Adsorption, desorption, and redox reactions at iron oxide nanoparticle surfaces

Abstract

Iron oxide nanoparticles are involved in several important biogeochemical processes. The interfaces between aqueous solutions and iron oxide nanoparticle surfaces are found everywhere in nature, and the chemical and microbial processes occurring at these complex interfaces control e.g. nutrient and contaminant availability and transport. Recently, it has been shown that certain ectomycorrhizal (ECM) fungi decompose dissolved organic matter (DOM) via non-enzymatic reactions involving the attack by reactive oxygen species (ROS), particularly the hydroxyl radical (•OH) generated via the Fenton reaction (Fe2+ + H2O2 → Fe3+ + •OH + OH-). Previous studies on fungal non-enzymatic DOM decomposition included soluble Fe3+ complexes that were reduced by metabolites to Fe2+ in order to initiate the Fenton reaction. However, the mechanisms of •OH formation in soil environments where solid and low-solubility iron oxide nanoparticles are the predominating iron source, are very much unknown.
This thesis focused on the reactions between ferrihydrite or goethite nanoparticles and the model metabolite 2,6- dimethoxyhydroquinone (2,6-DMHQ) or DOM modified by the ECM fungus P. involutus. These reactions were studied at different experimental conditions, primarily varying pH and the O2 level. In order to accomplish the set aims, this PhD project included batch experiments combined with conventional wet-chemical analyses as well as the Simultaneous Infrared and Potentiometric Titration (SIPT) method to monitor the reactions at the water-mineral interfaces in real-time.
The overall results showed that iron oxide nanoparticles were reductively dissolved by 2,6-DMHQ at pH 4.0 and 4.5. Under aerobic conditions these reactions produced both Fenton reagents and •OH was generated. The extent of •OH generation was sensitive to the reduction potential (EH) of the iron oxide, the O2 concentration and the competitive adsorption of organic and inorganic anions. The reactions between 2,6-DMHQ and the iron oxides at pH 7.0 and under aerobic conditions generated low amounts of •OH. At these conditions reductive dissolution was of minor importance. Instead, catalytic oxidation of 2,6-DMHQ produced H2O2 that partly was degraded by the iron oxide surfaces into •OH. Co-adsorbed anions further promoted this process,
DOM modified by P. involutus increased the reductive dissolution of iron oxides at pH 4.0 as compared to fresh DOM. Reactions between the Fe2+ produced and H2O2 generated •OH that preferentially oxidized some of the DOM components. These results suggested that modified DOM contained secondary metabolites that possibly serve both as iron reducers and antioxidants.
This thesis has provided new knowledge on the complex reaction mechanisms between iron oxide nanoparticles and redox-active organic compounds. It has increased the understanding of non-enzymatic •OH generation, and the knowledge obtained will help to understand the role of this process in organic matter decomposition. Finally, the research has identified possible mechanisms behind toxicity of iron oxide nanoparticles.

Abstract (Swedish)

