happen to the ecology of the Southern Ocean if we sustained it with a high level of iron fertilization over several years? We have no idea. On a time scale longer than a few days, the response of the system to a steady addition of a limiting nutrient such as iron would become dependent on complex feedback processes between biology and chemistry (such as the production of new chelating agents whose identity and functions are yet unknown) and be dominated by unpredictable successions of primary producers and consumers. Our present understanding of the role of trace metals in marine ecology is certainly no better on an oceanic scale than it is on the scale of red tides or oil slicks. The possible unforeseen environmental consequences, however, are proportionately much greater. The three hypothetical examples of bioremediation by trace metals discussed above point to an urgent need for a sound understanding of the relation between the marine biota and its chemical milieu, at the molecular, organismic, ecologic, and oceanographic levels. Our knowledge of the biochemistry and physiology of marine plants and bacteria is very primitive compared with that of their distant terrestrial cousins. For example, we have only recently become aware of the existence of families of photosynthetic marine prokaryotes —Synechococcus and Prochlorococcus— which are probably the most abundant photosynthetic organisms on earth. Large eukaryotic microalgae such as diatoms and coccolithophores, which are responsible for most of the export of organic carbon to the deep ocean (as well as the bulk of the precipitation of silica and calcium carbonate in the oceans—the process of “reverse weathering”), are evolutionarily very distant from land plants. Their enzymes often bear little homology with those of green plants, and their physiology is poorly understood. There is clearly a need for a sizable research effort on the basic biochemistry and physiology of the microorganisms that are the basis of marine ecosystems. Focusing the efforts of several laboratories on well chosen model experimental organisms (and sequencing their genome) could in a few years lead to a new understanding of how these organisms are adapted to life in the marine environment—an environment characterized chiefly by very low concentrations of nutrients, in-
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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP cluding trace metals. Such research could also be targeted at developing analytical tools and protocols that would allow oceanographers to probe the physiology of these organisms in the field. New biochemical, genetic or immunological markers may allow us to assess directly what elements may be limiting or toxic to the ambient microflora in a given locale at a given time. With appropriate field research, we then should be able to translate this physiological insight into an understanding of the ecological relationships among major taxa of marine microorganisms. To provide the areal coverage necessary for an understanding of these physiological and ecological processes at the scale of oceans, the new experimental molecular tools will have to be made inexpensive and easy to use. If we develop the appropriate knowledge base, we should be able to harness new technology such as “gene chips” to great effect in oceanography. However, if we do not begin now to acquire a fundamental understanding of marine processes at a level commensurate with the advances in the basic disciplines (e.g., biology and chemistry), the application to the marine environment of biotechnology any more refined than major nutrient addition (e.g., modulation of trace metal chemistry), is likely to be technically inefficient and perhaps imprudent. REFERENCES Anderson DM, Garrison DJ, eds. 1997 The ecology and oceanography of harmful algal blooms. Limnol Oceanogr 42: 1009-1305. Chisholm SW, Morel FMM, eds. 1991 What controls phytoplankton production in nutrient-rich areas of the open sea? Limnol Oceanogr 36:1507-1970. Price NM, Morel FMM. 1998 Biological cycling of iron in the ocean. In: Sigel A, Sigel H, eds. Iron Transport and Storage in Microorganisms, Plants, and Animals. Vol 35: Metal Ions in Biological Systems. New York: M. Dekker, Inc.