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

Alejandro Belanche,Alison H Kingston-Smith,Charles J Newbold,Gareth W Griffith

doi:10.3389/fmicb.2019.00122

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.

Highlights

Rumen bacteria, archaea, anaerobic fungi, protozoa and phages make up the complex microbial ecosystem which enables ruminants to efficiently utilize forage
This community was formed by 35 dominant genera including Prevotella, Sporobacter, Ruminococcus, Anaeroplasma, Treponema, Ruminobacter, Succinivibrio, Fibrobacter, Selenomonas, representing 20% of the bacterial community
Our study found that diet-specific core communities were small in size (

Summary

Introduction

Archaea, anaerobic fungi, protozoa and phages make up the complex microbial ecosystem which enables ruminants to efficiently utilize forage. This multi-kingdom rumen microbiota has been described as “the most elegant and highly evolved cellulose-digesting system in nature” (Weimer et al, 2009). Fresh grass has traditionally been a major feedstuff for ruminants and grazing systems generally have a positive perception in society in terms of animal well-being (Somers et al, 2005). In the context of growing demand for animal products, modern ruminant production systems based on large scale farms tend to replace fresh pastures with preserved forages, such as hay, supplemented with concentrate feeds during certain periods of the year when the grass is unavailable (e.g., winter time) or when a greater control of the diet is required (e.g., lactation period). The decision “to graze or not to graze” is often arbitrary without taking into consideration the impact on the rumen microbiota, feed efficiency and on the environment (Pol-van Dasselaar et al, 2008)

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