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Nitrate-dependent ferrous iron oxidation by anaerobic ammonium oxidation (anammox) bacteria.

ABSTRACT: We examined nitrate-dependent Fe(2+) oxidation mediated by anaerobic ammonium oxidation (anammox) bacteria. Enrichment cultures of "Candidatus Brocadia sinica" anaerobically oxidized Fe(2+) and reduced NO3(-) to nitrogen gas at rates of 3.7 ± 0.2 and 1.3 ± 0.1 (mean ± standard deviation [SD]) nmol mg protein(-1) min(-1), respectively (37°C and pH 7.3). This nitrate reduction rate is an order of magnitude lower than the anammox activity of "Ca. Brocadia sinica" (10 to 75 nmol NH4(+) mg protein(-1) min(-1)). A (15)N tracer experiment demonstrated that coupling of nitrate-dependent Fe(2+) oxidation and the anammox reaction was responsible for producing nitrogen gas from NO3(-) by "Ca. Brocadia sinica." The activities of nitrate-dependent Fe(2+) oxidation were dependent on temperature and pH, and the highest activities were seen at temperatures of 30 to 45°C and pHs ranging from 5.9 to 9.8. The mean half-saturation constant for NO3(-) ± SD of "Ca. Brocadia sinica" was determined to be 51 ± 21 ?M. Nitrate-dependent Fe(2+) oxidation was further demonstrated by another anammox bacterium, "Candidatus Scalindua sp.," whose rates of Fe(2+) oxidation and NO3(-) reduction were 4.7 ± 0.59 and 1.45 ± 0.05 nmol mg protein(-1) min(-1), respectively (20°C and pH 7.3). Co-occurrence of nitrate-dependent Fe(2+) oxidation and the anammox reaction decreased the molar ratios of consumed NO2(-) to consumed NH4(+) (?NO2(-)/?NH4(+)) and produced NO3(-) to consumed NH4(+) (?NO3(-)/?NH4(+)). These reactions are preferable to the application of anammox processes for wastewater treatment.

SUBMITTER: Oshiki M

PROVIDER: S-EPMC3697569 | biostudies-literature | 2013 Jul

REPOSITORIES: biostudies-literature

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Nitrate-dependent ferrous iron oxidation by anaerobic ammonium oxidation (anammox) bacteria.

Oshiki M M Ishii S S Yoshida K K Fujii N N Ishiguro M M Satoh H H Okabe S S

Applied and environmental microbiology 20130426 13

We examined nitrate-dependent Fe(2+) oxidation mediated by anaerobic ammonium oxidation (anammox) bacteria. Enrichment cultures of "Candidatus Brocadia sinica" anaerobically oxidized Fe(2+) and reduced NO3(-) to nitrogen gas at rates of 3.7 ± 0.2 and 1.3 ± 0.1 (mean ± standard deviation [SD]) nmol mg protein(-1) min(-1), respectively (37°C and pH 7.3). This nitrate reduction rate is an order of magnitude lower than the anammox activity of "Ca. Brocadia sinica" (10 to 75 nmol NH4(+) mg protein(-1 ...[more]

