Anaerobic methane oxidation by archaea/sulfate-reducing bacteria aggregates: 1. Thermodynamic and physical constraints

Abstract

Aggregates of archaea and sulfate-reducing bacteria (SRB) recently discovered in methane-seep sediments are widely assumed to engage in anaerobic methane oxidation (AMO), but the reaction mechanism remains poorly understood. We used a spherical diffusion-reaction model that incorporates thermodynamic controls, realistic aggregate morphology, and essential elements of cell structure to quantify maximum reaction rates and energy yields for competing mechanisms, to determine how cellular energy yields are affected by aggregate size and morphology, and to investigate the impact of organic-matter remineralization on archaea and SRB in the aggregate. The model provides the following insights: (a) syntrophic AMO is thermodynamically and physically possible for a variety of intermediate compounds (including H 2 , formate, and acetate); (b) the energy yield for syntrophic AMO is low but compatible with the maintenance needs of non- or slowly-growing cells; (c) archaea and SRB engaged in syntrophic AMO face a substantial energetic cost for aggregating; (d) direct contact between archaea and SRB provides only a modest energetic advantage compared to a loose association; and (e) sulfidogenic-methanogenic aggregates that take advantage of fermentation products released during organic-matter decay have a substantial energetic advantage over aggregates that rely exclusively on syntrophic AMO. Moreover, the model calls attention to a discrepancy between the observed sulfate-reduction rate at a well-characterized methane-seep site and the theoretical upper-limit rate of syntrophic AMO by a mechanism involving interspecies transfer of H 2 , formate, acetate, or other chemical intermediates. An analysis of possible errors, ambiguities, and artifacts in modeling and experimental techniques leads us to a surprising conclusion: that archaea/SRB aggregates in methane-seep sediments may be methanogenic rather than methanotrophic. In contrast, AMO in non-seep (diffusion-dominated) sediments is best explained by a consortium involving methanogenic archaea (that oxidize methane and release H 2 ) and hydrogenotrophic SRB.