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Humic substances as fully regenerable electron acceptors in recurrently anoxic environments


Humic substances form through the degradation of microbial and plant precursors, and make up a significant fraction of natural organic matter in terrestrial and aquatic environments1. Humic substances are redox-active2,3,4 and can act as terminal electron acceptors in anaerobic microbial respiration4. Reduced humic substances may become re-oxidized during aeration of temporarily anoxic systems, such as wetlands, sediments and many soils. If the transfer of electrons from anaerobic respiration through humic substances to oxygen is sustained over many redox cycles, it may competitively suppress electron transfer to carbon dioxide, and thereby lower the formation of methane in temporarily anoxic systems5,6,7,8. Here, we monitor changes in the redox states of four chemically distinct dissolved humic substances over successive cycles of reduction by the bacterium Shewanella oneidensis MR-1 and oxidation by oxygen, in a series of laboratory experiments. We show that electron transfer to and from these substances is fully reversible and sustainable over successive redox cycles. We suggest that redox cycling of humic substances may largely suppress methane production in temporarily anoxic systems.

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Figure 1: Redox cycling of HS in temporarily anoxic systems.
Figure 2: Redox states of inoculated and sterile HAs during successive anoxic and oxic incubations.
Figure 3: Thermodynamic analyses of microbial HA reduction.
Figure 4: Reduction potential ranges of aerobic and anaerobic microbial respiration using different TEAs, including HS.

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This research was financially supported by grants from the Swiss National Science Foundation to M.S. and L.K. (Project 200021–135515) and from the German Research Foundation to A.K. and A.P. (KA 1736/3-2, research group eTrap). We thank M. Aeschbacher, S. E. Page, J. Keller, K-H. Knorr, C. A. Gorski, K. Wammer and K. McNeill for discussions.

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The concept of redox cycling of HAs was developed by A.P., A.K., L.K. and M.S. M.S. and A.K. coordinated the overall project. L.K. and M.S. conducted redox cycling and electrochemical analyses of HA and model compounds, analysed the data, and wrote the paper. A.P. and A.K. prepared the HA and model compound solutions and the S. oneidensis MR-1 inocula, and contributed to writing the paper.

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Correspondence to Andreas Kappler or Michael Sander.

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The authors declare no competing financial interests.

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Klüpfel, L., Piepenbrock, A., Kappler, A. et al. Humic substances as fully regenerable electron acceptors in recurrently anoxic environments. Nature Geosci 7, 195–200 (2014).

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