Mobilization Of Iron By Siderophores 21 Iron availability in the plant rhizosphere

Iron availability in the plant rhizosphere is limited by the extreme insolubility of inorganic iron minerals that dissolve at much slower rates than are required to support plant and microbial growth (Lindsay, 1995). The solubility of inorganic iron is controlled both by the pH and redox of the soil solution and involves a series of iron hydrolysis species that are in equilibrium with iron bearing minerals that have different solubilities that reflect their crystallinity and stability, the most soluble being amorphous iron hydroxide and the least soluble being goethite. The amounts of soluble iron that are maintained by equilibrium with iron minerals have been modelled and can be predicted for specific pH and redox conditions (Figure 8-1).

Figure 8-1. Solubility of inorganic iron in soils as controlled by pH and redox. Diagram is simplified only to show Fe + ion (solid line) and changes in Fe + (short dashed line), the latter which becomes increasingly soluble under reduced conditions (Solubility diagram adapted from Lindsay and Schwab, 1982; Crowley, 2001).

Figure 8-1. Solubility of inorganic iron in soils as controlled by pH and redox. Diagram is simplified only to show Fe + ion (solid line) and changes in Fe + (short dashed line), the latter which becomes increasingly soluble under reduced conditions (Solubility diagram adapted from Lindsay and Schwab, 1982; Crowley, 2001).

As shown in Figure 8-1, the soluble concentrations of the two main hydrolysis species, Fe3+ or Fe2+, are well below the levels that are required by plants and microorganisms. In addition to these two hydrolysis species, there are several others in which the dissolved iron is coordinated by water molecules that dissociate to different degrees to generate Fe(OH)2+, FeOH2+, and Fe(OH)3o (Lindsay, 1979). In the soil solution, the Fe(OH)V, FeOH2+, Fe3+, hydrolysis species of iron all have a similar solubility of approximately 10-6 M at pH 3 and decline thereafter by factors of 10, 100, and 1000-fold, respectively, for every unit increase in pH. Above pH 7, under aerated conditions, the only iron hydrolysis species with any relevance for diffusion of inorganic iron in the soil solution is the neutral hydrolysis species Fe(OH)3o which does not change with respect to pH, and which maintains a constant equilibrium concentration of approximately 10-10 M across all pH values. In contrast to the low concentrations of soluble iron maintained by equilibrium with mineral iron, plants and microorganisms require approximately 1-10 ^.M soluble iron to meet the normal demand for this element during active growth. This is approximately 10,000-fold more than the concentration of inorganic iron in solution that is maintained above pH 4 under aerated conditions.

To solve this problem, plants and microorganisms respond by several different mechanisms to increase the solubility of iron. Strategy I dicots employ reductases and excrete protons to acidify the rhizosphere and lower the redox conditions to increase the solubility of inorganic iron. Microorganisms and Strategy II monocots, on the other hand, rely on organic molecules to increase the solubility of iron. These molecules, called siderophores, are released into the environment to scavenge the low levels of iron in solution and also attack the surfaces of iron minerals to directly mobilize iron from the solid phase minerals. Siderophores may also remove iron from organic iron complexes and stable humic and fulvic acid organic matter where iron is held in complexes with various ligands. Iron availability via siderophores thus involves interactions of these molecules with all of the various sources of iron that are present in the environment as well as between the chelators themselves which may strip iron from other siderophores by ligand exchange. With the exception of the soluble iron in solution, which is chelated almost instantly by these compounds, all other processes involve ligand exchange or dissolution reactions that are much slower and dependent on kinetic processes that are not easy to predict and must be measured empirically. This makes modelling of siderophore function in the environment very difficult to predict, especially in complex mixtures where many factors may influence kinetic processes involving iron dissolution and ligand exchange.

As shown in the conceptual model in Figure 8-2, several pools of iron can potentially be accessed by siderophores. The primary source for replenishing these pools of iron is the solid phase minerals, which represent the largest reservoir of iron in the soil. The dissolution of iron from solid phase iron minerals will have different kinetic rates depending on the crystallinity and surface area of the predominant iron minerals. In addition to the solid phase iron minerals, another source of relatively labile inorganic iron is adsorbed to exchange sites on partially decomposed plant detritus and on stable organic matter in the form of humin, humic and fulvic acids, or on the glycoprotein glomalin, which is produced by mycorrhizal fungi. In the stable organic matter fraction, both humin and humic acids are insoluble, but provide cation binding sites where iron may be tightly complexed but still available for complexation with organic acids or siderophores depending on how well the iron is protected within the organic complexes. Large molecular weight organic complexes may shield access by siderophores, whereas smaller fulvic acid complexes with iron may be more accessible.

Figure 8-2. Conceptual model of iron mobilization by siderophores showing the different sources of iron that are potentially mobilized including inorganic iron, iron in plant detritus and microbial biomass, and in iron humic complexes with organic matter. Iron may also be exchanged from weak complexes with fulvic acid and organic acids in the soil solution or that are adsorbed in clay organic matter complexes.

Figure 8-2. Conceptual model of iron mobilization by siderophores showing the different sources of iron that are potentially mobilized including inorganic iron, iron in plant detritus and microbial biomass, and in iron humic complexes with organic matter. Iron may also be exchanged from weak complexes with fulvic acid and organic acids in the soil solution or that are adsorbed in clay organic matter complexes.

