The FeL model of iron acquisition: Nondissociative reduction of ferric complexes in the marine environment

Recently there has been recognition of the importance of reductive processes in the acquisition of iron by microorganisms in marine environments with Fe(III) reduction induced by either membrane-bound reductases or by superoxide, a powerful Fe(III) reducing agent generated either by photochemical or biological means. We have measured the relative rates of iron uptake achieved by the cyanobacterium L. majuscula in the presence of a variety of modeland naturally-derived organic ligands exhibiting a broad range of conditional ferric and ferrous stability constants. Additionally, we have investigated the effect upon iron uptake rate of varying the concentration of both iron and the iron-binding ligands. We have reconciled this data with previous work in which we measured rates of reduction by exogenous superoxide of Fe(III) bound to these same complexes. We show that the rate of formation of ferrous iron and the rate of uptake of iron by Lyngbya majuscula are each independent of the concentration of Fe9 and demonstrate that this is consistent with our previous finding that this organism acquires iron via nondissociative reduction of ferric complexes. We also show that the rate of reoxidation of organically complexed Fe(II) is a critical determinant of the subsequent bioavailability of iron, a feature not previously addressed in the literature. In view of the central importance of the complexation and redox behavior of the iron– organic complexes to iron uptake rate, we propose a new kinetic model of iron acquisition, termed the FeL model, that is consistent with presented and previously published data and which describes processes both in natural and artificial conditions. Iron is an essential micronutrient for all known forms of marine life (Crichton 2001; Sunda 2002) yet is quite insoluble under pH and redox conditions typical of marine systems, and the resultant particulate form is generally considered relatively nonbioavailable. Consequently, a variety of iron acquisition strategies have been developed by marine organisms, in some cases requiring great expenditure of other metabolic resources. Many common metabolic activities require iron as a cofactor, particularly those involving redox exchanges such as oxidative respiration. Photosynthesis and nitrogen fixation are two complex aspects of metabolism with a high requirement for iron (Rueter and Petersenc 1987; Raven 1988; Rueter 1988; Geider and La Roche 1994). Each is prevalent among marine microorganisms, which make up the great majority of marine biota (Whitman et al. 1998); thus, in combination, they determine a high proportion of the total biological iron requirement in both oceanic and coastal waters (Capone et al. 1997). In natural waters, iron exists predominantly in either the reduced ferrous (Fe[II]) or the oxidized ferric (Fe[III]) redox states, each of which can react with various oxygen species present in the aquatic system (Gledhill and van den Berg 1995; Millero et al. 1995; Waite et al. 1995). These oxygen species include the fully oxidized form, dioxygen (O2), and partially reduced forms known as reactive oxygen species. Given the redox potentials of the iron and oxygen systems, ferric iron is the thermodynamically favored form of iron in oxygenated marine waters. Ferric iron is highly insoluble at circumneutral pH and is rapidly hydrolyzed to form amorphous, particulate oxyhydroxides that are biologically unavailable. Importantly however, terrestrially 1 Corresponding author ([email protected]). Acknowledgments We thank Simon Albert and the Marine Botany group at The University of Queensland for provision of Lyngbya majuscula and assistance with field aspects of this study. Tredwell Lukondeh is thanked for assistance with laboratory investigations. The input provided by anonymous reviewers improved the manuscript significantly. This work was supported by ARC Linkage Grant LP0219352 and ARC Discovery Grant DP0558710. Limnol. Oceanogr., 51(4), 2006, 1744–1754 E 2006, by the American Society of Limnology and Oceanography, Inc.