A Multi-Kingdom Study Reveals the Plasticity of the Rumen Microbiota in Response to a Shift From Non-grazing to Grazing Diets in Sheep

Abstract

Increasing feed efficiency is a key target in ruminant science which requires a better understanding of rumen microbiota. This study investigated the effect of a shift from a non-grazing to a grazing diet on the rumen bacterial, methanogenic archaea, fungal, and protozoal communities. A systems biology approach based on a description of the community structure, core microbiota, network analysis, and taxon abundance linked to the rumen fermentation was used to explore the benefits of increasing depth of the community analysis. A total of 24 sheep were fed ryegrass hay supplemented with concentrate (CON) and subsequently ryegrass pasture (PAS) following a straight through experimental design. Results showed that concentrate supplementation in CON-fed animals (mainly starch) promoted a simplified rumen microbiota in terms of network density and bacterial, methanogen and fungal species richness which favored the proliferation of amylolytic microbes and VFA production (+48%), but led to a lower (ca. 4-fold) ammonia concentration making the N availability a limiting factor certain microbes. The adaptation process from the CON to the PAS diet consisted on an increase in the microbial concentration (biomass of bacteria, methanogens, and protozoa), diversity (+221, +3, and +21 OTUs for bacteria, methanogens, and fungi, respectively), microbial network complexity (+18 nodes and +86 edges) and in the abundance of key microbes involved in cellulolysis (Ruminococcus, Butyrivibrio, and Orpinomyces), proteolysis (Prevotella and Entodiniinae), lactate production (Streptococcus and Selenomonas), as well as methylotrophic archaea (Methanomassiliicoccaceae). This microbial adaptation indicated that pasture degradation is a complex process which requires a diverse consortium of microbes working together. The correlations between the abundance of microbial taxa and rumen fermentation parameters were not consistent across diets suggesting a metabolic plasticity which allowed microbes to adapt to different substrates and to shift their fermentation products. The core microbiota was composed of 34, 9, and 13 genera for bacteria, methanogens, and fungi, respectively, which were shared by all sheep, independent of diet. This systems biology approach adds a new dimension to our understanding of the rumen microbial interactions and may provide new clues to describe the mode of action of future nutritional interventions.

Keywords: core microbes; grazing; network analysis; rumen microbiota; taxa abundance.

Figure 1

(A) Venn diagrams describing the effect of the diet on the core microbial communities in the rumen. (B) Microbial network data describing the effect of the diet on the number of nodes, edges and microbial abundance in the rumen of sheep. Networks were generated based on those genera which positively or negatively correlated (r > 0.5 and adjusted-P < 0.05). CON, ryegrass hay diet supplemented with concentrate; PAS, ryegrass pasture.

Figure 2

(A) Canonical correspondence analysis illustrating the effect of the diet on the relationship between the structure of the bacterial community and the rumen fermentation. PERMANOVA indicating the effect of the diet based on the Bray-Curtis dissimilarity. (B) Effect of the diet on the abundance of the main bacterial taxa in sheep. CON, ryegrass hay supplemented with concentrate; PAS, ryegrass pasture.

Figure 3

(A) Canonical correspondence analysis illustrating the effect of the diet on the relationship between the structure of the methanogen community and the rumen fermentation. PERMANOVA indicating the effect of the diet based on the Bray-Curtis dissimilarity. (B) Effect of the diet on the abundance of the main methanogen taxa in sheep. CON, ryegrass hay supplemented with concentrate; PAS, ryegrass pasture.

Figure 4

(A) Canonical correspondence analysis illustrating the effect of the diet on the relationship between the structure of the fungal community and the rumen fermentation. PERMANOVA indicating the effect of the diet based on the Bray-Curtis dissimilarity. (B) Effect of the diet on the abundance of the main fungal taxa in sheep. CON, ryegrass hay supplemented with concentrate; PAS, ryegrass pasture.