Dataset Information

Rumen microbial communities influence metabolic phenotypes in lambs.

ABSTRACT: The rumen microbiota is an essential part of ruminants shaping their nutrition and health. Despite its importance, it is not fully understood how various groups of rumen microbes affect host-microbe relationships and functions. The aim of the study was to simultaneously explore the rumen microbiota and the metabolic phenotype of lambs for identifying host-microbe associations and potential biomarkers of digestive functions. Twin lambs, separated in two groups after birth were exposed to practices (isolation and gavage with rumen fluid with protozoa or protozoa-depleted) that differentially restricted the acquisition of microbes. Rumen microbiota, fermentation parameters, digestibility and growth were monitored for up to 31 weeks of age. Microbiota assembled in isolation from other ruminants lacked protozoa and had low bacterial and archaeal diversity whereas digestibility was not affected. Exposure to adult sheep microbiota increased bacterial and archaeal diversity independently of protozoa presence. For archaea, Methanomassiliicoccales displaced Methanosphaera. Notwithstanding, protozoa induced differences in functional traits such as digestibility and significantly shaped bacterial community structure, notably Ruminococcaceae and Lachnospiraceae lower up to 6 folds, Prevotellaceae lower by ~40%, and Clostridiaceae and Veillonellaceae higher up to 10 folds compared to microbiota without protozoa. An orthogonal partial least squares-discriminant analysis of urinary metabolome matched differences in microbiota structure. Discriminant metabolites were mainly involved in amino acids and protein metabolic pathways while a negative interaction was observed between methylotrophic methanogens Methanomassiliicoccales and trimethylamine N-oxide. These results stress the influence of gut microbes on animal phenotype and show the potential of metabolomics for monitoring rumen microbial functions.

SUBMITTER: Morgavi DP

PROVIDER: S-EPMC4601264 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Rumen microbial communities influence metabolic phenotypes in lambs.

Morgavi Diego P DP Rathahao-Paris Estelle E Popova Milka M Boccard Julien J Nielsen Kristian F KF Boudra Hamid H

Frontiers in microbiology 20151012

The rumen microbiota is an essential part of ruminants shaping their nutrition and health. Despite its importance, it is not fully understood how various groups of rumen microbes affect host-microbe relationships and functions. The aim of the study was to simultaneously explore the rumen microbiota and the metabolic phenotype of lambs for identifying host-microbe associations and potential biomarkers of digestive functions. Twin lambs, separated in two groups after birth were exposed to practice ...[more]

PMID: 26528248

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Project description:The pre-weaning period is crucial for rumen developmental plasticity, which can have a long-term impact on animal performance. Understanding the rumen microbiota during early life is important to elucidate its potential role in rumen development. In this study, the rumen microbiota of 10-day-old Hu lambs fed either milk replacer (B-10), milk replacer and starter (STA) or milk replacer and starter supplemented with alfalfa (S-ALF) in the pre- (d17, 24, and 38) and post-weaning periods (d45 and 66) were assessed to characterize rumen microbial colonization during early life and its response to fiber intervention. In the rumens of B-10 lambs, 498 operational taxonomic units belonging to 33 predominant genera were observed, and the top six predicted functions included "Membrane transport," "carbohydrate metabolism," "amino acid metabolism," "replication and repair," "translation," and "energy metabolism." Prevotella, Succinivibrio, Bifidobacterium, and Butyrivibrio abundances were increased at d38 for both STA and S-ALF groups compared to the B-10 group, whereas fibrolytic bacteria of the taxa Lachnospiraceae and Treponema were only increased in the S-ALF group at d38. A number of saccharolytic bacteria (Bacteroidaceae), organic acid-producing bacteria (Coprococcus and Actinomyces), proteolytic and amino acid fermenters (Fusobacterium) and fibrolytic bacteria (unclassified Ruminococcaceae) were significantly decreased in the STA lambs but not in the S-ALF lambs at d38. After weaning and exposed to alfalfa, the rumen microbial composition in the STA group started to appear similar to that of the S-ALF lambs. The relative abundance of unclassified Clostridiales was higher in S-ALF lambs than STA lambs after weaning. Spearman's correlation analysis showed positive relationships between unclassified Lachnospiraceae, unclassified Clostridiales, Treponema, unclassified Bacteroidales, Coprococcus and crude protein intake, neutral detergent fiber intake, and plasma β-hydroxybutyrate. The unclassified Lachnospiraceae and Treponema were also positively correlated with average daily gain. Our results revealed that alfalfa stimulated changes in rumen microbiota during the pre- and post-weaning periods and was consistent with rumen development for better feed intake and animal performance before and after weaning. The findings of this study provide clues for strategies to improve rumen function through manipulation of the rumen microbiota during early life.

