Bovine Host Genetic Variation Influences Rumen Microbial Methane Production with Best Selection Criterion for Low Methane Emitting and Efficiently Feed Converting Hosts Based on Metagenomic Gene Abundance

Methane produced by methanogenic archaea in ruminants contributes significantly to anthropogenic greenhouse gas emissions. The host genetic link controlling microbial methane production is unknown and appropriate genetic selection strategies are not developed. We used sire progeny group differences to estimate the host genetic influence on rumen microbial methane production in a factorial experiment consisting of crossbred breed types and diets. Rumen metagenomic profiling was undertaken to investigate links between microbial genes and methane emissions or feed conversion efficiency. Sire progeny groups differed significantly in their methane emissions measured in respiration chambers. Ranking of the sire progeny groups based on methane emissions or relative archaeal abundance was consistent overall and within diet, suggesting that archaeal abundance in ruminal digesta is under host genetic control and can be used to genetically select animals without measuring methane directly. In the metagenomic analysis of rumen contents, we identified 3970 microbial genes of which 20 and 49 genes were significantly associated with methane emissions and feed conversion efficiency respectively. These explained 81% and 86% of the respective variation and were clustered in distinct functional gene networks. Methanogenesis genes (e.g. mcrA and fmdB) were associated with methane emissions, whilst host-microbiome cross talk genes (e.g. TSTA3 and FucI) were associated with feed conversion efficiency. These results strengthen the idea that the host animal controls its own microbiota to a significant extent and open up the implementation of effective breeding strategies using rumen microbial gene abundance as a predictor for difficult-to-measure traits on a large number of hosts. Generally, the results provide a proof of principle to use the relative abundance of microbial genes in the gastrointestinal tract of different species to predict their influence on traits e.g. human metabolism, health and behaviour, as well as to understand the genetic link between host and microbiome.

反刍动物中产甲烷古菌（methanogenic archaea）产生的甲烷，对人为温室气体排放具有显著贡献。目前，调控微生物甲烷生成的宿主遗传关联尚不明确，适配的遗传选育策略也尚未建立。本研究借助包含杂交品种类型与日粮的析因试验，利用父系后代组间差异，评估宿主遗传对瘤胃微生物甲烷生成的影响。本研究开展瘤胃宏基因组分析（metagenomic profiling），以探究微生物基因与甲烷排放、饲料转化效率之间的关联。父系后代组在呼吸测热室中测得的甲烷排放水平存在显著差异。基于甲烷排放或古菌相对丰度的父系后代组排名，在整体水平与各日粮组内均保持一致，这表明瘤胃内容物（ruminal digesta）中的古菌丰度受宿主遗传调控，且可用于无需直接测量甲烷的动物遗传选育。在瘤胃内容物的宏基因组分析中，我们共鉴定出3970个微生物基因，其中分别有20个、49个基因与甲烷排放、饲料转化效率显著相关。这些基因分别解释了对应性状81%、86%的表型变异，并聚集于不同的功能基因网络中。产甲烷功能基因（如mcrA与fmdB）与甲烷排放相关，而宿主-微生物组互作（host-microbiome cross talk）基因（如TSTA3与FucI）则与饲料转化效率相关。上述研究结果进一步证实，宿主动物可在较大程度上调控自身菌群，并为以瘤胃微生物基因丰度作为难测性状的预测指标、开展大规模宿主遗传选育提供了可行路径。总体而言，本研究为利用不同物种胃肠道内微生物基因的相对丰度，预测其对宿主性状（如人类代谢、健康与行为）的影响，以及解析宿主与微生物组之间的遗传关联，提供了原理性验证依据。