Identifying active rumen epithelial associated bacteria and archaea in beef cattle divergent in feed efficiency using total RNA-seq.
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ABSTRACT:
SUBMITTER: Tan RSG
PROVIDER: S-EPMC8610342 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:The importance of the rumen microbiota on nutrient cycling to the animal is well recognized; however, our understanding of the influence of the rumen microbiome composition on feed efficiency is limited. The rumen microbiomes of two large animal cohorts (125 heifers and 122 steers) were characterized to identify specific bacterial members (operational taxonomic units [OTUs]) associated with feed efficiency traits (ADFI, ADG, and G:F) in beef cattle. The heifer and steer cohorts were fed a forage-based diet and a concentrate-based diet, respectively. A rumen sample was obtained from each animal via esophageal tubing and bacterial community composition was determined through 16S rRNA gene sequencing of the V4 region. Based on a regression approach that used individual performance measures, animals were classified into divergent feed efficiency groups. Within cohort, an extreme set of 16 animals from these divergent groups was selected as a discovery population to identify differentially abundant OTUs across the rumen bacterial communities. The remaining samples from each cohort were selected to perform forward stepwise regressions using the differentially abundant OTUs as explanatory variables to distinguish predictive OTUs for the feed efficiency traits and to quantify the OTUs collective impact on feed efficiency phenotypes. OTUs belonging to the families Prevotellaceae and Victivallaceae were present across models for heifers, whereas OTUs belonging to the families Prevotellaceae and Lachnospiraceae were present across models for steers. Within the heifer cohort, models explained 19.3%, 25.3%, and 19.8% of the variation for ADFI, ADG, and G:F, respectively. Within the steer cohort, models explained 27.7%, 32.5%, and 26.9% of the variation for ADFI, ADG, and G:F, respectively. Overall, this study suggests a substantial role of the rumen microbiome on feed efficiency responses.
| S-EPMC6093515 | biostudies-literature
Project description:The rumen microbiome is critical to nutrient utilization and feed efficiency in cattle. Consequently, the objective of this study was to identify microbial and biochemical factors in Angus steers affecting divergences in feed efficiency using 16S amplicon sequencing and untargeted metabolomics. Based on calculated average residual feed intake (RFI), steers were divided into high- and low-RFI groups. Features were ranked in relation to RFI through supervised machine learning on microbial and metabolite compositions. Residual feed intake was associated with several features of the bacterial community in the rumen. Decreased bacterial ?- (P?=?0.03) and ?- diversity (P?<?0.001) was associated with Low-RFI steers. RFI was associated with several serum metabolites. Low-RFI steers had greater abundances of pantothenate (P?=?0.02) based on fold change (high/low RFI). Machine learning on RFI was predictive of both rumen bacterial composition and serum metabolomic signature (AUC???0.7). Log-ratio proportions of the bacterial classes Flavobacteriia over Fusobacteriia were enriched in low-RFI steers (F?=?6.8, P?=?0.01). Reductions in Fusobacteriia and/or greater proportions of pantothenate-producing bacteria, such as Flavobacteriia, may result in improved nutrient utilization in low-RFI steers. Flavobacteriia and Pantothenate may potentially serve as novel biomarkers to predict or evaluate feed efficiency in Angus steers.
| S-EPMC6917770 | biostudies-literature
Project description:BACKGROUND:Understanding the host impact on its symbiotic microbiota is important in redirecting the rumen microbiota and thus improving animal performance. The current study aimed to understand how rumen microbiota were altered and re-established after being emptied and receiving content from donor, thus to understand the impact of such process on rumen microbial fermentation and to explore the microbial phylotypes with higher manipulation potentials. RESULTS:Individual animal had strong effect on the re-establishment of the bacterial community according to the observed profiles detected by both fingerprinting and pyrosequencing. Most of the bacterial profile recovery patterns and extents at genus level varied among steers; and each identified bacterial genus responded to transfaunation differently within each host. Coriobacteriaceae, Coprococcus, and Lactobacillus were found to be the most responsive and tunable genera by exchanging rumen content. Besides, the association of 18 bacterial phylotypes with host fermentation parameters suggest that these phylotypes should also be considered as the regulating targets in improving host feed efficiency. In addition, the archaeal community had different re-establishment patterns for each host as determined by fingerprint profiling: it was altered after receiving non-native microbiome in some animals, while it resumed its original status after the adaptation period in the other ones. CONCLUSIONS:The highly individualized microbial re-establishment process suggested the importance of considering host genetics, microbial functional genomics, and host fermentation/performance assessment when developing effective and selective microbial manipulation methods for improving animal feed efficiency.
| S-EPMC5869788 | biostudies-literature
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.
