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

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 We thank Trisha May for technical assistance, and R. P. Kienc and D. R. Lovley for review of an earlier version of the manuscript. This work was supported by grants DEB 92-20822 and DEB9407233 from the U.S. National Science Foundation. This paper is a contribution from the Center for Freshwater Studies, University of Alabama. ganic matter-rich freshwater sediments (Capone and Kiene 1988). Contrary to this general paradigm, however, several recent studies have shown that unidentified nonmethanogenic organic carbon oxidation pathways equal or exceed methanogenesis in a variety of freshwater wetland sediments (e.g. Kelly et al. 1990; Happell and Chanton 1993; Pulliam 1993). These findings raise the question of what nonmethanogenic pathways may be significant in freshwater wetland sediment carbon metabolism. It is well known that neither sulfate reduction nor methanogenesis predominate in anaerobic sediment metabolism until microbially reducible Fe(III) oxides are depleted, because Fe(III)-reducing bacteria are able to outcompete both sulfate-reducing and methanogenic bacteria for organic substrates (Lovley 199 1). This mechanism is analogous to that documented for the competition between sulfate-reducing and mcthanogenic bacteria. Although Fe(III) oxides are often abundant in freshwater sediments and submerged soils, and microbial Fe(III) reduction has been studied in a variety of such environments (Lovley 199 l), when compared to sulfate reduction and methanogenesis, the contribution of Fe(III) reduction to in situ anaerobic sediment metabolism has not been well documented (Westermann 1993). One difficulty in this regard is that use of a radiotracer assay for Fe(III) oxide reduction is not possible because rapid isotopic exchange occurs among sedimentary Fe(III) and Fe(II) pools (Roden and Lovley 1993). Several lake sediment studies (see Lovley 199 1) concluded that Fe(III) reduction was of minor importance for organic carbon decomposition. However, these studies considered only the formation of dissolved Fe(II),