Rumen metagenome and metatranscriptome analyses of low methane yield sheep reveals a Sharpea-enriched microbiome characterised by lactic acid formation and utilisation.

Janine Kamke,Siva Ganesh,Jeff Froula,Edward M Rubin,Priya Soni,Graeme T Attwood,Yang Li,Michael Tavendale,Weibing Shi,Peter H Janssen,Sandra Kittelmann

doi:10.1186/s40168-016-0201-2

Janine Kamke, Siva Ganesh + Show 9 more

Open Access

https://doi.org/10.1186/s40168-016-0201-2

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Abstract

BackgroundEnteric fermentation by farmed ruminant animals is a major source of methane and constitutes the second largest anthropogenic contributor to global warming. Reducing methane emissions from ruminants is needed to ensure sustainable animal production in the future. Methane yield varies naturally in sheep and is a heritable trait that can be used to select animals that yield less methane per unit of feed eaten. We previously demonstrated elevated expression of hydrogenotrophic methanogenesis pathway genes of methanogenic archaea in the rumens of high methane yield (HMY) sheep compared to their low methane yield (LMY) counterparts. Methane production in the rumen is strongly connected to microbial hydrogen production through fermentation processes. In this study, we investigate the contribution that rumen bacteria make to methane yield phenotypes in sheep.ResultsUsing deep sequence metagenome and metatranscriptome datasets in combination with 16S rRNA gene amplicon sequencing from HMY and LMY sheep, we show enrichment of lactate-producing Sharpea spp. in LMY sheep bacterial communities. Increased gene and transcript abundances for sugar import and utilisation and production of lactate, propionate and butyrate were also observed in LMY animals. Sharpea azabuensis and Megasphaera spp. act as important drivers of lactate production and utilisation according to phylogenetic analysis and read mappings.ConclusionsOur findings show that the rumen microbiome in LMY animals supports a rapid heterofermentative growth, leading to lactate production. We postulate that lactate is subsequently metabolised mainly to butyrate in LMY animals, producing 2 mol of hydrogen and 0.5 mol of methane per mol hexose, which represents 24 % less than the 0.66 mol of methane formed from the 2.66 mol of hydrogen produced if hexose fermentation was directly to acetate and butyrate. These findings are consistent with the theory that a smaller rumen size with a higher turnover rate, where rapid heterofermentative growth would be an advantage, results in lower hydrogen production and lower methane formation. Together with previous methanogen gene expression data, this builds a strong concept of how animal traits and microbial communities shape the methane phenotype in sheep.Electronic supplementary materialThe online version of this article (doi:10.1186/s40168-016-0201-2) contains supplementary material, which is available to authorized users.

Highlights

Enteric fermentation by farmed ruminant animals is a major source of methane and constitutes the second largest anthropogenic contributor to global warming
Microbial community composition of high methane yield (HMY) and low methane yield (LMY) animals At a threshold >0.2 % relative abundance, 70 bacterial taxa (97 % sequence similarity) were recovered from the Animal measurements An overview of the analyses of methane emissions, pH, fermentation acids, 16S ribosomal ribonucleic acid (rRNA) gene amplicon sequencing and metagenome/metatranscriptome sequencing is provided in Additional file 1: Table S1
The most notable were Sharpea sp. and S. azabuensis, which were more abundant in LMY animals based on both amplicon and metagenome datasets, making up 6.3 and 7.5 % of the bacterial 16S rRNA gene reads from the LMY animals, respectively

Summary

Introduction

Enteric fermentation by farmed ruminant animals is a major source of methane and constitutes the second largest anthropogenic contributor to global warming. We previously demonstrated elevated expression of hydrogenotrophic methanogenesis pathway genes of methanogenic archaea in the rumens of high methane yield (HMY) sheep compared to their low methane yield (LMY) counterparts. A third of all methane emissions derived from human-related activities are from enteric fermentation in livestock [2] and are emitted mostly from ruminant animals. Animal breeding has been used for many years to select for desirable production traits in ruminant livestock, and breeding low methane emitting animals is being investigated [3,4,5,6]. The methane yield trait is heritable, and feed particle retention time [7, 8] and rumen volume [3] are thought to contribute to the phenotype. It was reported that the main difference between rumen methanogen communities from rumen samples of LMY and HMY sheep was the differentially higher expression of genes involved in the hydrogenotrophic methanogenesis pathway in HMY sheep [9]

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