Single cell activity reveals direct electron transfer in methanotrophic consortia

Abstract

Multicellular assemblages of microorganisms are ubiquitous in nature, and the proximity afforded by aggregation is thought to permit intercellular metabolic coupling that can accommodate otherwise unfavourable reactions. Consortia of methane-oxidizing archaea and sulphate-reducing bacteria are a well-known environmental example of microbial co-aggregation; however, the coupling mechanisms between these paired organisms is not well understood, despite the attention given them because of the global significance of anaerobic methane oxidation. Here we examined the influence of interspecies spatial positioning as it relates to biosynthetic activity within structurally diverse uncultured methane-oxidizing consortia by measuring stable isotope incorporation for individual archaeal and bacterial cells to constrain their potential metabolic interactions. In contrast to conventional models of syntrophy based on the passage of molecular intermediates, cellular activities were found to be independent of both species intermixing and distance between syntrophic partners within consortia. A generalized model of electric conductivity between co-associated archaea and bacteria best fit the empirical data. Combined with the detection of large multi-haem cytochromes in the genomes of methanotrophic archaea and the demonstration of redox-dependent staining of the matrix between cells in consortia, these results provide evidence for syntrophic coupling through direct electron transfer.

Archaea catalyze iron-dependent anaerobic oxidation of methane

“…The AAA in our enrichment culture encode numerous (41 species) multiheme c-type cytochromes (Table S1). This number is much higher than for methanogens, of which only Methanosarcinales encodes few multiheme cytochromes, but similar to M. nitroreducens (38 species) (5), the sulfate-dependent ANME-1 (11 species) (28), ANME-2a (16 species) (29,31), as well as the iron-reducing archaea Ferroglobus placidus (22 species) and Geoglobus (15 species) (32).…”

“…This genomic blueprint suggests that AAA, and possibly also the cytochrome-rich ANME-1 (28) and ANME-2a (29,31) archaea, known for sulfate-dependent methane oxidation, could be versatile methanotrophs that are able to switch between different electron acceptors, depending on environmental conditions (17). It is also conceivable that ANME-2a and ANME-2c archaea, which were shown to couple the reduction of solubilized iron species (iron citrate) to methane oxidation recently (22) .…”

Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia

“…In marine seeps, AOM is predominantly catalyzed by a symbiosis of anaerobic methane-oxidizing euryarchaeotes (ANME) with sulfate-reducing bacteria (SRB), which form consortia of varying cell numbers (∼10 to ∼10 5 cells) and morphology (7,26). Their syntrophic partnership is hypothesized to be mediated by direct electron transfer (27)(28)(29) and/or diffusible intermediates (30,31).…”

Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction

“…Sample preparation for aggregate embedding, sectioning, FISH, and nanoSIMS Sample preparation was carried out following the recently optimized protocol in our lab outlined in (8). Briefly: Paraformaldehyde fixed consortia were detached from the sediment particles via sonication on ice with a sterile remote-tapered microtip probe (Branson) inserted into the liquid.…”