Metagenomic analysis reveals a dynamic microbiome with diversified adaptive functions to utilize high lignocellulosic forages in the cattle rumen

Abstract

Rumen microbiota play a key role in the digestion and utilization of plant materials by the ruminant species, which have important implications for greenhouse gas emission. Yet, little is known about the key taxa and potential gene functions involved in the digestion process. Here, we performed a genome-centric analysis of rumen microbiota attached to six different lignocellulosic biomasses in rumen-fistulated cattle. Our metagenome sequencing provided novel genomic insights into functional potential of 523 uncultured bacteria and 15 mostly uncultured archaea in the rumen. The assembled genomes belonged mainly to Bacteroidota, Firmicutes, Verrucomicrobiota, and Fibrobacterota and were enriched for genes related to the degradation of lignocellulosic polymers and the fermentation of degraded products into short chain volatile fatty acids. We also found a shift from copiotrophic to oligotrophic taxa during the course of rumen fermentation, potentially important for the digestion of recalcitrant lignocellulosic substrates in the physiochemically complex and varying environment of the rumen. Differential colonization of forages (the incubated lignocellulosic materials) by rumen microbiota suggests that taxonomic and metabolic diversification is an evolutionary adaptation to diverse lignocellulosic substrates constituting a major component of the cattle’s diet. Our data also provide novel insights into the key role of unique microbial diversity and associated gene functions in the degradation of recalcitrant lignocellulosic materials in the rumen.

Fig. 1: The majority of the reconstituted rumen-uncultured genomes (RUGs) are novel and do not have any representatives in the publicly available databases.
Fig. 2: The community composition of fiber-attached microbiota changes with incubation time.
Fig. 3: Phylogenetic diversity of fiber-attached RUGs depends on both feed type and sampling times.
Fig. 4: The novelty of the predicted CAZymes and their distribution in RUGs.

Data availability

The raw sequence data have been deposited in NCBI short read archive (SRA) under BioProject ID PRJNA631951. All metagenome assemblies including co-assembly and forage-specific assemblies and the sequences of RUGs have been deposited in NCBI under the same BioProject ID.

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Acknowledgements

This research was funded by the Agricultural Biotechnology Research Institute of Iran (ABRII), the international cooperation and exchange program of the National Natural Science Foundation of China (No. 31461143020), and the Chinese government contribution to CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources in Beijing. The paper contributes to the CGIAR Research Program on Livestock.

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Correspondence to Xue-Zhi Ding or Ghasem Hosseini Salekdeh.

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Gharechahi, J., Vahidi, M.F., Bahram, M. et al. Metagenomic analysis reveals a dynamic microbiome with diversified adaptive functions to utilize high lignocellulosic forages in the cattle rumen. ISME J (2020). https://doi.org/10.1038/s41396-020-00837-2

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