Host-rumen microbiome interactions and influences on feed conversion efficiency (FCE), methane production and other productivity traits


The rumen microbiome has the important task of supplying ruminants with most of their dietary requirements and is responsible for providing them with up to 70% of their metabolic needs and protein supply (Siciliano-Jones and Murphy, 1989; Bergman, 1990). This tremendous feat is possible due to the large diversity of microorganisms in the rumen, operating on different trophic levels (Flint et al„ 2008; Morais and Mizrahi, 2019a,b). As such, ruminants are considered the hallmark of obligatory host-microbe interactions. The notion that differences in microbial composition could affect the animals' physiology, efficiency and waste output, has been suggested for the past 70 years of ruminant research, much earlier than the development of high throughput technology, which allowed researchers in the past decade to establish such a link (Krause et al., 2003). Hungate, in his seminal book The Rumen and Its Microbes (Hungate, 2013), suggested that a modulation of the microbial community toward improving fiber digestion may represent an avenue for increased productivity. Indeed the early works regarding the rumen microbiome largely focused on a subset of cultivable bacteria for which improved function was © Burleigh Dodds Science Publishing Limited. 2020. All rights reserved.

thought to increase animal productivity (Krause et al., 2003). However, these early attempts at modifying the rumen microbial composition toward improved efficiency have mostly failed to sustain a desired phenotype (Attwood et al., 1988; Flint et al., 1989; Wallace and Walker, 1993; Miyagi et al., 1995; Krause et al„ 1999, 2003). It has been pointed out that, in order to achieve this goal, one has to first understand the role of each component of the microbiome and its effect on the overall microbial community and the host.

Today, with our ability to assess the composition of the rumen microbial community as a whole, a new holistic view of the microbiome has emerged, whereby application of basic ecological principles on the overall microbiome structure and the physiological response of the host can be studied. This will lead us to an increased understanding of the role of the microbiome and its components on production efficiency, health and waste emissions such as methane. This chapter focuses on the recent discovery about the role of the ruminant microbiome on energy harvest, methane emission and the potential genetic factors determining its microbial composition and selection.

Core community, resilience and natural variation in rumen microbiome composition

2.1 Core community

Identifying common microbial features can lead to an understanding of the more basic requirements of the rumen ecosystem as they likely serve key functions in rumen metabolism. Several independent studies recognize the existence of a core microbial community in the rumen shared between and within ruminant lineages (Jami and Mizrahi, 2012a; Henderson et al., 2015). A comprehensive analysis of the microbiome of 32 ruminant and pseudoruminant species (Henderson et al., 2015) emphasized the shared and divergent nature of the rumen microbiome composition across a wide geographical range, animal lineages and management conditions (Henderson et al„ 2015). The authors identified a core community of taxa at the genus and species level, shared across different ruminant animal lineages. These include Prevotella, the most dominant genus in the rumen, Butyrivibrio and Ruminococcus, which harbor the main cellulolytic species in the rumen, as well as unclassified Lachnospiraceae, Ruminococcaceae, Clostridiales (all Firmicutes) and Bacteroidales (Bacteroidetes) for bacteria. The bovine rumen was also shown to be particularly enriched with Fibrobacter, an important cellulolytic species, shown to be most abundant in cattle-fed high-forage diet (Henderson et al., 2015). The members of the Methanobrevibacter gottschalkii and Methanobrevibacter ruminantium clades represent the core methanogenic community observed in the rumen (Henderson et al., 2015). This shared presence of bacterial taxa across different foregut animal lineages suggests that the core taxa have a key role in rumen metabolism and function (Shade and Handelsman, 2012). This suggestion is reinforced by the recent observation that species defined as core are more associated with physiological traits of the host in dairy cattle (Li et al., 2019; Wallace et al., 2019).

2.2 Variation

In all model animalstested, including ruminants, inter-individual variation in both microbial composition and abundance exists between animals despite stringent account for external factors such as housing, management and diet (Brule et al., 2009; Jami and Mizrahi, 2012a; Henderson et al., 2015). Brule et al. (2009) conducted a pioneering study characterizing the rumen microbial composition using shotgun metagenomics sequencing and showed broad differences in the community composition of three steers. One of the steers exhibited a different composition compared with the other two steers despite being under the same diet. Similarly, the characterization of 16 dairy cows under the same diet and management condition exhibited a 0.51 average pairwise similarity using the Bray-Curtis index, which takes into account the presence, and abundance of taxa. Some genera appeared to be relatively stable in terms of presence and abundance while others can exhibit up to two orders of magnitude differences in abundance between the cows (Jami and Mizrahi, 2012a,b).

2.3 Resilience

While studies have consistently pointed out that samples taken from different host animals can exhibit high variation in composition (Brule et al., 2009; Li et al., 2009; Jami and Mizrahi, 2012a), microbiome assessment across different sampling time points within the same cow reveals a remarkable stability (Li et al., 2009; Welkie et al., 2009). In a study using automated ribosomal intergenic spacer analysis (ARISA) to examine the changes in ruminal bacterial communities during the feeding cycle, similar observations were made, emphasizing both the stability of the rumen microbial community when established within a cow and the large differences in composition between different cows (Welkie et al., 2009). In steers, long-term temporal assessment of the changes in microbiome composition after dietary change revealed that, after 25 days on a new diet, the microbiome shows little variation hereafter (Snelling et al., 2019). The microbiome is resilient to such an extent that even large perturbations, such as transfaunation, where the rumen fluid of one cow is almost completely replaced with the rumen fluid of another, showed that within just a few weeks, rumen microbiome content reverted to a composition more closely resembling the original (Weimer et al., 2017). This stresses that host factors may strongly influence microbial assembly. Recent studies show a connection between the individual animals' genetics and its respective microbiome, as well as heritability of some rumen microbiome components (Roehe et al., 2016; Li et al., 2016; Sasson et al., 2017; Wallace et al., 2019). A larger experiment showed that following transfaunation, each individual cow exhibited unique patterns of reestablishment further strengthening the possibility of large host effect on the microbial community (Zhou et al., 2018).

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