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

Abstract

Phylogenetically diverse species of bacteria can catalyze the oxidation of ferrous iron [Fe(II)] coupled to nitrate (NO 3؊ ) reduction, often referred to as nitrate-dependent iron oxidation (NDFO). Very little is known about the biochemistry of NDFO, and though growth benefits have been observed, mineral encrustations and nitrite accumulation likely limit growth. Acidovorax ebreus, like other species in the Acidovorax genus, is proficient at catalyzing NDFO. Our results suggest that the induction of specific Fe(II) oxidoreductase proteins is not required for NDFO. No upregulated periplasmic or outer membrane redox-active proteins, like those involved in Fe(II) oxidation by acidophilic iron oxidizers or anaerobic photoferrotrophs, were observed in proteomic experiments. We demonstrate that while "abiotic" extracellular reactions between Fe(II) and biogenic NO 2 ؊ /NO can be involved in NDFO, intracellular reactions between Fe(II) and periplasmic components are essential to initiate extensive NDFO. We present evidence that an organic cosubstrate inhibits NDFO, likely by keeping periplasmic enzymes in their reduced state, stimulating metal efflux pumping, or both, and that growth during NDFO relies on the capacity of a nitrate-reducing bacterium to overcome the toxicity of Fe(II) and reactive nitrogen species. On the basis of our data and evidence in the literature, we postulate that all respiratory nitrate-reducing bacteria are innately capable of catalyzing NDFO. Our findings have implications for a mechanistic understanding of NDFO, the biogeochemical controls on anaerobic Fe(II) oxidation, and the production of NO 2 ؊ , NO, and N 2 O in the environment.

Coexistence of Microaerophilic, Nitrate-Reducing, and Phototrophic Fe(II) Oxidizers and Fe(III) Reducers in Coastal Marine Sediment

“…For the cultivated mixotrophic nitratereducing Fe(II) oxidizers, it could be that Fe(II) oxidation is not an enzymatic process but an abiotic side reaction caused by nitrite that is formed during heterotrophic denitrification (27). It could even be that this side reaction is unavoidable during denitrification in the presence of Fe(II) (28). Thus, such indirect Fe(II) oxidation could be important in nitrate-and organic-rich marine sediments, such as in Norsminde Fjord.…”

“…For these mixotrophic strains, it is not yet known whether Fe(II) oxidation is just a chemical side reaction with nitrite, which is produced during heterotrophic denitrification (26,27), or if it is an enzymatic reaction from which the bacteria can gain energy. Interestingly, Fe(II) oxidation seems to be a universal ability of all NO 3 Ϫ -reducing bacteria when an organic substrate is provided (28). A unique feature of this group of Fe(II) oxidizers is that the cells become encrusted with Fe(III) minerals during Fe(II) oxidation (27), a process that is potentially harmful to the cells (29).…”

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

“…Evidence for an enzymatic Fe(II) oxidation was provided by Chakraborty and Picardal (23), who found that Fe(II) oxidation is inducible at an enzymatic level for Acidovorax strain 2AN. In contrast, Carlson et al (50) did not see inducible Fe(II) oxidation for Acidovorax ebreus strain TPSY, and in a proteomic study with the same strain, those authors did not find any specific proteins responsible for Fe(II) oxidation. Although the main question therefore still remains whether in these strains Fe(II) oxidation may be caused partly or even completely by an abiotic reaction with nitrite/NO, our present study showed that ordinary nitrate-reducing bacteria show nitrite accumulation and Fe(II) oxidation rates similar to those of two nitrate-reducing strains that were isolated as Fe(II) oxidizers.…”

Internal phosphorus loading in Canadian fresh waters: a critical review and data analysis

“…Their use as an electron acceptor in anaerobic microbial metabolism is more thermodynamically favourable than ferric oxides (Hyacinthe and Van Cappellen 2004). Conversely, ferrous phosphates have been shown to be sensitive to rapid oxidative dissolution and precipitation as ferric phases in the presence of oxygen (e.g., Roldán et al 2002) and by nitrate-reducing, iron-oxidizing bacteria (Miot et al 2009;Carlson et al 2013).…”