Metabolic influence of core ciliates within the rumen microbiome

Abstract

Protozoa comprise a major fraction of the microbial biomass in the rumen microbiome, of which the genus Entodinium has been consistently observed to be dominant across a diverse genetic and geographical range of ruminant hosts. Despite the apparent core role that species such as Entodinium caudatum exert, their major biological and metabolic contributions to rumen function remain largely undescribed. Here, we have leveraged (meta)genome-centric metaproteomes from rumen fluid samples originating from both cattle and goats fed diets with varying inclusion levels of lipids and starch, to detail the specific metabolic niches that E. caudatum occupies in the context of its microbial co-habitants. Initial proteome estimations via total protein counts and label-free quantification highlight that E. caudatum comprises an extensive fraction of the total rumen metaproteome. Our analysis also suggested increased microbial predation and volatile fatty acid (VFA) metabolism by E. caudatum to occur in high methane-emitting animals, although with no apparent direct metabolic link to methanogenesis. Despite E. caudatum having a well-established reputation for digesting starch, it was unexpectedly less detectable in low methane emitting-animals fed high starch diets, which were instead dominated by propionate/succinate-producing bacterial populations suspected of being resistant to predation irrespective of host. Finally, we reaffirmed our abovementioned observations in geographically independent datasets, thus illuminating the substantial metabolic influence that under-explored eukaryotic populations have in the rumen, with greater implications for both digestion and methane metabolism.

Giants’ cooperation: a draft genome of the giant ciliate Muniziella cunhai suggests its ecological role in the capybara’s digestive metabolism

“…glucose), that are metabolized into pyruvate and/or phosphoenolpyruvate through glycolytic pathways. Pyruvate and phosphoenolpyruvate lead to the production of short-chain fatty acids (SCFAs), such as acetate, lactate, propionate, and butyrate, that might be released in gastrointestinal tract of the host [25,52,54]. These pathways were confirmed in our annotations: besides CAZymes, we observed several genes belonging to the Pyruvate Metabolic Pathway (e.g.…”

Emergence of putative energy parasites withinClostridiarevealed by genome analysis of a novel endosymbiotic clade

“…Thus, these protists might be the hosts for the clostridia of the small genome clade. Previous reports focused on prey-predator relationships between eukaryotes and prokaryotes in the gastrointestinal tract of mammals [86,87]; intracellular parasitism should also be considered.…”

Yaks Are Dependent on Gut Microbiota for Survival in the Environment of the Qinghai Tibet Plateau

“…In ruminants with high methane emissions, protozoan enrichment in hydrogenase metabolic pathways were detected, which increases rumen hydrogen production, while no similar phenomenon was detected in ruminants with low methane emissions [89,90], thus, it can be speculated that the abundance of hydrogen-producing protozoa in the yak rumen is low. In fermentation studies on rumen fluid from yak and cattle, hydrogen utilization was greater in cattle than yak, and a high utilization of hydrogen leads to an increase in methane production [91].…”