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Extracellular electron transfer through microbial reduction of solid-phase humic substances

Nature Geoscience volume 3, pages 417–421 (2010)Cite this article

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Abstract

The decay of soil and sedimentary organic matter yieldsorganic compounds with a high molecular weight, termed humic substances1. Microorganisms can transfer electrons to dissolved humic substances2, and reduced humic substances can rapidly reduce iron(III) oxides3. Thus, dissolved humic substances can serve as electron shuttles that promote iron(III) oxide reduction in sediments2,4. However, most humic substances in soils and sediments are in particulate, rather than dissolved, form1; the ability of microorganisms to reduce solid-phase humics and their capacity to shuttle electrons is thus far unknown. Here we show through incubation experiments and electron spin resonance measurements that iron(III)-oxide-reducing bacteria can transfer electrons to solid-phase humic substances in sediments sampled from wetlands. Although the electron-accepting capacity of the solid-phase humics was modest, solid-phase humics significantly accelerated iron(III) oxide reduction, by shuttling electrons from bacteria to oxide surfaces. Microbial solid-phase humics reduction represents a new mechanism for extracellular electron transfer that can facilitate reduction of iron(III) oxide and other redox reactions in sediments and soils.

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Figure 1: Microbial and chemical reduction of Fe-stripped Talladega Wetland surface sediment.
Figure 2: ESR spectra of reduced and non-reduced Fe-stripped Talladega Wetland surface sediment.
Figure 3: Microbial reduction of synthetic Fe(III) am by FeRB in the presence and absence of freeze-dried Talladega Wetland surface sediment.
Figure 4: TEM analysis of Fe(III) am/Fe-stripped Talladega Wetland sediment mixture.

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Acknowledgements

This research was financially supported by grants from the US Department of Energy (Office of Biological and Environmental Research) and the US National Science Foundation (Directorates for Biological Sciences and Geosciences) to E.E.R.; by an IPSWaT fellowship from the German Federal Ministry for Science and Education to J.J.; by financial support from the German Research Foundation to A.K. and A.P. and financial support from the Stifterverband der Wissenschaft to A.K. We thank G. Scott, B. Golson and B. Kollah for technical assistance, and the late R. G. Wetzel for fruitful early discussions of microbial humics transformation. This letter is dedicated to the memory of R. G. Wetzel.

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Authors and Affiliations

  1. Department of Geoscience, University of Wisconsin-Madison, 1215 W. Dayton St., Madison, Wisconsin 53706, USA

    Eric E. Roden, Hiromi Konishi & Huifang Xu

  2. Geomicrobiology, Center for Applied Geoscience, Eberhard-Karls-University of Tuebingen, Sigwartstrasse 10, 72076 Tuebingen, Germany

    Andreas Kappler, Iris Bauer & Jie Jiang

  3. Division I.4 Process Analytical Technology, BAM Federal Institute of Materials Research and Testing, Richard-Willstaetter-Str. 11, 12489 Berlin, Germany

    Andrea Paul

  4. Department of Chemistry, Humboldt University Berlin, Unter den Linden 6, 10099 Berlin, Germany

    Reinhard Stoesser

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  1. Eric E. Roden
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Contributions

The concept of HSsolid reduction was developed together by E.E.R. and A.K. E.E.R. coordinated the overall project, conducted or directed microbial and chemical reduction assays, analysed data and wrote the paper. A.K. directed the S. oneidensis reduction assays, coordinated with A.P. and R.S. on the ESR analyses and wrote the paper. I.B. and J.J. conducted the S. oneidensis microbial reduction assays, and I.B. helped to coordinate the ESR analyses. A.P. and R.S. conducted and interpreted the ESR analyses; H.K. and H.X. conducted and interpreted the TEM analyses.

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Correspondence to Eric E. Roden.

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Roden, E., Kappler, A., Bauer, I. et al. Extracellular electron transfer through microbial reduction of solid-phase humic substances. Nature Geosci 3, 417–421 (2010). https://doi.org/10.1038/ngeo870

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