Dietary selection of metabolically distinct microorganisms drives hydrogen metabolism in ruminants

产甲烷 瘤胃 生物 细菌 食品科学 生物化学 微生物 氢化酶 古细菌 产甲烷菌 广域古菌界 淀粉 甲烷 新陈代谢 微生物学 发酵 生态学 遗传学
作者
Qiu Shuang Li,Rong Wang,Zhiyuan Ma,Xiu Min Zhang,Jinzhen Jiao,Zhi Gang Zhang,Emilio M. Ungerfeld,Kang Le Yi,Bai Zhong Zhang,Long Liang,Yun Long,Ye Tao,Tao Huang,Chris Greening,Zhi Liang Tan,Min Wang
出处
期刊:The ISME Journal [Springer Nature]
卷期号:16 (11): 2535-2546 被引量:66
标识
DOI:10.1038/s41396-022-01294-9
摘要

Abstract Ruminants are important for global food security but emit the greenhouse gas methane. Rumen microorganisms break down complex carbohydrates to produce volatile fatty acids and molecular hydrogen. This hydrogen is mainly converted into methane by archaea, but can also be used by hydrogenotrophic acetogenic and respiratory bacteria to produce useful metabolites. A better mechanistic understanding is needed on how dietary carbohydrates influence hydrogen metabolism and methanogenesis. We profiled the composition, metabolic pathways, and activities of rumen microbiota in 24 beef cattle adapted to either fiber-rich or starch-rich diets. The fiber-rich diet selected for fibrolytic bacteria and methanogens resulting in increased fiber utilization, while the starch-rich diet selected for amylolytic bacteria and lactate utilizers, allowing the maintenance of a healthy rumen and decreasing methane production (p < 0.05). Furthermore, the fiber-rich diet enriched for hydrogenotrophic methanogens and acetogens leading to increased electron-bifurcating [FeFe]-hydrogenases, methanogenic [NiFe]- and [Fe]-hydrogenases and acetyl-CoA synthase, with lower dissolved hydrogen (42%, p < 0.001). In contrast, the starch-rich diet enriched for respiratory hydrogenotrophs with greater hydrogen-producing group B [FeFe]-hydrogenases and respiratory group 1d [NiFe]-hydrogenases. Parallel in vitro experiments showed that the fiber-rich selected microbiome enhanced acetate and butyrate production while decreasing methane production (p < 0.05), suggesting that the enriched hydrogenotrophic acetogens converted some hydrogen that would otherwise be used by methanogenesis. These insights into hydrogen metabolism and methanogenesis improve understanding of energy harvesting strategies, healthy rumen maintenance, and methane mitigation in ruminants.

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