Organic carbon oxidation and suppression of methane production by microbial Fe(III) oxide reduction in vegetated and unvegetated freshwater wetland sediments

Abstract

High concentrations (20-75 pmol cm-3) of amorphous Fe(III) oxide were observed in unvegetated surface and Juncus eflusus rhizosphere sediments of a freshwater wetland in the southeastern United States. Incubation experiments demonstrated that microbial Fe(III) oxide reduction suppressed sulfate reduction and methanogenesis in surface scdimcnts and mediated 240% of depth-integrated (O-10 cm) unvegetated sediment carbon metabolism, compared to I 10% for sulfate reduction. In situ CO2 and CH, flux measurements verified that nonmethanogenic pathways accounted for -50% of unvegetated sediment carbon metabolism. Lower (-1 O-fold) rates of dark/anaerobic CH, flux from experimental vegetated cores relative to unvegetated controls suggested that methanogenesis was inhibited in the Juncus rhizosphere, in which active Fe(III) oxide reduction was indicated by the presence of low but readily detectable levels of dissolved and solid-phase Fe(II). Fe(III) oxide reduction accounted for 65% of total carbon metabolism in rhizosphere sediment incubations, compared to 22% for methanogenesis. In contrast, methanogenesis dominated carbon metabolism (72% of total) in experimental unvegetatcd sediment cores. The high Fe(III) oxide concentrations and reduction rates observed in unvegetated surface and Juncus rhizosphere sediments were perpetuated by rapid Fe(III) regeneration via oxidation of Fe(II) compounds coupled to 0, input from the overlying water and plant roots, respectively. The results indicate that Fe(III) oxide reduction could mediate a considerable amount of organic carbon oxidation and significantly suppress CH, production in freshwater wetlands situated within globally extensive iron-rich tropical and subtropical soil regimes.Natural and agricultural wetlands generate up to 50% of annual CH4 input to the atmosphere (Cicerone and Orcmland 19 8 8). Understanding factors responsible for regional variations in wetland CH4 emission is important for refining global atmospheric flux estimates, and hence assessing the current and projected contribution of CH4 to atmospheric warming (Bartlett and Harriss 1993). Recent studies indicate that a variety of factors such as wetland plant productivity (Whiting and Chanton 1993), microbial CH4 oxidation (King 1993), water table height (Freeman et al. 1993;Moore and Dalva 1993), and temperature (Bartlett and Harriss 1993) affect rates of wetland CH4 production and release. Another important factor is competition among methanogenic and other anaerobic respiratory bacteria for organic substrates in wetland sediments (Kiene 199 1). In sulfate-rich marine and brackish environments, sulfate-reducing bacteria effectively outcompete methanogens (Capone and Kiene 1988), and rates of wetland CH4 production and flux are uniformly low in such environments (Bartlett and Harriss 1993). In contrast, methanogenesis is considered to be the dominant anaerobic carbon oxidation process in sulfate-poor, orAcknowledgments

Potential for Microscale Bacterial Fe Redox Cycling at the Aerobic-Anaerobic Interface

“…Since opposing gradients of O 2 and Fe(II) are ubiquitous in nonsulfidogenic sedimentary environments (including the rhizosphere of aquatic plants, where a dynamic, microbially catalyzed Fe redox cycle is likely to exist; (Roden and Wetzel 1996;Emerson et al 1999;Frenzel, Bosse, and Janssen 1999;Weiss et al 2003), bacterial catalysis may be a widespread mechanism for Fe(II) oxidation in nature. In addition, by altering the spatial locus of Fe(III) oxide deposition in the redox transition zone (e.g.…”

“…This organism, designated strain TW2, falls within the β-subclass of the Proteobacteria with 91% 16S rRNA gene sequence identity with G. ferruginea (Sobolev and Roden 2004). The sediments in the Talladega Wetland (TW) from which strain TW2 was isolated are typical of organic-rich freshwater wetlands (Westermann 1993), characterized by steep gradients of dissolved O 2 and high concentrations of dissolved and solid-phase Fe(II) within mm of the sediment-water interface (Roden and Wetzel 1996;Sobolev and Roden 2002). It is important to acknowledge that our findings with strain TW2 may not necessarily apply to other phylogenetically and physiologically different neutrophilic FeOB, in particular the unicellular FeOB from the γ -subclass of the Proteobacteria that have been isolated from a variety of environments by Emerson and colleagues (Emerson and Moyer 1997;Emerson et al 1999;Emerson and Moyer 2002;Neubauer et al 2002;Weiss et al 2003).…”

“…Dissolved Fe(II) concentrations were likely on the order of several hundred µM in the zone of Fe(II) oxidation a few cm above the bottom layer (see Figure 5). These reaction systems mimic Fe-rich surface sediments in freshwater wetlands (e.g., Roden and Wetzel (1996)), as well as certain highly reducing groundwater environments (e.g., the landfill leachate-contaminated aquifers studied by Christensen et al 1994) in which porefluids containing 10s to 100s of micromoles of dissolved Fe(II) per L may impinge on downstream aerobic groundwaters.…”

Electron donors and acceptors influence anaerobic soil organic matter mineralization in tidal marshes

“…Nitrate data were log transformed prior to the analysis but values presented here are in the original units y . (Roden and Wetzel, 1996), the maximum rate of Fe(III) reduction previously measured at these sites (w7.5 mmol C g À1 dry soil d À1 ), and the measured dry mass:wet mass ratio for our soils (0.31 g g À1 for the Fresh soils and 0.13 g g À1 for the Brackish soils). Based on prior measurements of sulfate reduction at these two locations which showed that maximum rates were around 6 mmol C g À1 dry soil d À1 (Neubauer et al, 2005), and assuming the ratio of 1 mol of SO 4 2À reduced for every 2 mol of CO 2 , 128 mmol of SO 4 2À would provide more than enough SO 4 2À to stimulate sulfate reduction for one week.…”

Geobacter soli sp. nov., a dissimilatory Fe(III)-reducing bacterium isolated from forest soil

“…Dissimilatory Fe(III) reduction is an electron-accepting process coupled to the decomposition of organic matter in anaerobic environments (Canfield et al, 2005) and has great impacts on global biogeochemical cycles associated with nutrient availability, heavy metal toxicity, transformation of organic pollutants and greenhouse gas emission (Fredrickson & Gorby, 1996;Roden & Wetzel, 1996). Members of the genus Geobacter are often the predominant Fe(III)-reducing bacteria in subsurface anoxic environments (Lovley et al, 2004) and many species of the genus Geobacter have been isolated from hydrocarbon-contaminated environments and freshwater aquatic environments (Coates et al, 1996;Kunapuli et al, 2010;Prakash et al, 2010;Shelobolina et al, 2008;Viulu et al, 2013b).…”