Dataset Information

Identification of Microbial Genetic Capacities and Potential Mechanisms Within the Rumen Microbiome Explaining Differences in Beef Cattle Feed Efficiency.

ABSTRACT: In this study, Bos Taurus cattle offered one high concentrate diet (92% concentrate-8% straw) during two independent trials allowed us to classify 72 animals comprising of two cattle breeds as "Low" or "High" feed efficiency groups. Digesta samples were taken from individual beef cattle at the abattoir. After metagenomic sequencing, the rumen microbiome composition and genes were determined. Applying a targeted approach based on current biological evidence, 27 genes associated with host-microbiome interaction activities were selected. Partial least square analysis enabled the identification of the most significant genes and genera of feed efficiency (VIP > 0.8) across years of the trial and breeds when comparing all potential genes or genera together. As a result, limited number of genes explained about 40% of the variability in both feed efficiency indicators. Combining information from rumen metagenome-assembled genomes and partial least square analysis results, microbial genera carrying these genes were determined and indicated that a limited number of important genera impacting on feed efficiency. In addition, potential mechanisms explaining significant difference between Low and High feed efficiency animals were analyzed considering, based on the literature, their gastrointestinal location of action. High feed efficiency animals were associated with microbial species including several Eubacterium having the genetic capacity to form biofilm or releasing metabolites like butyrate or propionate known to provide a greater contribution to cattle energy requirements compared to acetate. Populations associated with fucose sensing or hemolysin production, both mechanisms specifically described in the lower gut by activating the immune system to compete with pathogenic colonizers, were also identified to affect feed efficiency using rumen microbiome information. Microbial mechanisms associated with low feed efficiency animals involved potential pathogens within Proteobacteria and Spirochaetales, releasing less energetic substrates (e.g., acetate) or producing sialic acid to avoid the host immune system. Therefore, this study focusing on genes known to be involved in host-microbiome interaction improved the identification of rumen microbial genetic capacities and potential mechanisms significantly impacting on feed efficiency in beef cattle fed high concentrate diet.

SUBMITTER: Auffret MD

PROVIDER: S-EPMC7292206 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Identification of Microbial Genetic Capacities and Potential Mechanisms Within the Rumen Microbiome Explaining Differences in Beef Cattle Feed Efficiency.

Auffret Marc D MD Stewart Robert D RD Dewhurst Richard J RJ Duthie Carol-Anne CA Watson Mick M Roehe Rainer R

Frontiers in microbiology 20200605

In this study, <i>Bos Taurus</i> cattle offered one high concentrate diet (92% concentrate-8% straw) during two independent trials allowed us to classify 72 animals comprising of two cattle breeds as "Low" or "High" feed efficiency groups. Digesta samples were taken from individual beef cattle at the abattoir. After metagenomic sequencing, the rumen microbiome composition and genes were determined. Applying a targeted approach based on current biological evidence, 27 genes associated with host-m ...[more]

PMID: 32582125

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Project description:Exploring compositional and functional characteristics of the rumen microbiome can improve the understanding of its role in rumen function and cattle feed efficiency. In this study, we applied metatranscriptomics to characterize the active rumen microbiomes of beef cattle with different feed efficiencies (efficient, n = 10; inefficient, n = 10) using total RNA sequencing. Active bacterial and archaeal compositions were estimated based on 16S rRNAs, and active microbial metabolic functions including carbohydrate-active enzymes (CAZymes) were assessed based on mRNAs from the same metatranscriptomic data sets. In total, six bacterial phyla (Proteobacteria, Firmicutes, Bacteroidetes, Spirochaetes, Cyanobacteria, and Synergistetes), eight bacterial families (Succinivibrionaceae, Prevotellaceae, Ruminococcaceae, Lachnospiraceae, Veillonellaceae, Spirochaetaceae, Dethiosulfovibrionaceae, and Mogibacteriaceae), four archaeal clades (Methanomassiliicoccales, Methanobrevibacter ruminantium, Methanobrevibacter gottschalkii, and Methanosphaera), 112 metabolic pathways, and 126 CAZymes were identified as core components of the active rumen microbiome. As determined by comparative analysis, three bacterial families (Lachnospiraceae, Lactobacillaceae, and Veillonellaceae) tended to be more abundant in low-feed-efficiency (inefficient) animals (P < 0.10), and one archaeal taxon (Methanomassiliicoccales) tended to be more abundant in high-feed-efficiency (efficient) cattle (P < 0.10). Meanwhile, 32 microbial metabolic pathways and 12 CAZymes were differentially abundant (linear discriminant analysis score of >2 with a P value of <0.05) between two groups. Among them, 30 metabolic pathways and 11 CAZymes were more abundant in the rumen of inefficient cattle, while 2 metabolic pathways and 1 CAZyme were more abundant in efficient animals. These findings suggest that the rumen microbiomes of inefficient cattle have more diverse activities than those of efficient cattle, which may be related to the host feed efficiency variation.IMPORTANCE This study applied total RNA-based metatranscriptomics and showed the linkage between the active rumen microbiome and feed efficiency (residual feed intake) in beef cattle. The data generated from the current study provide fundamental information on active rumen microbiome at both compositional and functional levels, which serve as a foundation to study rumen function and its role in cattle feed efficiency. The findings that the active rumen microbiome may contribute to variations in feed efficiency of beef cattle highlight the possibility of enhancing nutrient utilization and improve cattle feed efficiency through modification of rumen microbial functions.

