Two Different Bacterial Community Types Are Linked with the Low-Methane Emission Trait in Sheep

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.

Design, implementation and interpretation of in vitro batch culture experiments to assess enteric methane mitigation in ruminants—a review

“…Such variation has been associated, among other factors, with differences in the rumen microbiome associated with between-animal variation in passage rates, rumen volume and morphology, eating behaviour, etc. (Kittelmann et al, 2014). Martínez et al (2010) observed consistent differences in CH 4 production and H 2 recovery in vitro during incubations with rumen liquor collected from 6 different sheep fed the same diet.…”

Rumen prokaryotic communities of ruminants under different feeding paradigms on the Qinghai-Tibetan Plateau

“…The diet and feeding pattern are recognized as the key factors affecting rumen efficiency and the rumen microbial community composition [88]. Consequently, according to previous studies [9,33,35], it was speculated that differences in rumen microbial communities in yaks and Tibetan sheep under different feeding paradigms could cause variations in CH 4 formation and the conversion of feed to animal products. Consequently, a deep understanding of rumen microbial composition and variation is essential not only for developing appropriate feeding and management strategies for enhancing health and productivity of yaks and Tibetan sheep, but also for reducing CH 4 emission from ruminants on the QTP.…”

Natural variation in methane emission of sheep fed on a lucerne pellet diet is unrelated to rumen ciliate community type

“…The highest and lowest CH 4 -emitting animals within each separate cohort, based on their 4 day mean CH 4 yields (i.e. the mean of both rounds), were identified and a total of 236 samples from 118 animals were analysed for rumen ciliate community structure as described previously (Kittelmann et al, 2014). Briefly, nucleic acids were extracted from 30 mg freeze-dried and homogenized rumen content samples using a combined bead-beating, phenol/chloroform and column purification protocol (Rius et al, 2012).…”

“…Briefly, nucleic acids were extracted from 30 mg freeze-dried and homogenized rumen content samples using a combined bead-beating, phenol/chloroform and column purification protocol (Rius et al, 2012). Rumen ciliate 18S rRNA genes were amplified using barcoded primers RP841F (Kittelmann & Janssen, 2011) and Reg1302R (Regensbogenova et al, 2004) and prepared for 454 Titanium pyrosequencing at the Center for Genome Sciences and Systems Biology, Washington University of St Louis, USA, according to Kittelmann et al (2014). Sequence data have been deposited in the EMBL database under the study accession number ERP003772.…”

“…Recently, validation of next-generation sequencing against microscopy for comparative ciliate community structure analysis has enabled simultaneous analysis of ciliate communities in hundreds of samples (Kittelmann et al, 2015). Using this method, we previously reported that the relative abundances of individual genera of rumen ciliates are not significantly correlated with CH 4 yields of sheep feeding on lucerne pellets (Kittelmann et al, 2014). However, it remained to be elucidated whether the analysed samples could be classified into ciliate community types based on relative abundance data stemming from next-generation amplicon sequencing, and if the different ciliate community types that naturally occur in vivo were linked to significantly different CH 4 yields from sheep feeding on lucerne pellets.…”