Reductive acetogenesis is a dominant process in the ruminant hindgut

Abstract

Background The microbes residing in ruminant gastrointestinal tracts convert plant biomass to nutritious volatile fatty acids, the primary energy source for ruminants. Ruminants´ gastrointestinal tract comprises a foregut (rumen) and hindgut (cecum and colon), each with contrasting structures and functions in anaerobic digestion. With most previous studies focusing on the rumen microbiome, the cecal microbiome is much less investigated and understood, including the assembling microbial communities and overriding pathways of hydrogen metabolism. Results Here we comparatively investigated the composition, capabilities, and activities of the rumen and the cecum microbiome using goats as experimental ruminant model. In situ measurements showed that acetate and hydrogen levels were both higher in the cecum than in the rumen. Concurrently, microbes capable of host mucin degradation and fermentative hydrogen production were more abundant in the cecum, whereas fibrolytic fermentative bacteria, hydrogenotrophic respiratory bacteria, and methanogenic archaea were less abundant. Most strikingly, reductive acetogenic bacteria were 12-fold more abundant in the cecum, and genome-resolved analysis unveiled that cecum acetogens are both phylogenetically and functionally novel. Two in vitro experiments further supported that the pathways of hydrogen metabolism differ between the cecum and the rumen, with increased acetate production and reduced methanogenesis in the cecum. Moreover, a comparative analysis showed a strong enrichment of reductive acetogens in the hindguts of other ruminants. Conclusions These findings, by revealing an enrichment of acetogenesis in an important part of the gastrointestinal tract, reshape our understanding of ruminant hydrogen metabolism and how the H₂ can be managed in accord to livestock methane mitigation efforts.