Interspecies Formate Exchange Drives Syntrophic Growth of Syntrophotalea carbinolica and Methanococcus maripaludis.

The complete remineralization of organic matter in anoxic environments relies on communities of microorganisms that ferment organic acids and alcohols to CH. This is accomplished through syntrophic association of H or formate producing bacteria and methanogenic archaea, where exchange of these intermediates enables growth of both organisms. While these communities are essential to Earth's carbon cycle, our understanding of the dynamics of H or formate exchanged is limited. Here, we establish a model partnership between Syntrophotalea carbinolica and Methanococcus maripaludis. Through sequencing a transposon mutant library of M. maripaludis grown with ethanol oxidizing S. carbinolica, we found that genes encoding the F-dependent formate dehydrogenase (Fdh) and F-dependent methylene-tetrahydromethanopterin dehydrogenase (Mtd) are important for growth. Competitive growth of M. maripaludis mutants defective in either H or formate metabolism verified that, across multiple substrates, interspecies formate exchange was dominant in these communities. Agitation of these cultures to facilitate diffusive loss of H to the culture headspace resulted in an even greater competitive advantage for M. maripaludis strains capable of oxidizing formate. Finally, we verified that an M. maripaludis mutant had a defect during syntrophic growth. Together, these results highlight the importance of formate exchange for the growth of methanogens under syntrophic conditions. In the environment, methane is typically generated by fermentative bacteria and methanogenic archaea working together in a process called syntrophy. Efficient exchange of small molecules like H or formate is essential for growth of both organisms. However, difficulties in determining the relative contribution of these intermediates to methanogenesis often hamper efforts to understand syntrophic interactions. Here, we establish a model syntrophic coculture composed of S. carbinolica and the genetically tractable methanogen M. maripaludis. Using mutant strains of M. maripaludis that are defective for either H or formate metabolism, we determined that interspecies formate exchange drives syntrophic growth of these organisms. Together, these results advance our understanding of the degradation of organic matter in anoxic environments.