Life at the energetic edge: kinetics of circumneutral iron oxidation by lithotrophic iron-oxidizing bacteria isolated from the wetland-plant rhizosphere (original) (raw)
Related papers
2003
Iron plaque occurs on the roots of most wetland and submersed aquatic plant species and is a large pool of oxidized Fe(III) in some environments. Because plaque formation in wetlands with circumneutral pH has been largely assumed to be an abiotic process, no systematic effort has been made to describe plaque-associated microbial communities or their role in plaque deposition. We hypothesized that Fe(II)-oxidizing bacteria (FeOB) and Fe(III)-reducing bacteria (FeRB) are abundant in the rhizosphere of wetland plants across a wide range of biogeochemical environments. In a survey of 13 wetland and aquatic habitats in the Mid-Atlantic region, FeOB were present in the rhizosphere of 92% of the plant specimens collected (n = 37), representing 25 plant species. In a subsequent study at six of these sites, bacterial abundances were determined in the rhizosphere and bulk soil using the most probable number technique. The soil had significantly more total bacteria than the roots on a dry mass basis (
Geomicrobiology Journal, 2015
Oxidation and reduction of iron can occur through abiotic (chemical) and biotic (microbial) processes. Abiotic iron oxidation is a function of pH and O 2 concentration. Biotic iron oxidation is carried out by a diverse group of bacteria, using O 2 or NO 3 as terminal electron acceptors. At circumneutral pH, both processes occur at similar rates and compete with each other. Abiotic iron reduction is catalyzed by iron-sulfur minerals or different types of organic compounds, whereas biotic iron reduction is carried out by a diverse group of microorganisms, often using chemical agents to dissolve solid iron minerals. We used iron oxidizing microbial mats to assess the potential impact of microbial activity on the deposition of banded iron formations (BIF). The mats were collected during several years from experimental tanks connected to groundwater aquifers with different Fe 2C concentrations. To separate between biotic and abiotic iron oxidation, live and killed mats were incubated with 57 Fe 2C . Separate analyses of the water and solid phase revealed that the iron oxidation and reduction rates per mL of solid matter (biomass and iron precipitates) were 0.4-73 mmol L ¡1 d ¡1 and 30-280 mmol L ¡1 d ¡1 , respectively. No significant differences in iron oxidation rates were observed between the live and killed samples. The iron reduction rates, however, were higher in the live samples in mats from 3 out of 4 environments. We suggest that in natural systems, in the presence of organic matter, biotic and abiotic iron oxidation and reduction are not separable processes. Fe 2C will be biotically and abiotically oxidized as well as bind to exposed charged groups of organic substances. Either way, this iron may serve as a nucleation matrix for further abiotic iron precipitation. The oxidized iron is then susceptible to iron reduction, which can likewise be a direct metabolic or an abiotic process. Nevertheless, it is important to note the significance of organic matter, since both the abiotic oxidation and reduction of iron are often mediated by substrates of biological origin.
FEMS Microbiology Ecology, 2009
In order to assess the importance of nitrate-dependent Fe(II) oxidation and its impact on the growth physiology of dominant Fe oxidizers, we counted these bacteria in freshwater lake sediments and studied their growth physiology. Most probable number counts of nitrate-reducing Fe(II)-oxidizing bacteria in the sediment of Lake Constance, a freshwater lake in Southern Germany, yielded about 10 5 cells mL À1 of the total heterotrophic nitrate-reducing bacteria, with about 1% (10 3 cells mL À1 ) of nitrate-reducing Fe(II) oxidizers. We investigated the growth physiology of Acidovorax sp. strain BoFeN1, a dominant nitrate-reducing mixotrophic Fe(II) oxidizer isolated from this sediment. Strain BoFeN1 uses several organic compounds (but no sugars) as substrates for nitrate reduction. It also reduces nitrite, dinitrogen monoxide, and O 2 , but cannot reduce Fe(III). Growth experiments with cultures amended either with acetate plus Fe(II) or with acetate alone demonstrated that the simultaneous oxidation of Fe(II) and acetate enhanced growth yields with acetate alone (12.5 g dry mass mol À1 acetate) by about 1.4 g dry mass mol À1 Fe(II). Also, pure cultures of Pseudomonas stutzeri and Paracoccus denitrificans strains can oxidize Fe(II) with nitrate, whereas Pseudomonas fluorescens and Thiobacillus denitrificans strains did not. Our study demonstrates that nitrate-dependent Fe(II) oxidation contributes to the energy metabolism of these bacteria, and that nitrate-dependent Fe(II) oxidation can essentially contribute to anaerobic iron cycling.
