Abstract

The potent greenhouse gas methane (CH4) is produced in the rumens of ruminant animals from hydrogen produced during microbial degradation of ingested feed. The natural animal-to-animal variation in the amount of CH4 emitted and the heritability of this trait offer a means for reducing CH4 emissions by selecting low-CH4 emitting animals for breeding. We demonstrate that differences in rumen microbial community structure are linked to high and low CH4 emissions in sheep. Bacterial community structures in 236 rumen samples from 118 high- and low-CH4 emitting sheep formed gradual transitions between three ruminotypes. Two of these (Q and S) were linked to significantly lower CH4 yields (14.4 and 13.6 g CH4/kg dry matter intake [DMI], respectively) than the third type (H; 15.9 g CH4/kg DMI; p<0.001). Low-CH4 ruminotype Q was associated with a significantly lower ruminal acetate to propionate ratio (3.7±0.4) than S (4.4±0.7; p<0.001) and H (4.3±0.5; p<0.001), and harbored high relative abundances of the propionate-producing Quinella ovalis. Low-CH4 ruminotype S was characterized by lactate- and succinate-producing Fibrobacter spp., Kandleria vitulina, Olsenella spp., Prevotella bryantii, and Sharpea azabuensis. High-CH4 ruminotype H had higher relative abundances of species belonging to Ruminococcus, other Ruminococcaceae, Lachnospiraceae, Catabacteriaceae, Coprococcus, other Clostridiales, Prevotella, other Bacteroidales, and Alphaproteobacteria, many of which are known to form significant amounts of hydrogen. We hypothesize that lower CH4 yields are the result of bacterial communities that ferment ingested feed to relatively less hydrogen, which results in less CH4 being formed.

Highlights

  • The forestomachs of ruminant animals contain a great diversity of prokaryotic and eukaryotic microorganisms that together break down and ferment the feed ingested by the host animal

  • CH4 is of no nutritional value to the animal, and is eructed and exhaled into the atmosphere, where it acts as a potent greenhouse gas

  • Measurements of CH4 emissions from individual sheep in highly-sensitive open-circuit respiration chambers showed that animals in the same flock, even though feeding on the same diet, varied significantly and consistently in their CH4 yields, measured in g CH4 per kg of dry matter intake (DMI; [10])

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Summary

Introduction

The forestomachs of ruminant animals contain a great diversity of prokaryotic and eukaryotic microorganisms that together break down and ferment the feed ingested by the host animal. To reduce CH4 emissions from enteric fermentation, and increase animal productivity, a number of different mitigation strategies have been tested, e.g., feed supplementation with lipids [3,4,5], inhibition of enzymes involved in CH4 formation [6,7], depletion of ciliate protozoa [8], or vaccination against methanogens (for a recent review see Wedlock et al [9]) Another potentially very effective way to reduce CH4 emissions from ruminant animals is to select naturally low-CH4 emitting animals for breeding and to avoid proliferation of high-CH4 emitting animals. We applied high-throughput barcoded 454 Titanium amplicon sequencing of bacterial, archaeal, and eukaryotic marker genes to determine correlations between rumen microbial community structure and CH4 yields of 60 high- and 58 low-emitting sheep

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