Iron also is associated with various organic molecules such as heme and in iron sulfur proteins in the lysates that are generated from turnover of the microbial biomass and in plant detritus. Lastly, some portion of the potential iron chelating substances including siderophores, themselves, and organic acids will be adsorbed to clay and organic matter complexes through hydrophobic and ionic interactions, and thus may represent a relatively immobile phase of potentially available iron that may be remobilized by exchange with more polar or neutral siderophores and iron chelating substances.

The mechanisms by which siderophores mobilize iron from iron bearing minerals have been recently reviewed by Kraemer (2004), which provides a detailed view of the surface chemistry of iron oxides and iron complex formation by siderophores. At a molecular level, the actual means by which iron is liberated involves a stepwise process in which iron atoms are stripped from the exposed surfaces of iron minerals. Inorganic iron is found in a variety of solid phase minerals including clays, iron phosphates, and iron oxides that vary in their crystallinity and solubility. The iron oxide minerals occlude large amounts of iron within the mineral itself, but on the surface contain iron atoms that are arranged in an octahedral coordination with other atoms in the crystal lattice and with hydroxyl groups and water molecules that are strongly adsorbed in a monolayer on the mineral surface. Siderophores and certain organic acids that complex iron enter the water layer and form inner sphere complexes with iron atoms by attaching one or more ligands to the mineral surface that donate a shared electron to the iron atom and draw it into a new set of ligands that are provided by the siderophore. Once iron is completely removed from the mineral in a new octahedral complex, the siderophore is free to diffuse away and transport iron along a diffusion gradient to the surface of cells that remove iron from solution by uptake across the cell membrane, or that cleave iron from the siderophore by reducing Fe3+ to Fe2+ which is not held as tightly by the siderophore. The ability of the siderophore to diffuse without becoming sorbed onto other surfaces depends on its charge and hydrophobicity, which determine the partitioning of the iron chelate between the soil solution and adsorption onto clay and organic matter.

The rates of iron oxide dissolution vary with respect to their crystallinity, ranging from amorphous iron oxides that are relatively easy to dissolve to goethite and hematite, which have very slow dissolution rates. Iron oxides and clay silicates are often associated with humic and fulvic acids, organic acids, and polysaccharides in clay-organic matter complexes that can further affect their dissolution rates and surface chemistry. To date, there are only a few model systems that have been studied, in which the kinetics of iron dissolution from different solid phases has been determined empirically for a few representative siderophore and phytosiderophores types and with a few representative synthetic or natural iron oxides. As compared to chelation with soluble iron which is instantaneous, the surface dissolution kinetics of iron oxides is relatively slow and may take hours to days for all of the siderophore to become complexed with iron. The rates of dissolution will depend on the pH and ionic composition of the solution and relative amounts of siderophore in comparison to the surface area of iron oxides. Overall, there is a linear relationship between the surface excess of siderophores and the dissolution rates of iron oxides, such that dissolution rates increase proportionately with the concentration of siderophore (Cheah et al., 2003). In other words, at low concentrations the dissolution rates will be lower than when there is a large concentration of deferrated siderophore. The deferrated siderophore that accumulates in solution suppresses the concentrations of iron hydrolysis species in the solution to extremely low concentrations such that the only available iron is that which is chelated with siderophores. This establishes competition for iron depending on the ability of an organism to use the predominant siderophore types.

The second important source of iron that is potentially mobilizable by siderophores is that which is held by organic matter complexes either in stable organic matter fractions including humic and fulvic acids or in plant detritus. Siderophores are capable of mobilizing iron that is contained in humic acids, and have much greater specificity and stability with iron than soil organic matter. Access to this iron, however, can be limited by the structural complexity of soil organic matter where iron may be occluded by the surrounding matrix. Humic acids containing high amounts of aromatic constituents are apparently less accessible than those containing more aliphatic hydrocarbons, which reflect differences in the structural complexity of humic substances (Piccolo et al., 1993).

Along with humic substances, plant detritus is also an important iron source, some of which may be mobilized by siderophores and recycled into the biomass before precipitation as inorganic iron minerals (Mazoy and Lemos, 1991; Chen et al., 2000). Plants contain iron in many different redox proteins that have metal centers involving heme or iron sulfur complexes. This iron can be accessed during degradation of proteins, which release the soluble heme iron complex into the soil solution. Some microorganisms apparently have the ability to transport heme-iron which would negate the need for production of siderophores (Nienaber et al., 2001). Conversely, other compounds that are produced during plant decomposition such as polyphenols hold iron in a form that is accessible only to siderophore producing microorganisms (Mila et al., 1996). In this manner, soils that are rich in organic matter, or that have been amended with iron supplemented organic matter amendments provide an important source of iron that can be mobilized for uptake by microorganisms and possibly by plants that use siderophores directly or indirectly for iron nutrition. The impact of organic matter on reducing competition for iron between microorganisms and in reducing the amounts of siderophore that are needed to obtain iron also has been examined for composts (De Brito Alvarez et al., 1995). Higher numbers of siderophore producers were found in composts that were suppressive to an array of pathogenic fungi, which suggests that siderophores contained in composts could have a role in antagonism of plant pathogens by iron deprivation or are necessary to survival and efficacy of bacteria that are antagonistic to plant pathogens. There is clearly a need for more research on this topic to improve compost use for biocontrol of plant diseases.

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