Research ArticleORGANISMAL BIOLOGY

A heritable subset of the core rumen microbiome dictates dairy cow productivity and emissions

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Science Advances  03 Jul 2019:
Vol. 5, no. 7, eaav8391
DOI: 10.1126/sciadv.aav8391
  • Fig. 1 A phylogenetically cohesive core rumen microbiome was found across farms with highly conserved hierarchical structure and tight association to overall microbiome composition.

    (A) Core microbes are highly represented within individual animals, as a high fraction of them (>50% of the core microbes) are present in >70% of the individuals. (B) The prokaryotic core (blue) was represented by 10 phyla of the 30 found in the overall microbiome (x axis; ochre), including 11 prokaryotic, 2 fungal, and 1 protozoal orders, detected in >50% of the individuals in each farm. *The core microbiome was significantly enriched in Bacteroidetes (enrichment analysis, Fisher exact test, after Benjamini-Hochberg correction, P < 0.0005). SR1, candidate division sulphur river 1. Core prokaryotes (i) consisted of 454 microbes, mainly from the orders Bacteroidales (tree; green) and Clostridiales (tree; maroon). Core heritable taxa are presented as gray bar plots on the tree. (C) The core microbiome composed of a large fraction of the overall microbiome, ranging between three- and two-thirds of the relative abundance, depending on the farm (x axis). Bar plots represent the mean, and error bars represent the SE of the core relative abundance. (D) Core microbiome composition is highly correlated to noncore microbes, as shown by comparing the interanimal dissimilarity (Bray-Curtis) matrix based on core microbes to that based on noncore microbes. Violin plots for each farm (x axis) show the correlation between the two dissimilarity matrices (core and noncore; Mantel R), where the violin (gray) describes the null model (permuted) Mantel R values, and red points depict the actual R. (E) The core microbiome exhibits a clear hierarchical structure, in terms of microbial abundance, which agrees between farms. (i) A highly consistent core microbiome abundance pattern (ranking) across farms (x axis) was revealed by an abundance-ranked color-coded heatmap, where species-level microbial OTUs are ordered by their mean relative abundance across all animals in the cohort (no further clustering or normalization was performed). Color coding reflects the rank abundance of a given OTU in a given individual. (ii) Heatmap showing the degree of correlation in relative abundance profiles between the farms. Color coding reflects the degree of correlation in relative abundance profiles (Spearman r; all P < 0.001). (F) Phylogenetic distances between the core microbes were smaller, showing that they are closer phylogenetically, but also distinct, compared to the overall microbiome, as it was shown by mean pairwise phylogenetic distance (x axis) calculation between core (blue) and 1000 randomly selected noncore microbes (ochre) from the rumen (y axis; P < 0.001).

  • Fig. 2 Host genetics explains core microbiome composition with heritable microbes serving as hubs within the microbial interaction networks.

    The core microbiome is associated with animal genetics as (A) the variance in the core microbiome (y axis) was significantly explained by host genetics. CCA was performed between the matrix of the first 30 microbial (OTU table) principal component scores and host genotype principal component scores based on a common SNP. The analysis was accomplished for the largest Holstein farms in this study (x axis). (B) Heritability analysis based on the genetic relatedness matrix (GRM) showed 39 microbes (x axis) significantly correlating with the animal genotype. Heritability estimate—h2 (y axis; bar plots show mean estimate per microbe), and P values were calculated using genetics complex trait analysis (GCTA) software, followed by a multiple testing correction with Benjamini-Hochberg method. Confidence intervals (CIs; 95%) were estimated on the basis of heritability estimates and the GRM with Fast Confidence IntErvals using Stochastic Approximation (FIESTA) software. (C) Heritable microbes are central to the microbial interaction network, as revealed by the higher mean connectivity (y axis) of these microbes compared to the nonheritable ones. The interaction network was built using Sparse InversE Covariance estimation for Ecological Association and Statistical Inference (SpiecEasi). Results are presented as mean number of microbial interactions with SE. Indicated P values, *P < 0.05, **P < 0.005, ***P < 0.0005.

  • Fig. 3 Core rumen microbiome composition is linked to host traits and could significantly predict those traits.

    (A) Association analysis between microbes and host traits revealed 339 microbes associated with at least one trait. For a microbe to be associated with a given trait, it had to significantly and unidirectionally correlate with a trait within each of at least four farms (after Benjamini-Hochberg multiple testing correction) with no farm showing a significant correlation in the opposing direction. (B) Most of the trait-associated microbes are associated with rumen propionate and acetate. (C) Enrichment analysis, using Fisher exact test, showed that the core microbes are much more present (enriched) within trait-associated microbes compared to the noncore microbiome (P < 2.2 × 10−16). (D) Explained variation (r2) of different host traits as function of core microbiome composition. r2 estimates were derived from a machine learning approach where a trait value was predicted for a given animal using the Ridge regression that was constructed from other animals in the farm (leave-one-out k-fold regression). Thereafter, prediction r2 value was calculated between the vectors of observed and predicted trait values. Indicated host traits were significantly explained (via prediction) by core microbe (OTU) abundance profiles. Dots stand for individual farms’ prediction r2, while bar heights represent mean of individual farms’ r2. DMI, dry matter intake; ECM, energy-corrected milk; NDF, neutral-detergent fiber; DM, dry matter; BHB, β-hydroxybutyrate.

