Speciation and the Bioavailability Conundrum

Not surprisingly, the discovery of the importance of iron in regulating plankton productivity in HNLC areas of the ocean stimulated a renaissance of interest in the marine chemistry of this element. Very quickly, new knowledge began to emerge that made out understanding of this complex situation even more difficult. As already mentioned, iron is very difficult to measure accurately at the very low concentrations observed in seawater, and even now there is no universal agreement on its distribution in ocean waters. This is in spite of some carefully designed intercalibration experiments that have attempted to sort out the best experimental methods for sample collection, handling, and analysis. Nonetheless, some features are now clear.

As mentioned, in the modern ocean iron is present mostly as Fe(iii); this oxidation state is very insoluble in seawater at its normal pH of about 8 because of the very insoluble hydroxide Fe(OH)3. Careful laboratory measurements using purely inorganic salt solutions suggest that at this pH the solubility of Fe(OH)3 is about 0.2 nM. Yet the so-called 'dissolved' Fe concentrations, measured using filtered samples of seawater, are invariably up to 3-4 times higher, even in remote regions. One reason for this discrepancy is that Fe(iii) readily forms colloidal particles of Fe(OH)3 which are small enough to pass through most filters, thus masquerading as 'dissolved' Fe. However, very small ultrafilters can be used to eliminate a lot of the colloidal fraction, but even then the concentrations of the apparently soluble fraction still exceeds the theoretical solubility limit of 0.2 nM.

We now know that this is a result of the interaction of Fe(iii) with natural organic matter (NOM) dissolved in seawater which form coordination complexes with NOM ligands. A number of very sensitive techniques are now available to probe the nature of these NOM complexes, and while there is some variation in the reported results, some general trends are clear. Seawater appears to universally contain an excess of NOM ligands that bind Fe(iii), some of which are extremely strong in a thermo-dynamic sense (large equilibrium constant for formation). in surface waters, there is mounting evidence that the main NOM ligands are of direct biological origin, similar to the 'siderophore' compounds known to be produced by certain terrestrial microorganisms as a mechanism to sequester iron in, for example, soil waters. iron-binding NOM persists throughout the oceanic water column, and it has been estimated that as a result of their presence, the total oceanic inventory of Fe(iii) is raised by a factor of at least 4 over the solubility limit. Clearly this is very important, especially for phytoplankton growing in HNLC areas such as the Southern Ocean, where the main Fe supply may well be the upwelling of deep waters rich (relatively speaking) in NOM-bound iron.

increasing the solubility of dissolved Fe is advantageous only if the Fe bound to NOM can then be rapidly taken up and released as inorganic Fe inside the cell. This may not be a problem for marine prokaryotes. Heterotrophic bacteria and cyanobacteria isolated from marine habitats also produce siderophores when Fe-limited, some of which have been isolated and chemically characterized. Moreover, marine bacteria transport Fe bound to siderophores regardless of whether or not they produce their own. Little is known of the mechanism by which marine bacteria obtain sidero-phore-bound Fe, but there is evidence that its fundamental features resemble those of terrestrial bacteria, which possess outer-membrane receptors that transport a wide range of intact Fe(iii)-siderophore complexes through the cell wall.

However, the binding of Fe by NOM ligands generates a puzzling conundrum for marine eukaryotic phytoplankton. For these organisms, the principal effect of the formation of a coordination complex by a metal ion with NOM ligands is considered to be a 'reduction' in bioavailability. in this paradigm, in order for a metal ion to become available for cellular uptake, it must first dissociate from the NOM complex and become converted into a kinetically available inorganic form such as the free ion Fe3+ or its complexes formed with simple ligands such as OH~ or CP. Only these forms are considered kinetically accessible to ion-uptake mechanisms on the cell wall.

This is why the chelator ethylenediamine tetraacetic acid (EDTA) is added to many culture media. Without it, the metal ions present as impurities in the salts used to prepare the media would be far too toxic for any phyto-plankton to grow. Similarly, chelators like EDTA are used to strip metal ions like Pb2+ when people suffer from lead poisoning.

The conundrum is that Fe, a biologically essential element in drastically short supply in HNLC areas, appears to be bound up by NOM that ought to make it unavailable to much of the phytoplankton community. Worse still, the NOM appears to be of biological origin. So what is really going on with Fe(iii) and the NOM complexes it forms? it does not make sense that phyto-plankton, already struggling with a lack of iron supply, should synthesize iron-binding compounds like sidero-phores unless the formation of Fe(iii) complexes by these materials actually assists them in acquiring iron. That implies that they have some specific mechanisms on the cell surface for unlocking Fe bound by NOM. in support of this, some very elegant culture experiments using radiolabeled Fe conducted on board ship made it clear that oceanic plankton from HNLC areas were able to take up iron much faster than it could possibly dissociate from NOM complexes to form readily available inorganic forms of Fe(iii).

However, at the time of writing, we have no clear idea how this works. One possibility is that photochemistry may play a role. Fe(iii)-containing complexes can be photochemically reduced to Fe(ii) in seawater, in which form the Fe is much more biologically available. However, although recent work has shown that Fe(ii) is generated during daylight hours in seawater, the amount of Fe(ii) produced does not seem to be enough to support much plankton growth.

Biologically mediated reduction of Fe may be an alternative means to increase the biological availability of Fe bound to NOM. Experiments conducted on marine diatoms have shown that Fe(iii)-NOM complexes can be accessed through use of a cell membrane Fe(iii) reductase, similar to systems found in some vascular plants and other eukaryotes. Under Fe deficiency the activity of the reductase is enhanced, enabling these diatoms to acquire Fe bound to a number of natural and synthetic Fe chelators and to grow rapidly. in this type of non-ligand-specific system, reduction of organically bound Fe(iii) results in dissociation of the complex, allowing uptake as inorganic Fe(ii) or as Fe(iii) after reoxidation.

An interesting twist in the reductive uptake process of Fe NOM complexes is the possible involvement of copper. There is evidence from a marine diatom that Fe acquisition involves two consecutive redox transformations of Fe. First Fe(iii) is enzymatically reduced to Fe(ii) by cell membrane reductases, then Fe is taken up by a protein complex containing a multicopper oxidase, which oxidizes Fe(ii) back to Fe(iii) during the membrane transport step. Even though the oxidation of Fe(ii) occurs spontaneously and rapidly in oxygenated seawater, a multicopper oxidase may be important in order to acquire Fe before it diffuses away from the cell. This Fe transport pathway is highly analogous to that identified in common yeast, and some fungi and green algae. Genes homologous to those that encode for the proteins of this pathway have been identified in the recently sequenced genome of the diatom Thalassiosira pseudonana.

See a/so: Biogeochemical Approaches to Environmental Risk Assessment.

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