Abstract
The rumen harbors a complex microbial mixture of archaea, bacteria, protozoa, and fungi that efficiently breakdown plant biomass and its complex dietary carbohydrates into soluble sugars that can be fermented and subsequently converted into metabolites and nutrients utilized by the host animal. While rumen bacterial populations have been well documented, only a fraction of the rumen eukarya are taxonomically and functionally characterized, despite the recognition that they contribute to the cellulolytic phenotype of the rumen microbiota. To investigate how anaerobic fungi actively engage in digestion of recalcitrant fiber that is resistant to degradation, we resolved genome-centric metaproteome and metatranscriptome datasets generated from switchgrass samples incubated for 48 h in nylon bags within the rumen of cannulated dairy cows. Across a gene catalog covering anaerobic rumen bacteria, fungi and viruses, a significant portion of the detected proteins originated from fungal populations. Intriguingly, the carbohydrate-active enzyme (CAZyme) profile suggested a domain-specific functional specialization, with bacterial populations primarily engaged in the degradation of hemicelluloses, whereas fungi were inferred to target recalcitrant cellulose structures via the detection of a number of endo- and exo-acting enzymes belonging to the glycoside hydrolase (GH) family 5, 6, 8, and 48. Notably, members of the GH48 family were amongst the highest abundant CAZymes and detected representatives from this family also included dockerin domains that are associated with fungal cellulosomes. A eukaryote-selected metatranscriptome further reinforced the contribution of uncultured fungi in the ruminal degradation of recalcitrant fibers. These findings elucidate the intricate networks of in situ recalcitrant fiber deconstruction, and importantly, suggest that the anaerobic rumen fungi contribute a specific set of CAZymes that complement the enzyme repertoire provided by the specialized plant cell wall degrading rumen bacteria.
Highlights
It has been estimated that there are ~1 billion domesticated ruminant animals [1] and numbers are predicted to increase further in order to provide food security for the growing human population [2]
Thegenome-resolved metaproteome revealed that a high fraction of detected proteins within our metaproteome were of fungal origin (Fig. 1, numerical detection of proteins can be found in Supplementary Table S2)
The metaproteomics data revealed a higher level of protein grouping across the fungal genomes due to homologous proteins, suggesting that there are conserved features of the fungal genomes that have been sequenced to date
Summary
It has been estimated that there are ~1 billion domesticated ruminant animals [1] and numbers are predicted to increase further in order to provide food security for the growing human population [2]. Extended author information available on the last page of the article broadening the knowledge of the complex microbial interactions and the enzymatic machineries that are employed within the rumen microbiome is thought to provide means to efficiently optimize feed conversion, and the productivity and well-being of the host animal. To facilitate the degradation of complex plant carbohydrates, the rumen microbiome encodes a rich repertoire of carbohydrate-active enzymes (CAZymes). An enhanced focus on isolation, cultivation and characterization of novel anaerobic rumen fungi and protozoa has provided important insight into their lifestyle and enzymatic capacity [4, 7, 8], their quantitative metabolic contributions to the greater rumen ecosystem are still not fully understood
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