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The Role of Trace Metals in the Oceanic Cycles of Major Nutrients F

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The Role of Trace Metals in the Oceanic Cycles of Major Nutrients F 6.05 Marine Bioinorganic Chemistry: The Role of Trace Metals in the Oceanic Cycles of Major Nutrients F. M. M. Morel, A. J. Milligan, and M. A. Saito Princeton University, NJ, USA 6.05.1 INTRODUCTION: THE SCOPE OF MARINE BIOINORGANIC CHEMISTRY 113 6.05.2 TRACE METALS IN MARINE MICROORGANISMS 114 6.05.2.1 Concentrations 114 6.05.2.2 Uptake 116 6.05.2.3 Trace Element Storage 121 6.05.3 THE BIOCHEMICAL FUNCTIONS OF TRACE ELEMENTS IN THE UPTAKE AND TRANSFORMATIONS OF NUTRIENTS 122 6.05.3.1 Trace Metals and the Marine Carbon Cycle 123 6.05.3.1.1 Light reaction of photosynthesis 123 6.05.3.1.2 Dark reaction of photosynthesis 124 6.05.3.1.3 Carbon concentrating mechanisms 124 6.05.3.1.4 Respiration 125 6.05.3.2 Trace Metals and the Nitrogen Cycle 126 6.05.3.2.1 Acquisition of fixed nitrogen by phytoplankton 126 6.05.3.2.2 N2 fixation and the nitrogen cycle 127 6.05.3.3 Phosphorus Uptake 128 6.05.3.4 Silicon Uptake 128 6.05.4 EFFECTS OF TRACE METALS ON MARINE BIOGEOCHEMICAL CYCLES 128 6.05.4.1 Iron 128 6.05.4.1.1 Iron and growth rates 128 6.05.4.1.2 Iron uptake 129 6.05.4.1.3 Iron and electron transfer 130 6.05.4.1.4 Iron and nitrogen acquisition 131 6.05.4.2 Manganese 131 6.05.4.3 Zinc, Cobalt, and Cadmium 132 6.05.4.4 Copper 136 6.05.4.5 Nickel 137 6.05.5 EPILOGUE 138 6.05.5.1 Paleoceanographic Aspects 138 6.05.5.2 A View to the Future 139 ACKNOWLEDGMENTS 139 REFERENCES 140 6.05.1 INTRODUCTION: THE SCOPE OF hydrogen, oxygen, nitrogen, phosphorus, sodium, MARINE BIOINORGANIC CHEMISTRY potassium, chlorine, calcium, magnesium, sulfur (and silicon in diatoms)—whose proportions vary The bulk of living biomass is chiefly made up within a relatively narrow range in most organ- of only a dozen “major” elements—carbon, isms. A number of trace elements, particularly first 113 114 Marine Bioinorganic Chemistry row transition metals—manganese, iron, nickel, of the marine sulfur cycle. Seven trace metals cobalt, copper, and zinc—are also “essential” for provide the intrigue: manganese, iron, nickel, the growth of organisms. At the molecular level, cobalt, copper, zinc, and cadmium. But several the chemical mechanisms by which such elements other trace elements such as selenium, vanadium, function as active centers or structural factors in molybdenum, and tungsten (and, probably, others enzymes and by which they are accumulated and not yet identified) will assuredly add further twists stored by organisms is the central topic of in future episodes. bioinorganic chemistry. At the scale of ocean We begin this chapter by discussing what we basins, the interplay of physical, chemical, and know of the concentrations of trace elements in biological processes that govern the cycling of marine microorganisms and of the relevant biologically essential elements in seawater is the mechanisms and kinetics of trace-metal uptake. subject of marine biogeochemistry. For those We then review the biochemical role of trace interested in the growth of marine organisms, elements in the marine cycles of carbon, nitrogen, particularly in the one-half of the Earth’s primary phosphorus, and silicon. Using this information, production contributed by marine phytoplankton, we examine the evidence, emanating from both bioinorganic chemistry and marine biogeochem- laboratory cultures and field measurements, rele- istry are critically linked by the extraordinary vant to the mechanisms and the extent of control paucity of essential trace elements in surface by trace metals of marine biogeochemical cycles. seawater, which results from their biological utili- Before concluding with a wistful glimpse of the zation and incorporation in sinking organic matter. future of marine bioinorganic chemistry we How marine organisms acquire elements that are discuss briefly some paleoceanographic aspects present at nano- or picomolar concentrations in of this new field: how the chemistry of the planet surface seawater; how they perform critical “Earth”—particularly the concentrations of trace enzymatic functions when necessary metal cofac- elements in the oceans—has evolved since its tors are almost unavailable are the central topics of origin, chiefly as a result of biological processes “marine bioinorganic chemistry.” The central aim and how the evolution of life has, in turn, been of this field is to elucidate at the molecular level affected by the availability of essential trace the metal-dependent biological processes involved elements. in the major biogeochemical cycles. By examining the solutions that emerged from the problems posed by the scarcity of essential 6.05.2 TRACE METALS IN MARINE trace elements, marine bioinorganic chemists MICROORGANISMS bring to light hitherto unknown ways to take up or utilize trace elements, new molecules, and 6.05.2.1 Concentrations newer “essential” elements. Focusing on molecu- Bioinorganic chemists are now interested in the lar mechanisms involved in such processes as overall concentration and chemical speciation of inorganic carbon fixation, organic carbon respir- trace elements in cells (O’Halloran and Culotta, ation, or nitrogen transformation, they explain 2000). In parallel with the “genome” and the how the cycles of trace elements are critically “proteome” in organisms, some have begun to talk linked to those of major nutrients such as carbon of the “metallome” (Outten and O’Halloran, or nitrogen. But we have relatively little under- 2001) to designate the suite of trace-metal con- standing of the binding molecules and the centrations, and perhaps the topic of this section enzymes that mediate the biochemical role of could be described as “marine metallomics.” trace metals in the marine environment. In this What emerges from studies of trace-element sense, this chapter is more a “preview” than a concentrations in various types of cells, chiefly review of the field of marine bioinorganic in unicellular organisms, is that these cellular chemistry. To exemplify the concepts and concentrations are maintained at reasonably methods of this field, we have chosen to focus similar proportions among organisms from widely on one of its most important topics: the potentially different taxa. This is exemplified in Figure 1, limiting role of trace elements in primary marine which shows the trace-metal composition of a few production. As a result we center our discussion species of eukaryotic marine phytoplankton in on particular subsets of organisms, biogeochem- cultures (Ho et al., in press). Averaging the data ical cycles, and trace elements. Our chief actors given in Figure 1 provides an extension to are marine phytoplankton, particularly euka- Redfield formula (C106N16P1): ryotes, while heterotrophic bacteria make only cameo appearances. The biogeochemical cycles ðC106N16P1Þ£1000Fe8Mn4Zn0:8Cu0:4Co0:2Cd0:2 that will serve as our plot are those of the elements involved in phytoplankton growth, the major algal The stoichiometric coefficients of this average nutrients—carbon, nitrogen, phosphorus, and formula are within a factor of 3 of the elemental silicon—leaving aside, e.g., the interesting topic proportions measured for almost all individual Trace Metals in Marine Microorganisms 115 Figure 2 Cellular zinc normalized to carbon (a) and Figure 1 Cellular trace metals amounts normalized to specific growth rate (b) as functions of log(Zn0) 0 ¼ phosphorus in a variety of phytoplankton. Cd 20 pM; (unchelated zinc concentration) in a marine diatom 0 ¼ 0 ¼ 0 ¼ 0¼ Co 20 pM; Cu 0.2 pM; Fe 200 pM; Mn Thalassiosira weissflogii (squares) and two clones of a 0 ¼ 10 nM; Zn 20 pM (source Ho et al., in press). marine coccolithophorid Emiliana huxleyi (triangles) (after Sunda and Huntsman, 1992). species. As expected, iron and manganese are quantitatively the most important trace elements in is trace-metal-poor seawater (Morel et al., 1979; marine phytoplankton, being on average about 10 Price et al., 1988/1989). In most instances, it has times more abundant than zinc, copper, cobalt, or been found practical to control the bioavailability cadmium. But there are obvious differences among of trace metals by using strong chelating agents major taxa; e.g., green algae (which are rarely such as EDTA (designated Y). Because the rate of uptake of a metal, M, is usually proportional to its dominant in the oceans) have higher iron, zinc, and 0 copper than diatoms or coccolithophores, which unchelated concentration (often designated as M contain relatively higher proportions of manga- and sometimes referred to as the “inorganic” nese, cobalt, and cadmium. concentration of M), the chelated metal provides a M0 To what extent do the data presented in Figure 1 convenient buffer that maintains at constant low values in the growth medium over the course reflect the physiology of the organisms or the of a batch culture. The value of M0 can be composition of their growth medium? This is precisely adjusted by choosing an appropriate obviously a key question for marine metallomics ratio of the total concentrations of M and Y. and the extant literature on marine microorgan- A general observation is that the cellular isms indeed indicates particular attention given to concentration of an element—its so-called cellular the relation between the composition of organisms “quota”—varies in a sigmoidal fashion as a and their growth medium (e.g., Anderson and function of its concentration in the medium. This Morel, 1982; Hudson and Morel, 1990; Saito et al., is illustrated in Figure 2(a) for zinc in two model 2002; Sunda and Guillard, 1976; Sunda and species, a marine diatom and a coccolithophore Huntsman, 1992). Some of the differences (Sunda and Huntsman, 1992). Over a reasonably between the data of Figure 1 and similar data wide range of unchelated metal concentration, an published for S.
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