Environmental Science & Technology, 2018
Fe(II)-organic-matter (Fe(II)-OM) complexes are abundant in the environment and may play a key role for the behavior of Fe and pollutants. Mixotrophic nitrate-reducing Fe(II)-oxidizing bacteria (NRFeOx) reduce nitrate coupled to the oxidation of organic compounds and Fe(II). Fe(II) oxidation may occur enzymatically or abiotically by reaction with nitrite that forms during heterotrophic denitrification. However, it is unknown whether Fe(II)-OM complexes can be oxidized by NRFeOx. We used cellsuspension experiments with the mixotrophic nitrate-reducing Fe(II)-oxidizing bacterium Acidovorax sp. strain BoFeN1 to reveal the role of non-organically-bound Fe(II) (aqueous Fe(II)) and nitrite for the rates and extent of oxidation of Fe(II)-OM-complexes (Fe(II)-citrate, Fe(II)-EDTA, Fe(II)-humic-acid, and Fe(II)fulvic-acid). We found that Fe(II)-OM complexation inhibited microbial nitrate-reducing Fe(II) oxidation; large colloidal and negatively charged complexes showed lower oxidation rates than aqueous Fe(II). Accumulation of nitrite and fast abiotic oxidation of Fe(II)-OM complexes only happened in the presence of aqueous Fe(II) that probably interacted with (nitrite-reducing) enzymes in the periplasm causing nitrite accumulation in the periplasm and outside of the cells, whereas Fe(II)-OM complexes probably could not enter the periplasm and cause nitrite accumulation. These results suggest that Fe(II) oxidation by mixotrophic nitrate-reducers in the environment depends on Fe(II) speciation, and that aqueous Fe(II) potentially plays a critical role in regulating microbial denitrification processes.
Relative contributions of abiotic and biological factors in Fe(II) oxidation in mine drainage
Applied Geochemistry, 1999
The oxidation of Fe(II) is apparently the rate-limiting step in passive treatment of coal mine drainage. Little work has been done to determine the kinetics of oxidation in such ®eld systems, and no models of passive treatment systems explicitly consider iron oxidation kinetics. A Stella II 2 model using Fe(II) init concentration, pH, temperature, Thiobacillus ferrooxidans and O 2 concentration,¯ow rate, and pond volume is used to predict Fe(II) oxidation rates and concentrations in seventeen ponds under a wide range of conditions (pH 2.8 to 6.8 with Fe(II) concentrations of less than 240 mg L À 1 ) from 6 passive treatment facilities. The oxidation rate is modeled based on the combination of published abiotic and biological laboratory rate laws. Although many other variables have been observed to in¯uence Fe(II) oxidation rates, the 7 variables above allow ®eld systems to be modeled reasonably accurately for conditions in this study.
Thermodynamic Controls on the Kinetics of Microbial Low-pH Fe(II) Oxidation
Environmental Science & Technology, 2014
Acid mine drainage (AMD) is a major worldwide environmental threat to surface and groundwater quality. Microbial low-pH Fe(II) oxidation could be exploited for cost-effective AMD treatment; however, its use is limited because of uncertainties associated with its rate and ability to remove Fe from solution. We developed a thermodynamic-based framework to evaluate the kinetics of low-pH Fe(II) oxidation. We measured the kinetics of low-pH Fe(II) oxidation at five sites in the Appalachian Coal Basin in the US and three sites in the Iberian Pyrite Belt in Spain and found that the fastest rates of Fe(II) oxidation occurred at the sites with the lowest pH values. Thermodynamic calculations showed that the Gibbs free energy of Fe(II) oxidation (ΔG oxidation) was also most negative at the sites with the lowest pH values. We then conducted two series of microbial Fe(II) oxidation experiments in laboratory-scale chemostatic bioreactors operated through a series of pH values (2.1−4.2) and found the same relationships between Fe(II) oxidation kinetics, ΔG oxidation , and pH. Conditions that favored the fastest rates of Fe(II) oxidation coincided with higher Fe(III) solubility. The solubility of Fe(III) minerals, thus plays an important role on Fe(II) oxidation kinetics. Methods to incorporate microbial low-pH Fe(II) oxidation into active and passive AMD treatment systems are discussed in the context of these findings. This study presents a simplified model that describes the relationship between free energy and microbial kinetics and should be broadly applicable to many biogeochemical systems.