Ruminant livestock is a major source of the potent greenhouse gas methane. The complex rumen microbiome, consisting of bacteria, archaea, and microbial eukaryotes, facilitates anaerobic plant biomass degradation in the cow rumen, leading to
methane emissions. Using an integrated approach combining multidomain quantitative
metatranscriptomics with gas and volatile fatty acid (VFA) profiling, we aimed at obtaining the most comprehensive picture of the active rumen microbiome during feed degradation to date. Bacterial, archaeal, and eukaryotic biomass, but also methane emissions
and VFA concentrations, increased drastically within an hour after feed intake. mRNA
profiling revealed a dynamic response of carbohydrate-active enzyme transcripts, transcripts involved in VFA production and methanogenesis. While the relative abundances
of functional transcripts did not mirror observed processes, such as methane emissions,
transformation to mRNA abundance per gram of rumen fluid echoed ruminant processes. The microbiome composition was highly individual, with, e.g., ciliate,
Neocallimastigaceae,
Prevotellaceae,
Succinivibrionaceae, and
Fibrobacteraceae abundances differing
between cows. Microbiome individuality was accompanied by inter- and intradomain
multifunctional redundancy among microbiome members during feed degradation. This
likely enabled the robust performance of the anaerobic degradation process in each rumen.
Neocallimastigaceae and ciliates contributed an unexpectedly large share of transcripts for cellulose- and hemicellulose-degrading enzymes, respectively. Methyl-reducing
but not CO2-reducing methanogens were positively correlated with methane emissions.
While
Methanomassiliicoccales switched from methanol to methylamines as electron acceptors,
Methanosphaera became the dominating methanol-reducing methanogen. This
study for the first time linked rumen meta-omics with processes and enabled holistic insights into the contribution of all microbiome members to feed degradation.
Importance: Ruminant animals, such as cows, live in a tight symbiotic association
with microorganisms, allowing them to feed on otherwise indigestible plant biomass
as food sources. Methane is produced as an end product of the anaerobic feed degradation in ruminants and is emitted to the atmosphere, making ruminant animals
among the major anthropogenic sources of the potent greenhouse gas methane.
Using newly developed quantitative metatranscriptomics for holistic microbiome
analysis, we here identified bacterial, archaeal, and eukaryotic key players and the
short-term dynamics of the rumen microbiome during anaerobic plant biomass degradation and subsequent methane emissions. These novel insights might pave the
way for novel ecologically and economically sustainable methane mitigation strategies, much needed in times of global climate change.
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