Reductive acetogenesis is a dominant process in the ruminant hindgut
Abstract Background The microbes residing in ruminant gastrointestinal tracts play a crucial role in converting plant biomass to volatile fatty acids, which serve as the primary energy source for ruminants. This gastrointestinal tract comprises a foregut (rumen) and hindgut (cecum and colon), which...
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BMC
2025-01-01
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| Online Access: | https://doi.org/10.1186/s40168-024-02018-1 |
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| author | Qiushuang Li Jiabin Huo Gaofeng Ni Fan Zhang Shizhe Zhang Xiumin Zhang Rong Wang Jinzhen Jiao Zhongtang Yu Xuanxuan Pu Yipeng Yue Emilio M. Ungerfeld Xiaoli Zhang Jian Wu Zhiliang Tan Chris Greening Min Wang |
| author_facet | Qiushuang Li Jiabin Huo Gaofeng Ni Fan Zhang Shizhe Zhang Xiumin Zhang Rong Wang Jinzhen Jiao Zhongtang Yu Xuanxuan Pu Yipeng Yue Emilio M. Ungerfeld Xiaoli Zhang Jian Wu Zhiliang Tan Chris Greening Min Wang |
| author_sort | Qiushuang Li |
| collection | DOAJ |
| description | Abstract Background The microbes residing in ruminant gastrointestinal tracts play a crucial role in converting plant biomass to volatile fatty acids, which serve as the primary energy source for ruminants. This gastrointestinal tract comprises a foregut (rumen) and hindgut (cecum and colon), which differ in structures and functions, particularly with respect to feed digestion and fermentation. While the rumen microbiome has been extensively studied, the cecal microbiome remains much less investigated and understood, especially concerning the assembling microbial communities and overriding pathways of hydrogen metabolism. Results To address this gap, we comparatively investigated the composition, capabilities, and activities of the rumen and the cecum microbiome using goats as an experimental ruminant model. In situ measurements showed significantly higher levels of dissolved hydrogen and acetate in the cecum than in the rumen. Increased dissolved hydrogen indicated distinct processes and reduced coupling between fermentative H2 production and utilization, whereas higher levels of acetate could be caused by slower VFA absorption through cecal papillae than through the rumen papillae. Microbial profiling indicated that the cecum harbors a greater abundance of mucin-degrading microbes and fermentative hydrogen producers, whereas the rumen contains a higher abundance of fibrolytic fermentative bacteria, hydrogenotrophic respiratory bacteria, and methanogenic archaea. Most strikingly, reductive acetogenic bacteria were 12-fold more abundant in the cecum. Genome-resolved metagenomic analysis unveiled that the cecum acetogens are both phylogenetically and functionally distinct from those found in the rumen. Further supporting these findings, two in vitro experiments demonstrated a marked difference in hydrogen metabolism pathways between the cecum and the rumen, with increased acetate production and reduced methanogenesis in the cecum. Moreover, comparative analysis across multiple ruminant species confirmed a strong enrichment of reductive acetogens in the hindguts, suggesting a conserved functional role. Conclusions These findings highlight an enrichment of acetogenesis in a key region of the gastrointestinal tract and reshape our understanding of ruminant hydrogen metabolism and how the H2 can be managed in accord to livestock methane mitigation efforts. Video Abstract |
| format | Article |
| id | doaj-art-390ddb05a0b44aadade80f2f8a450f62 |
| institution | Kabale University |
| issn | 2049-2618 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj-art-390ddb05a0b44aadade80f2f8a450f622025-02-02T12:33:52ZengBMCMicrobiome2049-26182025-01-0113111510.1186/s40168-024-02018-1Reductive acetogenesis is a dominant process in the ruminant hindgutQiushuang Li0Jiabin Huo1Gaofeng Ni2Fan Zhang3Shizhe Zhang4Xiumin Zhang5Rong Wang6Jinzhen Jiao7Zhongtang Yu8Xuanxuan Pu9Yipeng Yue10Emilio M. Ungerfeld11Xiaoli Zhang12Jian Wu13Zhiliang Tan14Chris Greening15Min Wang16Key Laboratory for Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of SciencesKey Laboratory for Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of SciencesBiomedicine Discovery Institute, Department of Microbiology, Monash UniversityKey Laboratory for Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of SciencesKey Laboratory for Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of SciencesKey Laboratory for Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of SciencesKey Laboratory for Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of SciencesKey Laboratory for Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of SciencesDepartment of Animal Sciences, The Ohio State UniversityKey Laboratory for Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of SciencesKey Laboratory for Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of SciencesCentro Regional de Investigación Carillanca, Instituto de Investigaciones Agropecuarias (INIA)Key Laboratory for Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of SciencesKey Laboratory for Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of SciencesKey Laboratory for Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of SciencesBiomedicine Discovery Institute, Department of Microbiology, Monash UniversityKey Laboratory for Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of SciencesAbstract Background The microbes residing in ruminant gastrointestinal tracts play a crucial role in converting plant biomass to volatile fatty acids, which serve as the primary energy source for ruminants. This gastrointestinal tract comprises a foregut (rumen) and hindgut (cecum and colon), which differ in structures and functions, particularly with respect to feed digestion and fermentation. While the rumen microbiome has been extensively studied, the cecal microbiome remains much less investigated and understood, especially concerning the assembling microbial communities and overriding pathways of hydrogen metabolism. Results To address this gap, we comparatively investigated the composition, capabilities, and activities of the rumen and the cecum microbiome using goats as an experimental ruminant model. In situ measurements showed significantly higher levels of dissolved hydrogen and acetate in the cecum than in the rumen. Increased dissolved hydrogen indicated distinct processes and reduced coupling between fermentative H2 production and utilization, whereas higher levels of acetate could be caused by slower VFA absorption through cecal papillae than through the rumen papillae. Microbial profiling indicated that the cecum harbors a greater abundance of mucin-degrading microbes and fermentative hydrogen producers, whereas the rumen contains a higher abundance of fibrolytic fermentative bacteria, hydrogenotrophic respiratory bacteria, and methanogenic archaea. Most strikingly, reductive acetogenic bacteria were 12-fold more abundant in the cecum. Genome-resolved metagenomic analysis unveiled that the cecum acetogens are both phylogenetically and functionally distinct from those found in the rumen. Further supporting these findings, two in vitro experiments demonstrated a marked difference in hydrogen metabolism pathways between the cecum and the rumen, with increased acetate production and reduced methanogenesis in the cecum. Moreover, comparative analysis across multiple ruminant species confirmed a strong enrichment of reductive acetogens in the hindguts, suggesting a conserved functional role. Conclusions These findings highlight an enrichment of acetogenesis in a key region of the gastrointestinal tract and reshape our understanding of ruminant hydrogen metabolism and how the H2 can be managed in accord to livestock methane mitigation efforts. Video Abstracthttps://doi.org/10.1186/s40168-024-02018-1Molecular hydrogenFermentation pathwayHydrogenaseAcetogensMethanogenesis |
| spellingShingle | Qiushuang Li Jiabin Huo Gaofeng Ni Fan Zhang Shizhe Zhang Xiumin Zhang Rong Wang Jinzhen Jiao Zhongtang Yu Xuanxuan Pu Yipeng Yue Emilio M. Ungerfeld Xiaoli Zhang Jian Wu Zhiliang Tan Chris Greening Min Wang Reductive acetogenesis is a dominant process in the ruminant hindgut Microbiome Molecular hydrogen Fermentation pathway Hydrogenase Acetogens Methanogenesis |
| title | Reductive acetogenesis is a dominant process in the ruminant hindgut |
| title_full | Reductive acetogenesis is a dominant process in the ruminant hindgut |
| title_fullStr | Reductive acetogenesis is a dominant process in the ruminant hindgut |
| title_full_unstemmed | Reductive acetogenesis is a dominant process in the ruminant hindgut |
| title_short | Reductive acetogenesis is a dominant process in the ruminant hindgut |
| title_sort | reductive acetogenesis is a dominant process in the ruminant hindgut |
| topic | Molecular hydrogen Fermentation pathway Hydrogenase Acetogens Methanogenesis |
| url | https://doi.org/10.1186/s40168-024-02018-1 |
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