Membrane changes during syntrophic interactions of an archaeal-bacterial coculture.

Syntrophic interactions between bacteria and archaea are vital for anaerobic processes, relying on close cell-to-cell contact for efficient metabolite and electron transfer. Membrane-associated proteins and lipids likely play key roles in stabilizing these contacts, though little is known about membrane changes during syntrophy. These interactions are also central to theories of eukaryogenesis, where a symbiosis between an archaeal host - likely an Asgard archaeon - and a bacterial partner may have arisen from prior syntrophic interactions. Model systems of syntrophic microbes provide valuable insights into how such intimate associations could have led to the emergence of eukaryotic life. Here, we used syntrophic cocultures of the sulfate-reducing bacterium Desulfovibrio vulgaris and the methanogenic archaeon Methanococcus maripaludis to investigate membrane changes during a syntrophic interaction involving cell-to-cell contact. Evolved cocultures after several generations under syntrophic conditions were analyzed by proteomics and transcriptomics to identify differentially expressed proteins connected to cell-to-cell interactions, as well as by lipid analyses to determine changes in the cell membrane of both syntrophic partners. These data suggest a higher impact on the archaeon M. maripaludis, affecting transmembrane, signaling, and lipid biosynthesis proteins. To investigate the impact of evolutionary adaptation, both partners were re-isolated from a non-evolved ancestral coculture (coculture after mixing species), as well as from evolved (several generations) cocultures. While lipid profiles had changed in the coculture due to evolutionary adaptation, isolates were found to revert their lipid composition to the wildtype profile when growing independent again. This in-depth analysis of a model syntrophic coculture provides clues on how interdomain cell-to-cell interactions might have led to membrane changes during early eukaryogenesis.