Soils play a critical role in the carbon (C) cycle by regulating the atmospheric carbon dioxide (CO2) levels, and correspondingly the Earth’s climate. However, there are still countless questions of how biological and geochemical soil processes affect the C cycle. To be able to predict future implications on the Earth’s climate, we need to understand these processes. Globally, soils store more C than the terrestrial biomass and the atmosphere combined. The soil environment has an enormous impact on the soil C dynamics, whether C is captured, stored or released. Thus, depending on the soil environment, some soil organic matter (SOM) can persist for decades, while some SOM decomposes more rapidly. It has been shown that soil microbes (fungi, bacteria, archaea, etc.) play an important role in SOM decomposition into smaller molecules, ultimately, releasing CO2 to the atmosphere or playing an important role in the formation of soil aggregates, thus contributing to increased SOM stability.
Boreal and temperate forests store a large part of the terrestrial C, and in this environment ectomycorrhizal (ECM) fungi are abundant. ECM fungi form symbiotic relationships with plants i.e., plant hosts provide C as energy source for fungal growth and in return fungi transport nutrients to the plant host. A major part of soil nutrients is found in organic form, as part of SOM. Thus, to access and mobilize these nutrients, fungi are required to decompose SOM. Some ECM fungi use a degradation mechanism involving the Fenton reaction (Fe2+ + H2O2 → Fe3+ + •OH + OH-). For this mechanism to occur, the fungi need ferrous iron (Fe2+) and hydrogen peroxide (H2O2). H2O2 can be provided by fungi, however, in soils iron is primary found in oxidation state +3 and in solid state as iron oxides and other iron- containing minerals, and thereby, is not easily available. During the initial SOM decomposition, fungi produce low molecular weight organic compounds, secondary metabolites, which are not involved in sustaining fungi or the plant host growth. Some of these secondary metabolites have iron reducing capacity, which can reduce soluble ferric iron (Fe+3) salts, thus making Fe2+ more accessible. However, there is limited knowledge on how these secondary metabolites interact with and possibly reduce solid iron oxides.
In this thesis, common boreal and temperate forest soil iron oxides, ferrihydrite and goethite, were used to investigate whether Fenton reactions can be initiated by organic reductants, similar to fungal secondary metabolites or as part of dissolved organic matter (DOM), under different geochemical conditions. The aims of this
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PhD project were achieved by studying adsorption, desorption, and redox reactions between the iron oxide nanoparticles and these organic reductants. This research seeks to answer the question of whether some of these reactions can promote the generation of hydroxyl radicals (•OH) via Fenton reaction. Increased understanding of these mechanisms can improve our understanding of the stability of SOM and SOM-mineral aggregates.
Results obtained at pH 4.5 and 4.0 showed that a model compound (2,6-DMHQ), which is similar to a compound secreted by brown rot wood decay fungi, was able to reductively dissolve iron oxide nanoparticles and produce H2O2 under aerobic reaction conditions. Thus, reactions between 2,6-DMHQ and iron oxides allow the formation of both reactants to initiate the Fenton reaction. In anaerobic environments, due to a lack of oxygen (O2), the formation of H2O2 was negligible from reactions between 2,6-DMHQ and iron oxides, thus suppressing the Fenton reaction. Moreover, results showed that initiation of the Fenton reaction was not only affected by O2 concentrations, but also by different geochemical factors, such as pH, redox potentials and adsorption of organic and inorganic molecules.
Soils contain a wide range of inorganic and organic molecules that can adsorb on iron oxides, thus interfering with redox reactions at iron oxide surfaces. Results showed that 2,6-DMHQ was able to compete with inorganic and organic molecules for surface iron and to initiate the Fenton reaction. Moreover, adsorption of organic and inorganic molecules in some cases promoted the Fenton reaction to occur close to iron oxide nanoparticle surfaces. These surface reactions can have a considerable impact on adsorbed SOM decomposition and the provision of nutrients to plant hosts. At the same time, more extensive SOM decomposition can result in a greater CO2 release.
At neutral pH values, various organic pollutants, with molecular structures similar to 2,6-DMHQ, are found in groundwater and agricultural soils due to pesticide and fertilizer use. Injection of H2O2 into the soil or aquatic systems is a widely-applied technique to degrade these pollutants. Results at pH 7.0 showed that adsorption of inorganic and organic molecules on iron oxides resulted in a higher yield of the Fenton reaction from the 2,6-DMHQ-iron oxide interactions. Therefore, naturally occurring processes between iron oxides and 2,6-DMHQ-like molecules can help to increase organic contaminant degradation, for example, when the commonly added plant nutrient, phosphate, is adsorbed on iron oxide surfaces.
DOM modified by the ECM fungus Paxillus involutus, which contained secondary metabolites, has a higher affinity towards iron oxide surfaces than the initial DOM. This is in agreement with the hypothesis that organic matter decomposition can contribute to SOM stability. Results showed that modified DOM reductively dissolved ferrihydrite and goethite, but in order to initiate the Fenton reaction the addition of H2O2 was required. Further, results suggested that in the absence of
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H2O2, some Fe2+ was complexed to adsorbed DOM. When H2O2 was added the Fenton reaction occurred in close vicinity to the organic matter, which resulted in direct oxidation of DOM components. Moreover, experiments with DOM modified by P. involutus suggested that the produced secondary metabolites might act as antioxidants. Thus, these metabolites may inhibit the oxidation of other DOM components, thereby increasing the partial recalcitrance of DOM.
In summary, the results obtained in this PhD project suggested that in aerobic soil environments and in the presence of iron oxide nanoparticles, fungal secondary metabolites with molecule structures similar to 2,6-DMHQ might initiate the Fenton reaction and produce •OH. Yet, further studies are required to understand if and how these reactions affects the stability of the soil C. Moreover, the generation of •OH at iron oxide nanoparticles surfaces can be harmful and cause damage to organisms exposed to these nanoparticles. Thus, the reactions characterized in this study can be related to the potential toxicity of iron oxide nanoparticles.

• author: Krumina, Lelde
• supervisor: Per Persson; Anders Tunlid
• opponent: Dr. Müller, Katharina, Helmholtz-Zentrum Dresden-Rossendorf (HZDR), Institute of Resource Ecology, Dresden, Germany
• organization: Centre for Environmental and Climate Science (CEC); MEMEG; BECC: Biodiversity and Ecosystem services in a Changing Climate
• publishing date: 2017-12
• type: Thesis
• publication status: published
• subject: Natural Sciences
• keywords: Ferrihydrite, Goethite, Secondary metabolites, Reductive dissolution, Catalytic oxidation, hydroxyl radicals, Fenton reaction, SOM decomposition
• pages: 216 pages
• defense location: Lecture hall “Blå hallen”, Ecology building, Sölvegatan 37, Lund
• defense date: 2018-01-25 10:00:00
• ISBN: 978-91-7753-504-1
• ISBN: 978-91-7753-503-4
• language: English
• LU publication?: yes
• id: 47acae4d-de14-441c-9988-504d86b4429b
• date added to LUP: 2017-12-19 20:01:18
• date last changed: 2020-09-25 14:41:52