Project description:BackgroundMicroorganisms are responsible for fermentation within the rumen and have been reported to contribute to the variation in feed efficiency of cattle. However, to what extent the breed affects the rumen microbiome and its association with host feed efficiency is unknown. Here, rumen microbiomes of beef cattle (n = 48) from three breeds (Angus, Charolais, Kinsella composite hybrid) with high and low feed efficiency were explored using metagenomics and metatranscriptomics, aiming to identify differences between functional potentials and activities of same rumen microbiomes and to evaluate the effects of host breed and feed efficiency on the rumen microbiome.ResultsRumen metagenomes were more closely clustered together and thus more conserved among individuals than metatranscriptomes, suggesting that inter-individual functional variations at the RNA level were higher than those at the DNA level. However, while mRNA enrichment significantly increased the sequencing depth of mRNA and generated similar functional profiles to total RNA-based metatranscriptomics, it led to biased abundance estimation of several transcripts. We observed divergent rumen microbial composition (metatranscriptomic level) and functional potentials (metagenomic level) among three breeds, but differences in functional activity (metatranscriptomic level) were less apparent. Differential rumen microbial features (e.g., taxa, diversity indices, functional categories, and genes) were detected between cattle with high and low feed efficiency, and most of them were breed-specific.ConclusionsMetatranscriptomes represent real-time functional activities of microbiomes and have the potential to better associate rumen microorganisms with host performances compared to metagenomics. As total RNA-based metatranscriptomics seem to avoid potential biases caused by mRNA enrichment and allow simultaneous use of rRNA for generation of compositional profiles, we suggest their use for linking the rumen microbiome with host phenotypes in future studies. However, if exploration of specific lowly expressed genes is desired, mRNA enrichment is recommended as it will enhance the resolution of mRNA. Finally, the differential microbial features observed between efficient and inefficient steers tended to be specific to breeds, suggesting that interactions between host breed genotype and the rumen microbiome contribute to the variations in feed efficiency observed. These breed-associated differences represent an opportunity to engineer specific rumen microbiomes through selective breeding of the hosts.

Project description:Background: The impact of extreme changes in weather patterns on the economy and human welfare is one of the biggest challenges our civilization faces. From anthropogenic contributions to climate change, reducing the impact of farming activities is a priority since it is responsible for up to 18% of global greenhouse gas emissions. To this end, we tested whether ruminal and stool microbiome components could be used as biomarkers for methane emission and feed efficiency in bovine by studying 52 Brazilian Nelore bulls belonging to two feed intervention treatment groups, that is, conventional and by-product-based diets. Results: We identified a total of 5,693 amplicon sequence variants (ASVs) in the Nelore bulls' microbiomes. A Differential abundance analysis with the ANCOM approach identified 30 bacterial and 15 archaeal ASVs as differentially abundant (DA) among treatment groups. An association analysis using Maaslin2 software and a linear mixed model indicated that bacterial ASVs are linked to the host's residual methane emission (RCH4) and residual feed intake (RFI) phenotype variation, suggesting their potential as targets for interventions or biomarkers. Conclusion: The feed composition induced significant differences in both abundance and richness of ruminal and stool microbial populations in ruminants of the Nelore breed. The industrial by-product-based dietary treatment applied to our experimental groups influenced the microbiome diversity of bacteria and archaea but not of protozoa. ASVs were associated with RCH4 emission and RFI in ruminal and stool microbiomes. While ruminal ASVs were expected to influence CH4 emission and RFI, the relationship of stool taxa, such as Alistipes and Rikenellaceae (gut group RC9), with these traits was not reported before and might be associated with host health due to their link to anti-inflammatory compounds. Overall, the ASVs associated here have the potential to be used as biomarkers for these complex phenotypes.

Dataset Information

Identification of Microbial Genetic Capacities and Potential Mechanisms Within the Rumen Microbiome Explaining Differences in Beef Cattle Feed Efficiency.

Publications

Identification of Microbial Genetic Capacities and Potential Mechanisms Within the Rumen Microbiome Explaining Differences in Beef Cattle Feed Efficiency.

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