Field and laboratory studies of methane oxidation in an anoxic marine sediment: Evidence for a methanogen‐sulfate reducer consortium

Abstract

Field and laboratory studies of anoxic sediments from Cape Lookout Bight, North Carolina, suggest that anaerobic methane oxidation is mediated by a consortium of methanogenic and sulfate‐reducing bacteria. A seasonal survey of methane oxidation and CO2 reduction rates indicates that methane production was confined to sulfate‐depleted sediments at all times of year, while methane oxidation occurred in two modes. In the summer, methane oxidation was confined to sulfate‐depleted sediments and occurred at rates lower than those of CO2 reduction. In the winter, net methane oxidation occurred in an interval at the base of the sulfate‐containing zone. Sediment incubation experiments suggest both methanogens and sulfate reducers were responsible for the observed methane oxidation. In one incubation experiment both modes of oxidation were partially inhibited by 2‐bromoethanesulfonic acid (a specific inhibitor of methanogens). This evidence, along with the apparent confinement of methane oxidation to sulfate‐depleted sediments in the summer, indicates that methanogenic bacteria are involved in methane oxidation. In a second incubation experiment, net methane oxidation was induced by adding sulfate to homogenized methanogenic sediments, suggesting that sulfate reducers also play a role in the process. We hypothesize that methanogens oxidize methane and produce hydrogen via a reversal of CO2 reduction. The hydrogen is efficiently removed and maintained at low concentrations by sulfate reducers. Pore water H2 concentrations in the sediment incubation experiments (while net methane oxidation was occurring) were low enough that methanogenic bacteria could derive sufficient energy for growth from the oxidation of methane. The methanogen‐sulfate reducer consortium is consistent not only with the results of this study, but may also be a feasible mechanism for previously documented anaerobic methane oxidation in both freshwater and marine environments.

Hydrogen production by methanogens under low-hydrogen conditions

“…Given the transient nature of H 2 production, the lack of CH 4 oxidation during H 2 production, and the lack of sensitivity of H 2 production to the CH 4 level, it appears that none of the organisms studied are able to oxidize methane under these experimental conditions. While this does not disprove the hypothesis presented by Hoehler et al (1994), it does indicate that reverse methanogenesis is not a general feature of methanogens that is brought about by low H 2 levels.…”

“…3, are unlikely to support some of the observed H 2 partial pressures. The free-energy changes (∆G′) calculated for reverse methanogenesis (Hoehler et al 1994) for each experiment shown in Fig. 3 (at the maximum observed H 2 ) are: -5 kJ (mol CH 4 ) -1 , +15 kJ (mol CH 4 ) -1 , and -24 kJ (mol CH 4 ) -1 for Methanothermobacter marburgensis, Methanosarcina barkeri, and Methanosaeta thermophila, respectively.…”

“…Polysulfides (0.5 ml, 1 M) were added as indicated tium of archaea and sulfate-reducing bacteria (Boetius et al 2000;Elvert et al 1999;Hinrichs et al 1999;Hinrichs et al 2000;Hoehler and Alperin 1996;Hoehler et al 1994;Pancost et al 2000;Thiel et al 1999;. Hoehler et al (1994) outlined a consortium hypothesis to explain anaerobic methane oxidation, in which they postulated that methanogens operate in reverse to consume methane and produce H 2 when ambient H 2 is held low by sulfate-reducing bacteria. The levels of H 2 and methane achieved in much of this study were sufficient to allow reverse methanogenesis to proceed with energy conservation, though methane oxidation was never observed.…”

“…Several methanogens can use non-competitive substrates such as methylamines that may sustain growth even in environments where sulfate reducers scavenge H 2 and acetate (Oremland and Polcin 1982). It has also been proposed that methanogens are capable of reversing their metabolism under low H 2 (i.e., sulfate-reducing conditions) to convert CH 4 to CO 2 and H 2 syntrophically, a process referred to as reverse methanogenesis (Hoehler et al 1994). …”

Archaeal lipids in Mediterranean cold seeps: molecular proxies for anaerobic methane oxidation

“…However, it is unclear whether this has always been true or if this process can be disrupted by future climate change, and thus, it is important to understand the mechanism of anaerobic methane oxidation. However, the inability to culture anaerobic methane-oxidizing organisms combined with the apparently low energy yield of this reaction (Hoehler et al, 1994) has prevented previous workers from successfully identifying the responsible organisms.…”