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

Abstract

About 382 Tg yr−1 of methane rising through the seafloor is oxidized anaerobically (W. S. Reeburgh, Chem Rev 107:486–513, 2007, https://doi.org/10.1021/cr050362v), preventing it from reaching the atmosphere, where it acts as a strong greenhouse gas. Microbial consortia composed of anaerobic methanotrophic archaea and sulfate-reducing bacteria couple the oxidation of methane to the reduction of sulfate under anaerobic conditions via a syntrophic process. Recent experimental studies and modeling efforts indicate that direct interspecies electron transfer (DIET) is involved in this syntrophy. Here, we explore a fluorescent in situ hybridization-nanoscale secondary ion mass spectrometry data set of large, segregated anaerobic oxidation of methane (AOM) consortia that reveal a decline in metabolic activity away from the archaeal-bacterial interface and use a process-based model to identify the physiological controls on rates of AOM. Simulations reproducing the observational data reveal that ohmic resistance and activation loss are the two main factors causing the declining metabolic activity, where activation loss dominated at a distance of <8 μm. These voltage losses limit the maximum spatial distance between syntrophic partners with model simulations, indicating that sulfate-reducing bacterial cells can remain metabolically active up to ∼30 μm away from the archaeal-bacterial interface. Model simulations further predict that a hybrid metabolism that combines DIET with a small contribution of diffusive exchange of electron donors can offer energetic advantages for syntrophic consortia. IMPORTANCE Anaerobic oxidation of methane is a globally important, microbially mediated process reducing the emission of methane, a potent greenhouse gas. In this study, we investigate the mechanism of how a microbial consortium consisting of archaea and bacteria carries out this process and how these organisms interact with each other through the sharing of electrons. We present a process-based model validated by novel experimental measurements of the metabolic activity of individual, phylogenetically identified cells in very large (>20-μm-diameter) microbial aggregates. Model simulations indicate that extracellular electron transfer between archaeal and bacterial cells within a consortium is limited by potential losses and suggest that a flexible use of electron donors can provide energetic advantages for syntrophic consortia.

A Reduced F 420 -Dependent Nitrite Reductase in an Anaerobic Methanotrophic Archaeon

“…Collectively, these anaerobes employ a reversed methanogenesis pathway for methane oxidation ( 2 , 6 ). Over the last 2 decades, several mechanisms for the syntrophy in AOM have been put forward, and it remains an active research topic ( 2 – 4 , 7 – 13 ). In one case, it was hypothesized that ANME-2 archaea are capable of directly reducing sulfate to oxidize methane ( 3 ), bringing new attention to the genomic data linked to sulfate metabolism in ANME, including the homologs of F 420 -dependent sulfite reductase (Fsr) ( 8 , 14 – 18 ).…”

Physiological adaptation of sulfate reducing bacteria in syntrophic partnership with anaerobic methanotrophic archaea

“…It is possible that these syntrophic SRB scavenge formate from the environment. Alternatively, a recent paper found a hybrid of electron transfer by DIET and by diffusible intermediates (mediated interspecies electron transfer or MIET) to be energetically favorable[57]. In this model, the bulk of electrons would still be transferred by DIET, but up to 10 % of electrons could be shared by MIET via formate[57], an intermediate suggested in earlier studies[26,56].…”

Evolutionary Diversification of MethanotrophicCa. Methanophagales (ANME-1) and Their Expansive Virome

“…Hence, the physiological utility of hydrogenases may vary between lineages. Whereas hydrogen is likely not feasible as the sole intermediate for syntrophic AOM 11,20,45 , it could be produced by ANME-1c as an additional intermediate, as proposed in a mixed model involving direct electron transfer and metabolite exchange 5,46 .…”