Single cell activity reveals direct electron transfer in methanotrophic consortia

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. The anaerobic oxidation of methane in marine sediments is performed by consortia of methane-oxidizing archaea and sulfate-reducing bacteria; an examination of the role of interspecies spatial positioning on single cell activity reveals that interspecies electron transfer may overcome the requirement for close spatial proximity, a proposition supported by large multi-haem cytochromes in ANME-2 genomes as well as redox-active electron microscopy staining. A novel mechanism for microbial cooperation Anaerobic oxidation of methane in marine sediments, of central importance for the global methane cycle, is a collaborative process performed by consortia of methane-oxidizing archaea and sulfate-reducing bacteria. The biochemical basis of this syntrophic relationship is not fully understood. It has been suggested that exchange of a diffusible metabolite between the cooperating microbes is essential, but two groups reporting in this issue of Nature challenge this idea. Victoria Orphan and colleagues exa