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Biological Sciences Division
Research Highlights

May 2013

New Facet of Extracellular Electron Transfer Found

Biofilms move electrons long distances across two distinct layers, even under starving conditions

Biofilm images
Biofilms move electrons surprisingly long distances across two distinct layers, as illustrated in the transmission electron microscopy images of a Geobacter biofilm incubated with uranium above. Top: Metabolically active, upper biofilm layer with precipitates of reduced uranium associated with healthy bacterial membranes. Bottom: Metabolically inactive, lower biofilm layer with plasmolyzed cells and relatively low mineral precipitation.

Results: Bacteria can move electrons at least half a millimeter across a scaffolding made by themselves, of themselves, even under starving conditions; that is, when cells at the bottom of the bacterium biofilm do not have access to their electron donor and carbon source. This new finding by a scientific team from Pacific Northwest National Laboratory, Washington State University, and Argonne National Laboratory challenges conventional wisdom, which held that electrical resistance within bacterial biofilms-robust structures held together by a strong matrix-would restrict long-range electron transfer.

At the center of this study is Geobacter sulfurreducens, a biofilm-forming, metal-reducing bacterium. Like other metal-reducing bacteria, Geobacter give away their electrons as part of a series of electron exchanges that drives energy, or ATP, production.

Why It Matters: Although a significant amount of research has been performed to understand electron transfer mechanisms in biofilms respiring on electrodes, scientists do not currently know how electron donor concentration and biofilm structure relate to respiration rates. Understanding bacteria-metal electron exchange is important because it provides insight into how metals behave in their environment and how electrons might be captured to produce electricity.

Methods: The research team employed a novel electrochemical-nuclear magnetic resonance (EC-NMR) microimaging system, which allows biofilms to grow inside an NMR magnet. EC-NMR, designed and built by staff and users at EMSL, a national user facility located at PNNL, makes it possible for the first time to conduct simultaneous electrochemical and NMR studies on biofilms, revealing details about metabolic activity, structure, porosity, nutrient movement, and nutrient concentrations in multiple dimensions.

Coupling EC-NMR with X-ray absorption spectroscopy to measure the transfer of electrons to a uranium probe for validation, the team showed that the Geobacter biofilms contained a top layer of metabolically active bacteria sitting on an inactive layer. Surprisingly, the inactive layer serves as an extension of the electrode, providing a bioscaffold that allows electrons to flow from the biofilm top to the electrode surface on which the biofilm grew.

What's Next: This new finding will influence the design of bioelectrochemical systems, such as for producing hydrogen or for enhancing methods to treat wastewater while simultaneously generating electricity. It will also improve predictive models that describe electron transfer and provide a more rounded understanding of the behavior and role of biofilms in the environment.

Acknowledgments:

Sponsors: This study was supported by the U.S. Office of Naval Research as well as the U.S. Department of Energy's Office of Biological and Environmental Research (BER) as part of BER's Subsurface Biogeochemistry Research Program. The latter contribution stems, in part, from the Subsurface Biogeochemical Research (SBR) Scientific Focus Area (SFA) at PNNL; in addition, some study participants were given support by SBR's ANL SFA project. Development of the custom-built NMR microscopy and biofilm reactor hardware was supported by the National Institutes of Health. A portion of this research was performed using resources at EMSL, a BER-supported national scientific user facility. Use of the Advanced Photon Source was supported by the DOE-SC Office of Basic Energy Sciences.

User Facilities: EMSL, Advanced Photon Source

Research Team: Ryan Renslow, Jerome Babauta, and Haluk Beyenal, WSU; Alice Dohnalkova, Paul Majors, and Jim Fredrickson, PNNL; and MI Boyanov and Ken Kemner, ANL.

Research Area: Subsurface Science 

Reference: Renslow RS, JT Babauta, A Dohnalkova, MI Boyanov, KM Kemner, PD Majors, JK Fredrickson, and H Beyenal. 2013. "Metabolic spatial variability in electrode-respiring Geobacter sulfurreducens biofilms." Energy and Environmental Science 6(6):1827-1836. DOI: 10.1039/C3EE40203G.


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