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Cited by 142Ruminant Nutrition and Digestive PhysiologyAnaerobic Digestion and Biogas ProductionGut microbiota and health

Dietary selection of metabolically distinct microorganisms drives hydrogen metabolism in ruminants

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Li, Qiu Shuang, Wang, Rong, Ma, Zhi Yuan, Zhang, Xiu Min, Jiao, Jin Zhen, Zhang, Zhi Gang, Ungerfeld, Emilio M, Le Yi, Kang +8 more·2022·The ISME Journal
DOI 10.1038/s41396-022-01294-9PMC PMC9562222
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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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  • The increased acetate production and decreased methane production by the fiber-selected microbiome can be attributed to a greater community of reductive acetogens.

    “Inoculation with fiber-selected microbiome showed the paradoxically increased acetate production with decreased methane production than starch-selected microbiome, and could be attributed to the greater community of reductive acetogens [41].”

    From Reductive acetogenesis is a dominant process in the ruminant hindgut (2025) · cites this paper as [41]

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Authors
Li, Q. S., Wang, R., Ma, Z. Y., Zhang, X. M., Jiao, J. Z., Zhang, Z. G., Ungerfeld, E. M., Le Yi, K., Zhang, B. Z., Long, L., Long, Y., Tao, Y., Huang, T., Greening, C., Tan, Z. L., & Wang, M.
Affiliations
  • Chinese Academy of Sciences (CN)
  • Lanzhou University (CN)
  • Key Laboratory for Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences , Changsha, Hunan, China
  • Yunnan University (CN)
  • Instituto de Investigaciones Agropecuarias (CL)
  • Hunan Institute of Animal and Veterinary Science , Changsha, Hunan, China
  • Xiangxi Cattle Engineering Technology Center of Hunan Province , Huayuan, Hunan, China
  • Shanghai Biozeron Biotechnology Co., Ltd (China) (CN)
  • Monash University (AU)
Corresponding author
  • Tan, Zhi Liang
  • Wang, Min
ORCID
Venue
The ISME Journal
Publisher
Oxford University Press (OUP)
Published
2022-08-05
Volume
16
Issue
11
Pages
2535-2546
ISSN
  • 1751-7362 (ISSN-L)
  • 1751-7370
DOI
10.1038/s41396-022-01294-9
PMC
PMC9562222
OpenAlex
W4289860943
Cited by
142
References
1
Citations by year
2026: 42 · 2025: 46 · 2024: 36 · 2023: 15 · 2022: 3
FWCI
26.53
Type
journal article
Language
en
Open access
Licence
Locations
  • The ISME Journal (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • National Natural Science Foundation of China (31922080, 32002204, 31922080, 32002204, APP1178715)
  • Chinese Academy of Sciences (XDA26040203)
  • Youth Innovation Promotion Association of the Chinese Academy of Sciences (Y202078)
  • National Health and Medical Research Council (1178715)
  • Youth Innovation Promotion Association
Topics
  • Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Ruminant Nutrition and Digestive Physiology
  • Physical Sciences › Engineering › Building and Construction › Anaerobic Digestion and Biogas Production
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Keywords
hydrogen metabolism, methanogenesis, rumen microbiota, dietary fiber, starch-rich diet, beef cattle, hydrogenotrophic methanogens, [FeFe]-hydrogenase, [NiFe] hydrogenase, acetyl-CoA synthase, volatile fatty acids, methane mitigation, rumen health, carbohydrate utilization
MeSH terms
Greenhouse Gases, Acetyl Coenzyme A, Animals, Bacteria, Butyrates, Cattle, Diet, Dietary Carbohydrates, Fatty Acids, Volatile, Fermentation, Hydrogen, Lactates, Methane, Rumen, Ruminants, Starch, Euryarchaeota

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