| S-EPMC5394315 | biostudies-literature
Project description:Understanding host-microbial interactions in the rumen and its influence on desirable production traits may lead to potential microbiota manipulation or genetic selection for improved cattle feed efficiency. This study investigated the host transcriptome and its correlation with the rumen archaea and bacteria differential abundance of two pure beef cattle breeds (Angus and Charolais) and one composite beef hybrid (Kinsella) divergent for residual feed intake (RFI; low-RFI vs. high-RFI). Using RNA-Sequencing of rumen tissue and 16S rRNA gene amplicon sequencing, differentially expressed genes (FDR ≤ 0.05, |log2(Fold-change) >|2) and differentially abundant (p-value < 0.05) archaea and bacteria amplicon sequence variants (ASV) were determined. Significant correlations between gene expression and ASVs (p-value < 0.05) were determine using Spearman correlation. Interesting associations with muscle contraction and the modulation of the immune system were observed for the genes correlated with bacterial ASVs. Potential functional candidate genes for feed efficiency status were identified for Angus (CCL17, CCR3, and CXCL10), Charolais (KCNK9, GGT1 and IL6), and Kinsella breed (ESR2). The results obtained here provide more insights regarding the applicability of target host and rumen microbial traits for the selection and breeding of more feed efficient beef cattle.
| S-EPMC10533831 | biostudies-literature
Project description:Rumen content-associated (RC) and epithelial tissue-attached (RT) bacterial communities are composed of different phylotypes and play distinctive roles. This study aimed to compare the composition of the RT and RC bacterial communities of steers differing in feed efficiency. The microbiota of RT and RC samples collected from sixteen beef steers with high or low residual feed intake (RFI) were analyzed through sequencing of partial 16S rRNA gene amplicons. Bacteroidetes, Proteobacteria and Firmicutes were the predominant phyla and Prevotella was the most abundant genus in both RC and RT bacterial communities. In total, 19 OTUs of the RC samples and 19 OTUs of the RT samples were differentially abundant (DA) between H-RFI and l-RFI steers. Among them, a common DA OTU belonged to Prevotella genus was identified in both RC and RT samples, making it the potential key microbial marker for indicating feed efficiency of steers. The co-occurrence of the DA OTUs among RT and RC samples suggest the importance of these two communities function as a complete system in influencing host feed efficiency.
| S-EPMC8654779 | biostudies-literature
Project description:Exploring the compositional characteristics of rumen eukaryotic community can expand our understanding of their role in rumen function and feed efficiency. In this study, we applied metatranscriptomics to characterize the active rumen eukaryotic community (protozoa and fungi) in beef cattle (n = 48) of three breeds [Angus (AN), Charolais (CH), and Kinsella Composite (KC)] and with divergent residual feed intake (RFI). The composition of active rumen eukaryotic microbiota was evaluated based on enriched 18S rRNAs from the metatranscriptomic datasets. At the phylum level, a total of four protozoal taxa (Ciliophora, Parabasalia, unclassified SAR, and unclassified Alveolata), six fungal taxa (Neocallimastigomycota, Basidiomycota, unclassified Fungi, Mucoromycota, Ascomycota, and Chytridiomycota), and one sister group of kingdom Fungi (unclassified Opisthokonta) were detected with relative abundances higher than 0.01% and in at least 50% of animals within each breed. Among these, Ciliophora, Parabasalia, unclassified Opisthokonta, and Neocallimastigomycota were the top four active eukaryotic phyla. At the genus level, a total of 8 ciliated protozoa, 5 flagellated protozoa, 5 anaerobic fungi, and 10 aerobic fungi taxa were detected, with unclassified Trichostomatia, Tetratrichomonas, unclassified Neocallimastigaceae, and Pleurotus being the most predominant taxa of ciliated protozoa, flagellated protozoa, anaerobic fungi, and aerobic fungi, respectively. Differential abundance analysis revealed that breed had a significant effect on the phylogenetic lineages of rumen eukaryotes, and seven fungal taxa were more abundant (linear discriminant analysis score > 2 with P < 0.05) in the rumen of KC steers than in the rumen of AN and CH steers. Although principal coordinate analysis (PCoA) revealed that the ruminal active eukaryotic profiles were not distinguishable between high- and low-RFI groups, the diversity indices, including Faith's phylogenetic diversity (PD), observed operational taxonomic units (OTUs), and Shannon index of rumen eukaryotes were higher in low-RFI steers than those in high-RFI steers. Meanwhile, the abundance of genus Entodinium and the kingdom Fungi was higher in low-RFI steers than that in high-RFI steers. This information on active rumen eukaryotic microbiota and identified differential abundance of taxa between high- and low-RFI animals suggests the possibility of improving feed efficiency through altering rumen eukaryotic microbiota.
| S-EPMC7082318 | biostudies-literature
Project description: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.
