Natural organic matter (NOM) electron shuttling stimulates microbial Fe(III)-mineral reduction at centimeter-scales

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Dokumentart: PhDThesis
Date: 2020-12-02
Language: English
Faculty: 7 Mathematisch-Naturwissenschaftliche Fakultät
Department: Geographie, Geoökologie, Geowissenschaft
Advisor: Kappler, Andreas (Prof. Dr.)
Day of Oral Examination: 2020-07-07
DDC Classifikation: 333.7 - Natural resources and energy
Keywords: Eisenmineralien
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Iron (Fe)(III) minerals are an important terminal electron acceptor for microbial respiration under anoxic conditions. However, under neutral pH conditions, Fe(III) minerals have very low solubility and are mostly present as solid (oxyhydr)oxide. This imposes a limitation on the rate and extent of electron transfer between microbes and Fe(III) minerals. Therefore, microbes have developed several strategies to enable extracellular electron transfer. One of the most important strategies is to use the natural organic matter (NOM) as electron shuttles. NOM represents the complex of organic compounds that are derived from the decay of plant and animal matters in natural systems. Due to the presence of functional groups such as quinone and hydroquinone, NOM can undergo redox cycles and act as electron shuttles between spatially separated microbes and Fe(III) minerals. Although many previous studies have shown the stimulatory effects of NOM on the microbial Fe(III)-mineral reduction as electron shuttles, it remains unknown whether such a NOM electron shuttling process can happen over long (centimeter (cm)) distance. Moreover, the mechanism of NOM electron shuttling is still unclear, i.e., if the electron shuttling process is driven by the diffusion of the NOM or the “hop” of electrons between NOM molecules. Finally, previous studies used chemically extracted humic substances (HS) as a proxy for NOM. It is, however, unknown to which extent this chemical extraction method alters the redox properties of the HS. In Chapter 3 of this thesis, we extracted NOM from a forest soil (thus referred to as soil organic matter (SOM)) at neutral pH using water, and subsequently isolated HS chemically from the water-extracted SOM using sodium hydroxide (NaOH) at pH 12. Our results showed that, under anoxic extraction conditions, the HS extracted chemically from the water-extractable SOM had a 3-times higher electron exchange capacity (EEC) than the water-extracted SOM itself. With higher EEC, the HS also showed more stimulation effects (i.e., higher reduction rate and extent) on the microbial Fe(III)-mineral reduction as electron shuttles than the water-extracted SOM. Therefore, we suggest future studies to carefully consider the influence of the chemical extraction on the redox properties of HS when using HS to represent NOM in laboratory studies. In studies presented in Chapter 4 and Chapter 5, we developed a novel agar-solidified setup that separates the Fe(III)-reducing bacteria (Shewanella oneidensis MR-1 or Geobacter sulfurreducens) and Fe(III) minerals (ferrihydrite or goethite) over 2 cm distance, with either anthraquinone-2,6-disulfonate (AQDS) or NOM as electron shuttles. Fe concentration measurements coupled to a diffusion-reaction model clearly indicated Fe(III)-mineral reduction in the presence of AQDS or NOM as electron shuttles over 2 cm distance, independent of the type of the Fe(III)-reducing bacteria. Moreover, a linear correlation between the heterogeneous electron transfer rate constant and the diffusion coefficient of AQDS was obtained from the cyclic voltammogram of AQDS. This linear correlation is in good agreement with the “diffusion-electron hopping” model proposed in previous studies, indicating that the electron transfer via AQDS was accomplished by a combination of diffusion and electron hopping between AQDS molecules. Since AQDS is commonly used as the analogue for quinone and hydroquinone functional groups in NOM, we postulate that electron hopping also plays a crucial role to facilitate the electron transfer via NOM molecules over cm distance. Overall, studies in this thesis showed that, microbial Fe(III)-mineral reduction can happen at cm-scales with NOM as electron shuttles, and the long-distance electron shuttling is achieved by a combination of NOM diffusion and electron hopping between NOM molecules. These findings improved our understanding of the feasibility and mechanism of microbial Fe(III)-mineral reduction at cm-scales with NOM as electron shuttles in the environment.

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