Concerted Metabolic Shifts Give New Insights Into the Syntrophic Mechanism Between Propionate-Fermenting Pelotomaculum thermopropionicum and Hydrogenotrophic Methanocella conradii

Microbial syntrophy is a thermodynamically-based cooperation between microbial partners that share the small amounts of free energy for anaerobic growth. To gain insights into the mechanism by which syntrophic microorganisms coordinate their metabolism, we constructed cocultures of propionate-oxidizing Pelotomaculum thermopropionicum and hydrogenotrophic Methanocella conradii and compared them to monocultures. Transcriptome analysis was performed on these cultures using strand-specific mRNA sequencing (RNA-Seq). The results showed that in coculture both P. thermopropionicum and M. conradii significantly upregulated the expression of genes involved in catabolism but downregulated those for anabolic biosynthesis. Specifically, genes coding for the methylmalonyl-CoA pathway in P. thermopropionicum and key genes for methanogenesis in M. conradii were substantially upregulated in coculture compared to monoculture. The putative flavin-based electron bifurcation/confurcation systems in both organisms were also upregulated in coculture. Formate dehydrogenase encoding genes in both organisms were markedly upregulated, indicating that formate was produced and utilized by P. thermopropionicum and M. conradii, respectively. The inhibition of syntrophic activity by formate and 2-bromoethanesulphonate (2-BES) but not H(2)/CO(2) also suggested that formate production was used by P. thermopropionicum for the recycling of intracellular redox mediators. Finally, flagellum-induced signal transduction and amino acids exchange was upregulated for syntrophic interactions. Together, our study suggests that syntrophic organisms employ multiple strategies including global metabolic shift, utilization of electron bifurcation/confurcation and employing formate as an alternate electron carrier to optimize their metabolisms for syntrophic growth.