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Induction of nitrate-dependent Fe(II) oxidation by Fe(II) in Dechloromonas sp. strain UWNR4 and Acidovorax sp. strain 2AN.

ABSTRACT: We evaluated the inducibility of nitrate-dependent Fe(II)-EDTA oxidation (NDFO) in non-growth, chloramphenicol-amended, resting-cell suspensions of Dechloromonas sp. strain UWNR4 and Acidovorax sp. strain 2AN. Cells previously incubated with Fe(II)-EDTA oxidized ca. 6-fold more Fe(II)-EDTA than cells previously incubated with Fe(III)-EDTA. This is the first report of induction of NDFO by Fe(II).

SUBMITTER: Chakraborty A

PROVIDER: S-EPMC3553780 | biostudies-literature | 2013 Jan

REPOSITORIES: biostudies-literature

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Induction of nitrate-dependent Fe(II) oxidation by Fe(II) in Dechloromonas sp. strain UWNR4 and Acidovorax sp. strain 2AN.

Chakraborty Anirban A Picardal Flynn F

Applied and environmental microbiology 20121109 2

We evaluated the inducibility of nitrate-dependent Fe(II)-EDTA oxidation (NDFO) in non-growth, chloramphenicol-amended, resting-cell suspensions of Dechloromonas sp. strain UWNR4 and Acidovorax sp. strain 2AN. Cells previously incubated with Fe(II)-EDTA oxidized ca. 6-fold more Fe(II)-EDTA than cells previously incubated with Fe(III)-EDTA. This is the first report of induction of NDFO by Fe(II). ...[more]

PMID: 23144134

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Project description:Microbial nitrate-dependent Fe(II) oxidation is known to contribute to iron biogeochemical cycling; however, the microorganisms responsible are virtually unknown. In an effort to elucidate this microbial metabolic process in the context of an environmental system, a 14-cm sediment core was collected from a freshwater lake and geochemically characterized concurrently with the enumeration of the nitrate-dependent Fe(II)-oxidizing microbial community and subsequent isolation of a nitrate-dependent Fe(II)-oxidizing microorganism. Throughout the sediment core, ambient concentrations of Fe(II) and nitrate were observed to coexist. Concomitant most probable number enumeration revealed the presence of an abundant nitrate-dependent Fe(II)-oxidizing microbial community (2.4 x 10(3) to 1.5 x 10(4) cells g(-1) wet sediment) from which a novel anaerobic, lithoautotrophic, Fe(II)-oxidizing bacterium, strain 2002, was isolated. Analysis of the complete 16S rRNA gene sequence revealed that strain 2002 was a member of the beta subclass of the proteobacteria with 94.8% similarity to Chromobacterium violaceum, a bacterium not previously recognized for the ability to oxidize nitrate-dependent Fe(II). Under nongrowth conditions, both strain 2002 and C. violaceum incompletely reduced nitrate to nitrite with Fe(II) as the electron donor, while under growth conditions nitrate was reduced to gaseous end products (N2 and N2O). Lithoautotrophic metabolism under nitrate-dependent Fe(II)-oxidizing conditions was verified by the requirement of CO2 for growth as well as the assimilation of 14C-labeled CO2 into biomass. The isolation of strain 2002 represents the first example of an anaerobic, mesophilic, neutrophilic Fe(II)-oxidizing lithoautotroph isolated from freshwater samples. Our studies further demonstrate the abundance of nitrate-dependent Fe(II) oxidizers in freshwater lake sediments and provide further evidence for the potential of microbially mediated Fe(II) oxidation in anoxic environments.

Project description:Microbial biomineralization sometimes leads to periplasmic encrustation, which is predicted to enhance microorganism preservation in the fossil record. Mineral precipitation within the periplasm is, however, thought to induce death, as a result of permeability loss preventing nutrient and waste transit across the cell wall. This hypothesis had, however, never been investigated down to the single cell level. Here, we cultured the nitrate reducing Fe(II) oxidizing bacteria Acidovorax sp. strain BoFeN1 that have been previously shown to promote the precipitation of a diversity of Fe minerals (lepidocrocite, goethite, Fe phosphate) encrusting the periplasm. We investigated the connection of Fe biomineralization with carbon assimilation at the single cell level, using a combination of electron microscopy and Nano-Secondary Ion Mass Spectrometry. Our analyses revealed strong individual heterogeneities of Fe biomineralization. Noteworthy, a small proportion of cells remaining free of any precipitate persisted even at advanced stages of biomineralization. Using pulse chase experiments with (13)C-acetate, we provide evidence of individual phenotypic heterogeneities of carbon assimilation, correlated with the level of Fe biomineralization. Whereas non- and moderately encrusted cells were able to assimilate acetate, higher levels of periplasmic encrustation prevented any carbon incorporation. Carbon assimilation only depended on the level of Fe encrustation and not on the nature of Fe minerals precipitated in the cell wall. Carbon assimilation decreased exponentially with increasing cell-associated Fe content. Persistence of a small proportion of non-mineralized and metabolically active cells might constitute a survival strategy in highly ferruginous environments. Eventually, our results suggest that periplasmic Fe biomineralization may provide a signature of individual metabolic status, which could be looked for in the fossil record and in modern environmental samples.

Dataset Information

Induction of nitrate-dependent Fe(II) oxidation by Fe(II) in Dechloromonas sp. strain UWNR4 and Acidovorax sp. strain 2AN.

Publications

Induction of nitrate-dependent Fe(II) oxidation by Fe(II) in Dechloromonas sp. strain UWNR4 and Acidovorax sp. strain 2AN.

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