Potentiostatically Poised Electrodes Mimic Iron Oxide and Interact with Soil Microbial Communities to Alter the Biogeochemistry of Arctic Peat Soils

Abstract

Dissimilatory metal-reducing bacteria are ubiquitous in soils worldwide, possess the ability to transfer electrons outside of their cell membranes, and are capable of respiring with various metal oxides. Reduction of iron oxides is one of the more energetically favorable forms of anaerobic respiration, with a higher energy yield than both sulfate reduction and methanogenesis. As such, this process has significant implications for soil carbon balances, especially in the saturated, carbon-rich soils of the northern latitudes. However, the dynamics of these microbial processes within the context of the greater soil microbiome remain largely unstudied. Previously, we have demonstrated the capability of potentiostatically poised electrodes to mimic the redox potential of iron(III)-and humic acid-compounds and obtain a measure of metal-reducing respiration. Here, we extend this work by utilizing poised electrodes to provide an inexaustable electron acceptor for ironand humic acid-reducing microbes, and by measuring the effects on both microbial community structure and greenhouse gas emissions. The application of both nonpoised and poised graphite electrodes in peat soils stimulated methane emissions by 15%-43% compared to soils without electrodes. Poised electrodes resulted in higher (13%-24%) methane emissions than the nonpoised electrodes. The stimulation of methane emissions for both nonpoised and poised electrodes correlated with the enrichment of proteobacteria, verrucomicrobia, and bacteroidetes. Here, we demonstrate a tool for precisely manipulating OPEN ACCESSMinerals 2013, 3 319 localized redox conditions in situ (via poised electrodes) and for connecting microbial community dynamics with larger ecosystem processes. This work provides a foundation for further studies examining the role of dissimilatory metal-reducing bacteria in global biogeochemical cycles.

Methane Emission in a Specific Riparian-Zone Sediment Decreased with Bioelectrochemical Manipulation and Corresponded to the Microbial Community Dynamics

“…These BESs produce power in microbial fuel cells (MFCs; He et al, 2005 ; Fornero et al, 2010a , b ; Rosenbaum et al, 2011b ); produce chemical products in microbial electrolysis cells ( Rozendal et al, 2009 ; Villano et al, 2010 ; Cheng and Logan, 2011 ; Cusick et al, 2011 ; Rosenbaum et al, 2011a ); remediate pollutants ( Gregory and Lovley, 2005 ; Strycharz et al, 2010 ; Morris and Jin, 2012 ); sense environmental and chemical parameters ( Chang et al, 2005 ; Kumlanghan et al, 2007 ); and produce logic gates in biocomputing devices ( Li et al, 2011 ; TerAvest et al, 2011 ). In the environment, potentiostatically poised electrodes (i.e., electrodes held at a constant electrical potential using an electrical device called a potentiostat), can mimic iron(III)- and humic substance-compounds and act as the terminal electron acceptor for dissimilatory metal-reducing bacteria ( Williams et al, 2010 ; Zhang et al, 2010 ; Friedman et al, 2012 , 2013 ). The advantage of using an electrode instead of, for example, iron(III) is that the electrode can act as an inexhaustible terminal electron acceptor, which can be set precisely to the potential of interest without any other chemical interactions with the community.…”

Anaerobic Methane Oxidation in High-Arctic Alaskan Peatlands as a Significant Control on Net CH4 Fluxes

“…The anoxic basins representative of the North Slope landscape near Utqiaġvik are characterized by Fe-driven soil respiration [40,52,77]. We hypothesize that high native Fe concentrations and the importance of Fe-reduction respiration in these wetland soils favor AOM energetically linked with Fe-reduction, as has been seen in some high-Fe freshwater systems [22,24,82].…”

“…However, recent studies using 16s rRNA gene sequences in this landscape have shown the ubiquity of methanogen communities and a convergence in microbial composition within the active layer, regardless of basin age class [76]. Therefore, differences in microbial communities between age classes in this ecosystem appear to be more subtle than changes associated with soil depth and microtopography [40,71,77]. Utqiaġvik soil isolates related to methanogens capable of Fe(III)-reduction were detected [63], namely the Methanosarcina, Methanobacterium palustre, and Methanococcus clades ( Figure 2), grouping closely amongst ANME groups 2 and 3, with greater separation from the ANME group 1.…”

“…Extracellular electron transfer is a capability associated with both ANME-2 [78] and Geobacter [79] microorganisms that can reduce solid electron acceptors like metal oxides. From previous work we know Geobacter is a major contributor to ecosystem respiration from these soils [71,77]. Extracellular electron transfer is a recognized mechanism for metal-and organics-dependent AOM [80], tied functionally to ANME group 2 organisms [17,20,79].…”

“…This landscape has an abundance of alternative electron acceptors, particularly Fe and humic substances [40,51,77]. Increased thaw could therefore release more Fe (and humic substances) currently trapped in the frozen mineral layer, and warming-induced cryoturbation could redistribute minerals into the upper active layer [91].…”