Rhodobacter capsulatus Catalyzes Light-Dependent Fe(II) Oxidation under Anaerobic Conditions as a Potential Detoxification Mechanism

Abstract

Diverse bacteria are known to oxidize millimolar concentrations of ferrous iron [Fe(II)] under anaerobic conditions, both phototrophically and chemotrophically. Yet whether they can do this under conditions that are relevant to natural systems is understood less well. In this study, we tested how light, Fe(II) speciation, pH, and salinity affected the rate of Fe(II) oxidation by Rhodobacter capsulatus SB1003. Although R. capsulatus cannot grow photoautotrophically on Fe(II), it oxidizes Fe(II) at rates comparable to those of bacteria that do grow photoautotrophically on Fe(II) as soon as it is exposed to light, provided it has a functional photosystem. Chelation of Fe(II) by diverse organic ligands promotes Fe(II) oxidation, and as the pH increases, so does the oxidation rate, except in the presence of nitrilotriacetate; nonchelated forms of Fe(II) are also more rapidly oxidized at higher pH. Salt concentrations typical of marine environments inhibit Fe(II) oxidation. When growing photoheterotrophically on humic substances, R. capsulatus is highly sensitive to low concentrations of Fe(II); it is inhibited in the presence of concentrations as low as 5 M. The product of Fe(II) oxidation, ferric iron, does not hamper growth under these conditions. When other parameters, such as pH or the presence of chelators, are adjusted to promote Fe(II) oxidation, the growth inhibition effect of Fe(II) is alleviated. Together, these results suggest that Fe(II) is toxic to R. capsulatus growing under strictly anaerobic conditions and that Fe(II) oxidation alleviates this toxicity.

Fe(II) Oxidation Is an Innate Capability of Nitrate-Reducing Bacteria That Involves Abiotic and Biotic Reactions

“…1b). Similar concentrations of Fe(II) are inhibitory to the growth of Rhodobacter capsulatus grown under humic acid-oxidizing phototrophic conditions (19). A lag was also observed in NDFO cultures of A. ebreus containing higher Fe(II) concentrations (8 to 10 mM) (see Fig.…”

“…Some studies have demonstrated that Fe(II) at low concentrations is toxic to anaerobic bacteria such as anoxygenic phototrophs (19) or streptococci (20). Several possibilities for anaerobic Fe(II) toxicity include inhibition of the F-ATPase (20), binding to membranes (21), disruption of protein stability or replacement of active-site metal cofactors (22), and oxidation and precipitation of insoluble Fe(III) on cellular components to impair nutrient uptake (13).…”

Induction of Nitrate-Dependent Fe(II) Oxidation by Fe(II) in Dechloromonas sp. Strain UWNR4 and Acidovorax sp. Strain 2AN

“…3c and d) for cells preincubated with Fe(II)-EDTA, showing that Fe(II) exposure does not result in antibiotic resistance. In addition, Fe(II) oxidation has been suggested as a potential detoxification mechanism in the photoheterotrophic, Fe(II)-oxidizing strain Rhodobacter capsulatus SB1003 (32). However, upregulation of such a detoxification response seems unlikely in our studies as we have no evidence of either Fe(II)-or Fe(III)-EDTA toxicity (2).…”

Potential Role of Nitrite for Abiotic Fe(II) Oxidation and Cell Encrustation during Nitrate Reduction by Denitrifying Bacteria

“…Fe 2ϩ is known to be toxic due to the formation of oxygen radicals in the Fenton reaction under oxic conditions (64). There are only a few studies concerning the toxicity of Fe 2ϩ under anoxic conditions (65,66). Some nitrate-reducing Fe(II)-oxidizing strains are not able to grow on dissolved Fe(II) but instead require chelated Fe(II), for example, Paracoccus ferrooxidans (41) and Pseudogulbenkiania strain MAI-1 (67), and it was suggested by those authors that this was due to Fe 2ϩ toxicity.…”