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/5/7/eaav8391/DC1

    Supplementary Materials and Methods

    Supplementary Text. Interactions between main categories of ruminal microbes in abundance, diversity, and animal phenotype.

    Fig. S1. Rank abundance plot for core microbes along farms.

    Fig. S2. Overview of genetic components along the Holstein cohort and host SNP-microbe association effort.

    Fig. S3. Microbial species interaction within and between domains.

    Fig. S4. Species richness and abundance of rumen microbial domains reveal ecological interactions and connection to host traits.

    Fig. S5. Host genetics, core microbiome composition, and diet shape the host phenotypic landscape.

    Fig. S6. Heritable microbes tend to explain experimental variables better in comparison to nonheritable core microbes.

    Fig. S7. Explained variation (r2) of different host traits as function of core microbiome composition, according to RF prediction model.

    Fig. S8. The vast majority of core microbes do not show a seasonal association, and evidence for seasonality usually does not repeat in more than one farm.

    Table S1. Average diet formulations and composition on each farm.

    Table S2. Conditions for quantitative PCR.

    Data S1. Animals used in the experiment together with diet, measured phenotypes, and other experimental variables.

    Data S2. Presence of bacterial taxonomic groups that were found to be most abundant in Henderson et al. (6) and appear also in the current study.

    Data S3. Presence of archaeal taxonomic groups that were found to be most abundant in Henderson et al. (6) and appear also in the present study.

    Data S4. Presence of protozoal taxonomic groups that were found to be most abundant in Henderson et al. (6) and appear also in the present study.

    Data S5. Summary of abundance and occupancy of the core microbial species (prokaryotes, fungi, and protozoa).

    Data S6. Heritable microbes.

    Data S7. Microbes associated with phenotypic traits.

    Data S8. Closest representative sequenced genomes for heritable microbes.

    Data S9. Season-affected microbes.

    Data S10. Animal genotypes (SNP values).

    References (6770)

  • Supplementary Materials

    The PDF file includes:

    • Supplementary Materials and Methods
    • Supplementary Text. Interactions between main categories of ruminal microbes in abundance, diversity, and animal phenotype.
    • Fig. S1. Rank abundance plot for core microbes along farms.
    • Fig. S2. Overview of genetic components along the Holstein cohort and host SNP-microbe association effort.
    • Fig. S3. Microbial species interaction within and between domains.
    • Fig. S4. Species richness and abundance of rumen microbial domains reveal ecological interactions and connection to host traits.
    • Fig. S5. Host genetics, core microbiome composition, and diet shape the host phenotypic landscape.
    • Fig. S6. Heritable microbes tend to explain experimental variables better in comparison to nonheritable core microbes.
    • Fig. S7. Explained variation (r2) of different host traits as function of core microbiome composition, according to RF prediction model.
    • Fig. S8. The vast majority of core microbes do not show a seasonal association, and evidence for seasonality usually does not repeat in more than one farm.
    • Table S1. Average diet formulations and composition on each farm.
    • Table S2. Conditions for quantitative PCR.
    • Legends for data S1 to S10
    • References (6770)

    Download PDF

    Other Supplementary Material for this manuscript includes the following:

    • Data S1 (Microsoft Excel format). Animals used in the experiment together with diet, measured phenotypes, and other experimental variables.
    • Data S2 (Microsoft Word format). Presence of bacterial taxonomic groups that were found to be most abundant in Henderson et al. (6) and appear also in the current study.
    • Data S3 (Microsoft Word format). Presence of archaeal taxonomic groups that were found to be most abundant in Henderson et al. (6) and appear also in the present study.
    • Data S4 (Microsoft Word format). Presence of protozoal taxonomic groups that were found to be most abundant in Henderson et al. (6) and appear also in the present study.
    • Data S5 (Microsoft Excel format). Summary of abundance and occupancy of the core microbial species (prokaryotes, fungi, and protozoa).
    • Data S6 (Microsoft Excel format). Heritable microbes.
    • Data S7 (Microsoft Excel format). Microbes associated with phenotypic traits.
    • Data S8 (Microsoft Excel format). Closest representative sequenced genomes for heritable microbes.
    • Data S9 (Microsoft Excel format). Season-affected microbes.
    • Data S10 (.zip format). Animal genotypes (SNP values).

    Files in this Data Supplement:

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