PMID: 23624480

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Project description:Open-water unit process wetlands host a benthic diatomaceous and bacterial assemblage capable of nitrate removal from treated municipal wastewater with unexpected contributions from anammox processes. In exploring mechanistic drivers of anammox, 16S rRNA gene sequencing profiles of the biomat revealed significant microbial community shifts along the flow path and with depth. Notably, there was an increasing abundance of sulfate reducers (Desulfococcus and other Deltaproteobacteria) and anammox microorganisms (Brocadiaceae) with depth. Pore water profiles demonstrated that nitrate and sulfate concentrations exhibited a commensurate decrease with biomat depth accompanied by the accumulation of ammonium. Quantitative PCR targeting the anammox hydrazine synthase gene, hzsA, revealed a 3-fold increase in abundance with biomat depth as well as a 2-fold increase in the sulfate reductase gene, dsrA These microbial and geochemical trends were most pronounced in proximity to the influent region of the wetland where the biomat was thickest and influent nitrate concentrations were highest. While direct genetic queries for dissimilatory nitrate reduction to ammonium (DNRA) microorganisms proved unsuccessful, an increasing depth-dependent dominance of Gammaproteobacteria and diatoms that have previously been functionally linked to DNRA was observed. To further explore this potential, a series of microcosms containing field-derived biomat material confirmed the ability of the community to produce sulfide and reduce nitrate; however, significant ammonium production was observed only in the presence of hydrogen sulfide. Collectively, these results suggest that biogenic sulfide induces DNRA, which in turn can explain the requisite coproduction of ammonium and nitrite from nitrified effluent necessary to sustain the anammox community.IMPORTANCE This study aims to increase understanding of why and how anammox is occurring in an engineered wetland with limited exogenous contributions of ammonium and nitrite. In doing so, the study has implications for how geochemical parameters could potentially be leveraged to impact nutrient cycling and attenuation during the operation of treatment wetlands. The work also contributes to ongoing discussions about biogeochemical signatures surrounding anammox processes and enhances our understanding of the contributions of anammox processes in freshwater environments.

Project description:Anoxic iron-rich sediment samples that had been stored in the light showed development of brown, rusty patches. Subcultures in defined mineral media with ferrous iron (10 mmol/liter, mostly precipitated as FeCO3) yielded enrichments of anoxygenic phototrophic bacteria which used ferrous iron as the sole electron donor for photosynthesis. Two different types of purple bacteria, represented by strains L7 and SW2, were isolated which oxidized colorless ferrous iron under anoxic conditions in the light to brown ferric iron. Strain L7 had rod-shaped, nonmotile cells (1.3 by 2 to 3 microns) which frequently formed gas vesicles. In addition to ferrous iron, strain L7 used H2 + CO2, acetate, pyruvate, and glucose as substrate for phototrophic growth. Strain SW2 had small rod-shaped, nonmotile cells (0.5 by 1 to 1.5 microns). Besides ferrous iron, strain SW2 utilized H2 + CO2, monocarboxylic acids, glucose, and fructose. Neither strain utilized free sulfide; however, both strains grew on black ferrous sulfide (FeS) which was converted to ferric iron and sulfate. Strains L7 and SW2 grown photoheterotrophically without ferrous iron were purple to brownish red and yellowish brown, respectively; absorption spectra revealed peaks characteristic of bacteriochlorophyll a. The closest phototrophic relatives of strains L7 and SW2 so far examined on the basis of 16S rRNA sequences were species of the genera Chromatium (gamma subclass of proteobacteria) and Rhodobacter (alpha subclass), respectively. In mineral medium, the new isolates formed 7.6 g of cell dry mass per mol of Fe(II) oxidized, which is in good agreement with a photoautotrophic utilization of ferrous iron as electron donor for CO2 fixation. Dependence of ferrous iron oxidation on light and CO2 was also demonstrated in dense cell suspensions. In media containing both ferrous iron and an organic substrate (e.g., acetate, glucose), strain L7 utilized ferrous iron and the organic compound simultaneously; in contrast, strain SW2 started to oxidize ferrous iron only after consumption of the organic electron donor. Ferrous iron oxidation by anoxygenic phototrophs is understandable in terms of energetics. In contrast to the Fe3+/Fe2+ pair (E0 = +0.77 V) existing in acidic solutions, the relevant redox pair at pH 7 in bicarbonate-containing environments, Fe(OH)3 + HCO3-/FeCO3, has an E0' of +0.2 V. Ferrous iron at pH 7 can therefore donate electrons to the photosystem of anoxygenic phototrophs, which in purple bacteria has a midpoint potential around +0.45 V. The existence of ferrous iron-oxidizing anoxygenic phototrophs may offer an explanation for the deposition of early banded-iron formations in an assumed anoxic biosphere in Archean times.

Dataset Information

Nitrate-dependent ferrous iron oxidation by anaerobic ammonium oxidation (anammox) bacteria.

Publications

Nitrate-dependent ferrous iron oxidation by anaerobic ammonium oxidation (anammox) bacteria.

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