Magnetite Nanoparticles as Metastable Biogeobatteries in Consecutive Redox Cycles

Iron (Fe) is one of the most abundant elements on Earth, widely present in soils and sediments, and participates in global carbon, nitrogen, and oxygen cycles. The redox reactions of iron play a crucial role in biogeochemical cycles, particularly in the processes of iron oxidation and reduction. Iron minerals, especially mixed-valent iron minerals such as magnetite, can influence the migration and transformation of nutrients and contaminants in the environment due to their high surface area and redox activity. Recent studies have found that magnetite nanoparticles (MNPs) can serve as electron donors and acceptors for microorganisms, acting as “biogeobatteries” that store and release electrons in microbial-driven redox cycles. However, the stability of magnetite nanoparticles in consecutive redox cycles and their impact on mineral integrity and properties remain unclear.

This study aims to explore the feasibility of magnetite nanoparticles as biogeobatteries in consecutive redox cycles and investigate changes in their mineral properties and their effects on environmental contaminants and nutrients. Through microbial-driven redox cycling experiments, the authors revealed the dissolution and recrystallization of magnetite nanoparticles during long-term redox processes and the impact of these processes on iron-metabolizing microorganisms in the environment.

Source of the Paper

This paper was co-authored by Timm Bayer, Natalia Jakus, Andreas Kappler, and James M. Byrne, affiliated with the University of Tübingen in Germany, the École Polytechnique Fédérale de Lausanne in Switzerland, and the University of Bristol in the UK, respectively. The paper was published on May 7, 2024, in the journal Geo-Bio Interfaces, titled Magnetite Nanoparticles are Metastable Biogeobatteries in Consecutive Redox Cycles Driven by Microbial Fe Oxidation and Reduction.

Research Process

1. Synthesis of Magnetite Nanoparticles

The study first synthesized magnetite nanoparticles using a modified Pearce method. The specific steps involved mixing an Fe solution with an NH4OH solution under anoxic conditions to generate magnetite particles. The synthesized magnetite was washed multiple times and then suspended in a pH 7 bicarbonate buffer.

2. Microbial Cultivation

Two microorganisms were used: the nitrate-reducing iron-oxidizing culture KS and the iron-reducing bacterium Geobacter sulfurreducens. The KS culture was cultivated for 7 days in a medium containing nitrate, while G. sulfurreducens was cultivated for 5 days in a medium containing acetate. After cultivation, the cultures were pooled and used for subsequent experiments.

3. Experimental Design

The experiment was conducted in large-volume (1 L) and small-volume (50 mL) reaction bottles, each containing a bicarbonate buffer, magnetite nanoparticles, and nitrate. The KS culture was added to the reaction bottles, while the control group received an equal volume of buffer. The reaction bottles were sealed under anoxic conditions and sampled periodically for geochemical and mineralogical analysis.

4. Redox Cycling

Two complete redox cycles were conducted, each consisting of an oxidation phase driven by the KS culture and a reduction phase driven by G. sulfurreducens. At the end of each redox phase, the magnetite nanoparticles were washed to remove microorganisms, and new medium and microorganisms were added for the next cycle.

5. Geochemical Analysis

Samples were collected periodically during the experiment, centrifuged to separate the supernatant and pellet. The pellet was dissolved in sulfuric acid, and the supernatant was used to measure dissolved iron, nitrate, and acetate concentrations. Total iron concentration and the Fe(II)/Fe(III) ratio were determined using the Ferrozine assay.

6. Magnetic Susceptibility Measurements

A KLY-3 kappabridge was used to measure changes in the magnetic susceptibility of magnetite nanoparticles in the reaction bottles to assess magnetic changes during the redox processes.

7. Mineralogical Analysis

Mössbauer spectroscopy, X-ray diffraction (XRD), scanning electron microscopy (SEM), and Fourier-transform infrared spectroscopy (FTIR) were used to analyze changes in the mineral composition and morphology of magnetite nanoparticles after different redox phases.

Key Findings

1. Redox Cycling of Magnetite Nanoparticles

The experimental results showed that magnetite nanoparticles successfully functioned as biogeobatteries in two consecutive redox cycles. During the oxidation phase driven by the KS culture, the Fe(II)/Fe(III) ratio decreased from an initial 0.43 to 0.29, indicating that the KS culture successfully oxidized Fe(II) in the magnetite nanoparticles. During the reduction phase driven by G. sulfurreducens, the Fe(II)/Fe(III) ratio increased from 0.29 to 0.75, indicating that G. sulfurreducens successfully reduced Fe(III) in the magnetite nanoparticles.

2. Magnetic Changes

Magnetic susceptibility measurements showed that the magnetic susceptibility of magnetite nanoparticles decreased during the oxidation phase and increased during the reduction phase. The change in magnetic susceptibility during the second oxidation phase (-8.7%) was greater than that during the first oxidation phase (-3.9%), indicating that reduced magnetite nanoparticles were more easily oxidized.

3. Mineralogical Analysis

Mössbauer spectroscopy and XRD analysis revealed that during the reduction phase, magnetite nanoparticles partially dissolved and recrystallized into the Fe(II) mineral vivianite. SEM images further confirmed the formation of vivianite and showed close contact between magnetite nanoparticles and vivianite.

4. Impact of Long-Term Redox Cycling

The study found that the stability of magnetite nanoparticles gradually decreased with consecutive redox cycles, with some magnetite nanoparticles dissolving and transforming into vivianite. This suggests that long-term redox cycling leads to the consumption of magnetite nanoparticles, thereby affecting their biogeochemical functions in the environment.

Conclusion

This study is the first to reveal the feasibility of magnetite nanoparticles as biogeobatteries in consecutive redox cycles and demonstrate their dissolution and recrystallization during microbial-driven redox processes. The results indicate that magnetite nanoparticles can serve as electron donors and acceptors for iron-metabolizing microorganisms in the environment, but their long-term stability is significantly affected by redox cycling. This finding has important implications for understanding the dynamic processes of iron cycling in the environment and the application of magnetite nanoparticles in contaminant remediation and nutrient migration.

Research Highlights

1. First systematic study on the stability of magnetite nanoparticles in consecutive redox cycles: Long-term experiments revealed the dissolution and recrystallization of magnetite nanoparticles during microbial-driven redox cycles.
2. Revealed the potential of magnetite nanoparticles as biogeobatteries: The study found that magnetite nanoparticles can serve as electron donors and acceptors for microorganisms, but their long-term stability is significantly affected by redox cycling.
3. Discovered the formation of vivianite: Mineralogical analysis confirmed that magnetite nanoparticles partially dissolved and recrystallized into vivianite during the reduction phase, providing important insights into the transformation of iron minerals in the environment.

Research Value

This study not only deepens our understanding of the role of magnetite nanoparticles in biogeochemical cycles but also provides new insights into their application in environmental remediation and contaminant treatment. The results indicate that magnetite nanoparticles gradually dissolve during long-term redox cycling, suggesting that their long-term stability and environmental impact must be considered in practical applications.