Project description:The profiling of 16S rRNA revolutionized the exploration of microbiomes, allowing to describe community composition by enumerating relevant taxa and their abundances. However, taxonomic profiles alone lack interpretability in terms of bacterial metabolism, and their translation into functional characteristics of microbiomes is a challenging task. This bottom-up approach minimally requires a reference collection of major metabolic traits deduced from the complete genomes of individual organisms, an accurate method of projecting these traits from a reference collection to the analyzed amplicon sequence variants (ASVs), and, ultimately, an approach to a microbiome-wide aggregation of predicted individual traits into physiologically relevant cumulative metrics to characterize and compare multiple microbiome samples. In this study, we extended a previously introduced computational approach for the functional profiling of complex microbial communities, which is based on the concept of binary metabolic phenotypes encoding the presence ("1") or absence ("0") of various measurable physiological properties in individual organisms that are termed phenotype carriers or non-carriers, respectively. Derived from complete genomes via metabolic reconstruction, binary phenotypes provide a foundation for the prediction of functional traits for each ASV identified in a microbiome sample. Here, we introduced three distinct mapping schemes for a microbiome-wide phenotype prediction and assessed their accuracy on the 16S datasets of mock bacterial communities representing human gut microbiome (HGM) as well as on two large HGM datasets, the American Gut Project and the UK twins study. The 16S sequence-based scheme yielded a more accurate phenotype predictions, while the taxonomy-based schemes demonstrated a reasonable performance to warrant their application for other types of input data (e.g., from shotgun metagenomics or qPCR). In addition to the abundance-weighted Community Phenotype Indices (CPIs) reflecting the fractional representation of various phenotype carriers in microbiome samples, we employ metrics capturing the diversity of phenotype carriers, Phenotype Alpha Diversity (PAD) and Phenotype Beta Diversity (PBD). In combination with CPI, PAD allows to classify the robustness of metabolic phenotypes by their anticipated stability in the face of potential environmental perturbations. PBD provides a promising approach for detecting the metabolic features potentially contributing to disease-associated metabolic traits as illustrated by a comparative analysis of HGM samples from healthy and Crohn's disease cohorts.

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Project description:Several ruminal cellulolytic bacteria species are sensitive to pH and could therefore be used as biomarkers to determine the risk of sub-acute ruminal acidosis (SARA) in finishing lambs. This study compared a 2-4 h post feeding ruminal pH measurement to abundances of the ruminal pH-sensitive bacteria to evaluate the risk of SARA in a herd of 120 finishing lambs. The lambs were reared in individual units for 50 days. Ruminal fluid was collected by use of an orogastric tube on day 51 2-4 h after feeding. Although the lambs were fed an identical diet, they responded differently in the abundances of four ruminal pH sensitive cellulolytic bacteria (Ruminococcus albus, Ruminococcus flavefaciens and Fibrobacter succinogenes and Butyrivibrio fibrisolvens). Lambs with the most or the least cellulolytic bacteria were then classified as either lower SARA risk (LSR, n = 10) or higher SARA risk group (HSR, n = 10), respectively. Data showed that the ruminal pH and VFA profiles were uncorrelated with the number of cellulolytic bacteria (P > 0.050). Lambs with the HSR showed lower ruminal pH (P = 0.013) and acetate to propionate ratio (P = 0.018), higher concentrations of lactate (P = 0.035) and proportion of propionate (P = 0.033) compared to those with the LSR. The DMI and ADG did not differ in LSR and HSR lambs (P > 0.050). A diversity analysis revealed significantly lower diversity in HSR lambs than in LSR (Simpson index, P = 0.004). The relative abundances of the phyla Bacteroidetes, Fibrobacteres, Verruomicrobia, and Proteobacteria were higher in LSR lambs than in HSR (P < 0.050). The abundances of several phyla including Firmicutes, Tenericutes and Actinobacteria were higher in the HSR than in the LSR group (P < 0.050). The bacterial communities of the LSR and HSR clustered separately in rumen based on the Unifrac distances, indicating distinct bacteria communities at OTU level between the LSR and HSR lambs. Overall, there was no correlation between 2 and 4 h post-feeding ruminal pH and the abundance of pH-sensitive bacteria and the amount of these bacteria could be used as a potential biomarker of SARA in lamb herd.

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Dataset Information

Rumen microbial communities influence metabolic phenotypes in lambs.

Publications

Rumen microbial communities influence metabolic phenotypes in lambs.

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