Abstract
Ruminants are significant contributors to the livestock generated component of the greenhouse gas, methane (CH4). The CH4 is primarily produced by the rumen microbes. Although the composition of the diet and animal intake amount have the largest effect on CH4 production and yield (CH4 production/dry matter intake, DMI), the host also influences CH4 yield. Shorter rumen feed mean retention time (MRT) is associated with higher dry matter intake and lower CH4 yield, but the molecular mechanism(s) by which the host affects CH4 production remain unclear. We integrated rumen wall transcriptome data and CH4 phenotypes from two independent experiments conducted with sheep in Australia (AUS, n = 62) and New Zealand (NZ, n = 24). The inclusion of the AUS data validated the previously identified clusters and gene sets representing rumen epithelial, metabolic and muscular functions. In addition, the expression of the cell cycle genes as a group was consistently positively correlated with acetate and butyrate concentrations (p < 0.05, based on AUS and NZ data together). The expression of a group of metabolic genes showed positive correlations in both AUS and NZ datasets with CH4 production (p < 0.05) and yield (p < 0.01). These genes encode key enzymes in the ketone body synthesis pathway and included members of the poorly characterized aldo-keto reductase 1C (AKR1C) family. Several AKR1C family genes appear to have ruminant specific evolution patterns, supporting their specialized roles in the ruminants. Combining differential gene expression in the rumen wall muscle of the shortest and longest MRT AUS animals (no data available for the NZ animals) with correlation and network analysis, we identified a set of rumen muscle genes involved in cell junctions as potential regulators of MRT, presumably by influencing contraction rates of the smooth muscle component of the rumen wall. Higher rumen expression of these genes, including SYNPO (synaptopodin, p < 0.01) and NEXN (nexilin, p < 0.05), was associated with lower CH4 yield in both AUS and NZ datasets. Unlike the metabolic genes, the variations in the expression of which may reflect the availability of rumen metabolites, the muscle genes are currently our best candidates for causal genes that influence CH4 yield.
Highlights
The growing global human population is resulting in increased demand for meat and fiber products from livestock
In this study we integrated and analyzed a sheep (n = 62) full thickness rumen wall transcriptome data set generated from an experiment conducted in the Australian data (AUS) dataset (Bond et al, 2017), with the previously described dataset from an independent experiment conducted in New Zealand (NZ) (n = 24) (Xiang et al, 2016a), the NZ dataset (Table 1)
We combined transcriptomic datasets from two completely independent experiments conducted in AUS and NZ, where feeding regime, animals, and CH4 phenotype are significantly different
Summary
The growing global human population is resulting in increased demand for meat and fiber products from livestock. While satisfying human demands, increasing ruminant numbers, including cattle and sheep, have resulted in emissions of increasing amounts of methane (CH4) (Pachauri et al, 2014). Ruminants are the major means of converting low quality/human-inedible cellulosic plant material to high value animal protein (Chalupa, 1978; Wilkinson and Lee, 2017). Increasing the production of high quality meat while reducing CH4 produced by herbivores has been one of the major aims of international collaborations in livestock research (Scollan et al, 2011). Mitigation of ruminant CH4 production offers the opportunity to increase feed energy utilization in the host animal while reducing environmental impact (Pickering et al, 2015)
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