Microbial anaerobic oxidation of Fe(II)-organic matter complexes

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URI: http://hdl.handle.net/10900/86421
Dokumentart: PhDThesis
Date: 2019-02-14
Language: English
Faculty: 7 Mathematisch-Naturwissenschaftliche Fakultät
Department: Geographie, Geoökologie, Geowissenschaft
Advisor: Kappler, Andreas (Prof. Dr.)
Day of Oral Examination: 2019-02-08
DDC Classifikation: 550 - Earth sciences
Keywords: Umwelt , Mikroorganismus
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The oxidation of Fe(II) to Fe(III) influences both the behavior of environmental contaminants and many other biogeochemical cycles. In anoxic environments, Fe(II) can be microbially oxidized by two different types of anaerobic Fe(II)-oxidizing bacteria. Phototrophic Fe(II)-oxidizing bacteria utilize light as an energy source and oxidize Fe(II) coupled with carbon fixation. Nitrate-reducing Fe(II)-oxidizing bacteria (NRFeOx) oxidize Fe(II) while reducing nitrate (NO3-). These two types of bacteria have been identified in a variety of habitats and are thought to play an important role in determining Fe speciation in the environment. Research on anaerobic microbial Fe(II) oxidation has been conducted for a few decades, however, most of these previous studies focused on the oxidation of either non-organically-bound, dissolved free Fe(II) or Fe(II) minerals. In natural environments, free Fe(II) and Fe(II)-containing minerals are not the only Fe(II) sources available. Fe(II) can also be complexed by organic-matter (Fe(II)-OM) in solution. However, there is still a knowledge gap when it comes to the effect of Fe(II)-OM complexation on microbial Fe(II) oxidation. To fill this knowledge gap, this thesis combined geochemical modeling and microbial incubation experiments to study microbial Fe(II) oxidation when Fe(II) was fully complexed by OM and when both free Fe(II) and Fe(II)-OM complexes were present in the medium. Using these approaches, this thesis determined the rates and extent of oxidation of Fe(II)-OM complexes by the nitrate-reducing Fe(II)-oxidizing bacteria Acidovorax sp. BoFeN1 (Chapter 3), and the phototrophic Fe(II)-oxidizing bacteria Rhodopseudomonas palustris TIE-1 and Rhodobacter ferrooxidans SW2 (Chapters 4 and 5). Moreover, this thesis has also investigated the roles of free Fe(II) and nitrite in the oxidation of Fe(II)-OM complexes (Chapter 3), has characterized the products of microbial phototrophic oxidation of Fe(II)-OM complexes (Chapter 4). Moreover, results presented in this thesis have demonstrated a new type of light-driven cryptic Fe cycle involving abiotic photochemical reduction of Fe(III)-OM complexes and microbial phototrophic Fe(II) oxidation (Chapter 5). For nitrate-reducing Fe(II)-oxidizing bacteria, Fe(II)-OM complexation inhibited the oxidation of Fe(II) by Acidovorax sp. BoFeN1. The colloidal and negatively charged Fe(II)-OM complexes showed much lower oxidation rates than free Fe(II). In addition, accumulation of nitrite and fast oxidation of Fe(II)-OM complexes only happened in the presence of free Fe(II) which probably interacted with denitrifying enzymes in the cell periplasm causing nitrite accumulation in the cell periplasm and in the solution outside the cells. Compared to free Fe(II), Fe(II)-OM complexes can probably not enter into the periplasm and cause these changes due to their differences in charge, molecular size and solubility. These results suggest that Fe(II) oxidation by mixotrophic nitrate-reducers in the environment depends on Fe(II) speciation and free Fe(II) plays a critical role in regulating microbial denitrification processes. For phototrophic Fe(II)-oxidizing bacteria, Fe(II)-OM complexation significantly accelerated the rates of Fe(II) oxidation by Rhodopseudomonas palustris TIE-1, compared to the oxidation of free Fe(II). Different types of Fe(II)-OM complexes showed different Fe(II) oxidation rates, although a fraction of the Fe(II) present as colloidal Fe(II)-OM complexes seemed to resist to microbial oxidation. In addition to Rhodopseudomonas palustris TIE-1, Fe(II)-OM complexes also accelerated Fe(II) oxidation by another phototrophic Fe(II)-oxidizing bacteria, Rhodobacter ferrooxidans SW2, but this stimulating effect was weaker and did not apply to all of the Fe(II)-OM complexes. Moreover, our results showed that Rhodobacter ferrooxidans SW2 was capable of re-oxidizing Fe(II)-citrate produced by photochemical reduction of Fe(III)-citrate, which kept the dissolved Fe(II)-citrate concentration at low and stable concentrations (<10 μM) with a concomitant increase in cell numbers. This result demonstrated the potential for active cryptic Fe-cycling in the photic zone of anoxic aquatic environments, despite low measurable Fe(II) concentrations. These results indicate that Fe-cycling in photic anoxic environment could be much more active than previously thought. Taken together, the result presented in this thesis revealed that Fe(II)-OM complexation can play an important role for the microbial oxidation of Fe(II), and microbial Fe(II) oxidation in OM rich environments may strongly depend on the metabolic type of Fe(II)-oxidizing bacteria and the speciation of Fe(II), e.g. the identity of Fe(II)-OM complexes and the existence of free Fe(II). These new findings improve our understanding of microbial Fe-cycling and highlight the importance of Fe(II)-OM complexation in many environmental processes.

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