Untangling Syntrophic associations between bacteria and methanogenic archaea in ruminal anaerobic microbial ecosystem

Microbial syntrophy (obligate metabolic mutualism) is the hallmark of energy-constrained anaerobic microbial ecosystems. For example, methanogenic archaea and fermenting bacteria coexist by interspecies hydrogen transfer in the complex microbial ecosystem in the foregut of ruminants; however, these synergistic interactions between different microbes in the rumen are seldom investigated. We hypothesized that certain bacteria and archaea interact and form specific microbial cohorts in the rumen that have different functional attributes. To this end, we examined the total and metabolically active bacterial and archaeal communities in rumen samples of dairy cows collected at different times in a 24h period. Notably, we found the presence of distinct bacterial and archaeal networks that were correlated with molar proportions of specific volatile fatty acids. Furthermore, we demonstrated that these distinct microbial syntrophic networks were host-specific and differed between cows indicating a natural variation in specific microbial syntrophic networks in the rumen of dairy cows. Notably, we employed hypothesis-driven structural equation modeling to test the significance of and to quantify the extent of relationships between bacteria-archaea-volatile fatty acids in the rumen. This study provides new insights on microbial syntrophic interactions in anoxic environments that has broader applications on methane mitigation, energy conservation, and agricultural production.