Pathways of anaerobic carbon cycling across an ombrotrophic–minerotrophic peatland gradient

Peatland soils represent globally significant stores of carbon, and understanding carbon cycling pathways in these ecosystems has important implications for global climate change. We measured aceticlastic and autotrophic methanogenesis, sulfate reduction, denitrification, and iron reduction in a bog, an intermediate fen, and a rich fen in the Upper Peninsula of Michigan for one growing season. In 3-d anaerobic incubations of slurried peat, denitrification and iron reduction were minor components of anaerobic carbon mineralization. Experiments using 14C-labeled methanogenic substrates showed that methanogenesis in these peatlands was primarily through the aceticlastic pathway, except early in the growing season in more ombrotrophic peatlands, where the autotrophic pathway was dominant or codominant. Overall, methane production was responsible for 3–70% of anaerobic carbon mineralization. Sulfate reduction accounted for 0–26% of anaerobic carbon mineralization, suggesting a rapid turnover of a very small sulfate pool. A large percentage of anaerobic carbon mineralization (from 29% to 85%) was unexplained by any measured process, which could have resulted from fermentation or possibly from the use of organic molecules (e.g., humic acids) as alternative electron acceptors. Peatland soils contain an estimated 462 3 1015 g of carbon worldwide, approximately one-third of the terrestrial soil carbon pool (Maltby and Immirzi 1993). Much of this soil carbon exists below the water table, where it is subject to anaerobic microbial decomposition, which generates carbon dioxide (CO2) and methane (CH4) as end products. Both CO2 and CH4 are important greenhouse gases and combined are responsible for ,80% of the radiative forcing from all greenhouse gases (Ramaswamy et al. 2001). Although they occupy ,3% of the terrestrial land surface (Bridgham et al. 2001), peatlands are currently responsible for approximately 8% of the global CH4 flux (Bartlett and Harriss 1993). If future global change increases the release of CO2 and/or CH4 from peatlands to the atmosphere, it could accelerate ongoing climate change associated with these greenhouse gases (Bridgham et al. 1995; Gorham 1995). Under anaerobic conditions, the decomposition of organic carbon to CO2 and CH4 is carried out by a consortium of microbes. Complex organic polymers are initially degraded by fermenting bacteria to yield a few simple products, which are subsequently used by methanogens to produce CH4. In freshwater wetlands, the dominant methanogenic substrates are thought to be dihydrogen (H2) and CO2, which are used by autotrophic methanogens, and acetate, which is converted to CH4 and CO2 by aceticlastic methanogens (Conrad 1989). Methanogens compete for substrates generated by upstream fermentation (i.e., acetate and H2) with microbial processes that couple the decomposition of organic matter with the reduction of alternative inorganic electron acceptors and generate CO2 as a respiratory byproduct [i.e., denitrification, manganese [Mn(IV)] reduction, iron [Fe(III)] reduction, and sulfate reduction]. From a thermodynamic perspective, these electron acceptors should be used in a predictable sequence defined by their energetic yields [in order of decreasing yield: nitrate, Mn(IV), Fe(III), and sulfate], with CH4 production occurring only after these alternative inorganic electron acceptors have been depleted (Conrad 1989). However, heterogeneity in many wetland ecosystems enables these processes to occur simultaneously (Wieder et al. 1990; Yavitt and Lang 1990; Vile et al. 2003a), with the relative contribution of these mineralization pathways ultimately determining the amount of CO2 and CH4 produced anaerobically. Given the much greater global warming potential of CH4 as compared to CO2 on a mass basis (Ramaswamy et al. 2001), the ratio at which these gases are produced during anaerobic respiration in wetlands is of critical importance. A number of environmental controls over microbial respiration have been well studied in wetlands (reviewed by Segers 1998). For example, the importance of watertable level, temperature, pH, soil carbon quality, and nutrients in 1 To whom correspondence should be addressed. Present address: Smithsonian Environmental Research Center, P.O. Box 28, Edgewater, Maryland 21037-0028 ([email protected]).