| S-EPMC7292206 | biostudies-literature
Project description:Rumen microbiome composition and functionality is linked to animal feed efficiency, particularly for bovine ruminants. To investigate this in sheep, we compared rumen bacterial and archaeal populations (and predicted metabolic processes) of sheep divergent for the feed efficiency trait feed conversion ratio (FCR). In our study 50 Texel cross Scottish Blackface (TXSB) ram lambs were selected from an original cohort of 200 lambs. From these, 26 were further selected for experimentation based on their extreme FCR (High Feed Efficiency, HFE = 13; Low Feed Efficiency, LFE = 13). Animals were fed a 95% concentrate diet ad libitum over 36 days. 16S rRNA amplicon sequencing was used to investigate the rumen bacterial and archaeal communities in the liquid and solid rumen fractions of sheep divergent for FCR. Weighted UniFrac distances separated HFE and LFE archaea communities from the liquid rumen fraction (Permanova, P < 0.05), with greater variation observed for the LFE cohort (Permdisp, P < 0.05). LFE animals exhibited greater Shannon and Simpson diversity indices, which was significant for the liquid rumen fraction (P < 0.05). Methanobrevibacter olleyae (in liquid and solid fractions) and Methanobrevibacter millerae (liquid fraction) were differentially abundant, and increased in the LFE cohort (P.adj < 0.05), while Methanobrevibacter wolinii (liquid fraction) was increased in the HFE cohort (P.adj < 0.05). This suggests that methanogenic archaea may be responsible for a potential loss of energy for the LFE cohort. Bacterial community composition (Permanova, P > 0.1) and diversity (P > 0.1) was not affected by the FCR phenotype. Only the genus Prevotella 1 was differentially abundant between HFE and LFE cohorts. Although no major compositional shifts of bacterial populations were identified amongst the feed efficient cohorts (FDR > 0.05), correlation analysis identified putative drivers of feed efficiency with Ruminococcaceae UCG-014 (liquid, rho = -0.53; solid, rho = -0.56) and Olsenella (solid, rho = -0.40) exhibiting significant negative association with FCR (P < 0.05). Bifidobacterium and Megasphaera showed significant positive correlations with ADG. Major cellulolytic bacteria Fibrobacter (liquid, rho = 0.43) and Ruminococcus 1 (liquid, rho = 0.41; solid, rho = 41) correlated positively with FCR (P < 0.05). Our study provides evidence that feed efficiency in sheep is likely influenced by compositional changes to the archaeal community, and abundance changes of specific bacteria, rather than major overall shifts within the rumen microbiome.
| S-EPMC7477290 | biostudies-literature
Project description:BackgroundFeed efficient cattle consume less feed and produce less environmental waste than inefficient cattle. Many factors are known to contribute to differences in feed efficiency, however the underlying molecular mechanisms are largely unknown. Our study aimed to understand how host gene expression in the rumen epithelium contributes to differences in residual feed intake (RFI), a measure of feed efficiency, using a transcriptome profiling based approach.ResultsThe rumen epithelial transcriptome from highly efficient (low (L-) RFI, n = 9) and inefficient (high (H-) RFI, n = 9) Hereford x Angus steers was obtained using RNA-sequencing. There were 122 genes differentially expressed between the rumen epithelial tissues of L- and H- RFI steers (p < 0.05) with 85 up-regulated and 37 down-regulated in L-RFI steers. Functional analysis of up-regulated genes revealed their involvement in acetylation, remodeling of adherens junctions, cytoskeletal dynamics, cell migration, and cell turnover. Additionally, a weighted gene co-expression network analysis (WGCNA) identified a significant gene module containing 764 genes that was negatively correlated with RFI (r = -0.5, p = 0.03). Functional analysis revealed significant enrichment of genes involved in modulation of intercellular adhesion through adherens junctions, protein and cell turnover, and cytoskeletal organization that suggest possible increased tissue morphogenesis in the L-RFI steers. Additionally, the L-RFI epithelium had increased expression of genes involved with the mitochondrion, acetylation, and energy generating pathways such as glycolysis, tricarboxylic acid cycle, and oxidative phosphorylation. Further qPCR analysis of steers with different RFI (L-RFI, n = 35; M-RFI, n = 34; H-RFI, n = 35) revealed that the relative mitochondrial genome copy number per cell of the epithelium was positively correlated with RFI (r = 0.21, p = 0.03).ConclusionsOur results suggest that the rumen epithelium of L-RFI (efficient) steers may have increased tissue morphogenesis that possibly increases paracellular permeability for the absorption of nutrients and increased energy production to support the energetic demands of increased tissue morphogenesis compared to those of H-RFI (inefficient) animals. Greater expression of mitochondrial genes and lower relative mitochondrial genome copy numbers suggest a greater rate of transcription in the rumen epithelial mitochondria of L-RFI steers. Understanding how host gene expression profiles are associated with RFI could potentially lead to identification of mechanisms behind this trait, which are vital to develop strategies for the improvement of cattle feed efficiency.
| S-EPMC4979190 | biostudies-literature