Microbial interactions in the anaerobic oxidation of methane: model simulations constrained by process rates and activity patterns

Abstract

Summary Proposed syntrophic interactions between the archaeal and bacterial cells mediating anaerobic oxidation of methane coupled with sulfate reduction include electron transfer through (1) the exchange of H2 or small organic molecules between methane‐oxidizing archaea and sulfate‐reducing bacteria, (2) the delivery of disulfide from methane‐oxidizing archaea to bacteria for disproportionation and (3) direct interspecies electron transfer. Each of these mechanisms was implemented in a reactive transport model. The simulated activities across different arrangements of archaeal and bacterial cells and aggregate sizes were compared to empirical data for AOM rates and intra‐aggregate spatial patterns of cell‐specific anabolic activity determined by FISH‐nanoSIMS. Simulation results showed that rates for chemical diffusion by mechanism (1) were limited by the build‐up of metabolites, while mechanisms (2) and (3) yielded cell specific rates and archaeal activity distributions that were consistent with observations from single cell resolved FISH‐nanoSIMS analyses. The novel integration of both intra‐aggregate and environmental data provided powerful constraints on the model results, but the similarities in model outcomes for mechanisms (2) and (3) highlight the need for additional observational data (e.g. genomic or physiological) on electron transfer and metabolic functioning of these globally important methanotrophic consortia.

Spatially Resolved Electron Transport through Anode‐Respiring Geobacter sulfurreducens Biofilms: Controls and Constraints

“…No flux conditions were imposed at the anode surface, where Cytred was converted to Cytox at a rate set by Jc, representing the offloading of electrons to electrode. 10 -14 -10 -16 (6×10 -15 ) Cell-specific acetate consumption rate constant Estimated from [6] μ d -1 varied Cell growth rate Calculated using Eq (1) ρ gdw cell -1 9.5×10 -14 Biomass density Estimated from [115] YAc gdw mol-Ac -1 4.32 Growth yield Calculated using Eq (3)…”

Microbial and Reactive Transport Modeling Evidence for Hyporheic Flux‐Driven Cryptic Sulfur Cycling and Anaerobic Methane Oxidation in a Sulfate‐Impacted Wetland‐Stream System

“…Not only do SO ‐impacted environments have the most urgent need for clarifying the impact of S on overall wetland biogeochemistry, but they also provide the clearest test bed for examining S cycling in freshwater sediments. Previous reactive transport models have included AOM coupled to SO reduction for marine environments (see review by Regnier et al, , and He et al, ), but similar applications in freshwater ecosystems are minimal. Additionally, uncertainties about specific mechanisms and their rates have limited the incorporation of “cryptic” S cycling in any model applications.…”

Controls on Interspecies Electron Transport and Size Limitation of Anaerobically Methane-Oxidizing Microbial Consortia

“…These features suggest that DIET is the principal mechanism of sulfate-dependent AOM. While this hypothesis awaits direct experimental confirmation or indirect support through measurements that show the potential for conduction within the aggregates and is hampered by a lack of any pure cultures of microorganisms carrying out this metabolism, modeling efforts indicated that DIET can support cell-specific AOM rates and archaeal activity distributions that were consistent with observations from single-cell resolved fluorescent in situ hybridization-nanoscale secondary ion mass spectrometry (FISH-nanoSIMS) analyses (19).…”

“…Furthermore, direct interspecies extracellular electron transfer (DIET) has been observed in cocultures (10,11) and microbial aggregates (12)(13)(14)(15)(16). There is also a growing body of evidence that DIET also takes place between methanotrophic archaea and syntrophic sulfate-reducing bacteria in AOM consortia (17)(18)(19), where it serves as an effective transport mechanism over long spatial distances (17). It overcomes limitations inherent in the diffusive exchange of dissolved electron-carrying molecules (mediated interspecies electron transfer, or MIET) that lead to the build-up of reaction products and the subsequent shutdown of metabolic activity (19,20).…”