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

Abstract

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 model-and 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 ironorganic 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.

Enhancement of the reactive iron pool by marine diatoms

“…Conversely, the Fe(II) concentrations during the dark period in the incubations with C. brevis were higher than during the previous irradiance period and stayed stable during the second day of irradiance, although a slight increase in Fe(II) was observed in the bottle receiving UVB + UVA + VIS. This suggests that a light independent process, such as superoxide or membrane reductase mediated Fe(III) reduction, might play an additional role (Salmon et al, 2006). There are several mechanisms described for the reduction of Fe(III) by microorganisms that are independent of irradiance.…”

“…The Fe(II) concentration at the end of the dark period in experiment C was higher than the Fe(II) concentration during irradiance on the previous day. These high Fe(II) concentrations in the dark may be ascribed to two different conceivable mechanisms: reduction of Fe(III) in the dark by either superoxide produced by C. brevis as was shown by Kustka et al (2005) for the diatoms Thallassiosira weissflogii and Thallassiosira pseudonana or by extra-cellular enzymes (Maldonado and Price, 2000;Salmon et al, 2006;Shaked et al, 2005).…”

“…Some microorganisms employ an Fe uptake pathway in which Fe(III) is reduced to Fe(II) via superoxide radicals generated by enzymes in the cell membrane (Fujii et al, 2006;Kustka et al, 2005;. Alternatively, Fe(III) can be reduced by membrane reductases (Allnut and Bonner, 1987;Lynnes et al, 1998;Maldonado and Price, 2000;Weger et al, 2002) and additionally via either dissociative or non-dissociative reduction (Salmon et al, 2006) of Fe complexed to Fe-binding ligands.…”

“…Various phytoplankton species seem capable of enzymatic reduction of Fe(III) at the cell surface (Maldonado and Price, 2000). Recently, it was also suggested that reductase induced dissociative or non-dissociative reduction of Fe bound to Fe-binding ligands (Salmon et al, 2006) might form an important process resulting in Fe uptake and the production of Fe(II) in the surrounding medium. Furthermore, Kuma et al (1992) observed high concentrations of Fe(II) during spring blooms in Funka Bay (Japan) and related this to the release of organic components from phytoplankton inducing the photoreduction of Fe.…”

“…Specifically, the Fe redox cycle, as initiated by photochemical processes, is believed to be an important mechanism that converts (colloidal) Fe into more reactive species (defined by the research method applied) resulting in a higher bioavailability for phytoplankton (Finden et al, 1984;Miller and Kester, 1994;. Note, that Fe(II) is suggested to be more bioavailable than Fe(III) (Anderson and Morel, 1980;Anderson and Morel, 1982;Maldonado and Price, 2001;Salmon et al, 2006;Shaked et al, 2005).…”