Unraveling the phylogenomic diversity of Methanomassiliicoccales and implications for mitigating ruminant methane emissions
Abstract Background Methanomassiliicoccales are a recently identified order of methanogens that are diverse across global environments particularly the gastrointestinal tracts of animals; however, their metabolic capacities are defined via a limited number of cultured strains. Results Here, we profi...
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| Format: | Article |
| Language: | English |
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BMC
2024-01-01
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| Series: | Genome Biology |
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| Online Access: | https://doi.org/10.1186/s13059-024-03167-0 |
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| author | Fei Xie Shengwei Zhao Xiaoxiu Zhan Yang Zhou Yin Li Weiyun Zhu Phillip B. Pope Graeme T. Attwood Wei Jin Shengyong Mao |
| author_facet | Fei Xie Shengwei Zhao Xiaoxiu Zhan Yang Zhou Yin Li Weiyun Zhu Phillip B. Pope Graeme T. Attwood Wei Jin Shengyong Mao |
| author_sort | Fei Xie |
| collection | DOAJ |
| description | Abstract Background Methanomassiliicoccales are a recently identified order of methanogens that are diverse across global environments particularly the gastrointestinal tracts of animals; however, their metabolic capacities are defined via a limited number of cultured strains. Results Here, we profile and analyze 243 Methanomassiliicoccales genomes assembled from cultured representatives and uncultured metagenomes recovered from various biomes, including the gastrointestinal tracts of different animal species. Our analyses reveal the presence of numerous undefined genera and genetic variability in metabolic capabilities within Methanomassiliicoccales lineages, which is essential for adaptation to their ecological niches. In particular, gastrointestinal tract Methanomassiliicoccales demonstrate the presence of co-diversified members with their hosts over evolutionary timescales and likely originated in the natural environment. We highlight the presence of diverse clades of vitamin transporter BtuC proteins that distinguish Methanomassiliicoccales from other archaeal orders and likely provide a competitive advantage in efficiently handling B12. Furthermore, genome-centric metatranscriptomic analysis of ruminants with varying methane yields reveal elevated expression of select Methanomassiliicoccales genera in low methane animals and suggest that B12 exchanges could enable them to occupy ecological niches that possibly alter the direction of H2 utilization. Conclusions We provide a comprehensive and updated account of divergent Methanomassiliicoccales lineages, drawing from numerous uncultured genomes obtained from various habitats. We also highlight their unique metabolic capabilities involving B12, which could serve as promising targets for mitigating ruminant methane emissions by altering H2 flow. |
| first_indexed | 2024-03-07T15:29:21Z |
| format | Article |
| id | doaj.art-0adb2c8f322c46089d0c209e7f1e8bfd |
| institution | Directory Open Access Journal |
| issn | 1474-760X |
| language | English |
| last_indexed | 2024-03-07T15:29:21Z |
| publishDate | 2024-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Biology |
| spelling | doaj.art-0adb2c8f322c46089d0c209e7f1e8bfd2024-03-05T16:31:23ZengBMCGenome Biology1474-760X2024-01-0125113110.1186/s13059-024-03167-0Unraveling the phylogenomic diversity of Methanomassiliicoccales and implications for mitigating ruminant methane emissionsFei Xie0Shengwei Zhao1Xiaoxiu Zhan2Yang Zhou3Yin Li4Weiyun Zhu5Phillip B. Pope6Graeme T. Attwood7Wei Jin8Shengyong Mao9Ruminant Nutrition and Feed Engineering Technology Research Center, College of Animal Science and Technology, Nanjing Agricultural UniversityRuminant Nutrition and Feed Engineering Technology Research Center, College of Animal Science and Technology, Nanjing Agricultural UniversityRuminant Nutrition and Feed Engineering Technology Research Center, College of Animal Science and Technology, Nanjing Agricultural UniversityRuminant Nutrition and Feed Engineering Technology Research Center, College of Animal Science and Technology, Nanjing Agricultural UniversityRuminant Nutrition and Feed Engineering Technology Research Center, College of Animal Science and Technology, Nanjing Agricultural UniversityRuminant Nutrition and Feed Engineering Technology Research Center, College of Animal Science and Technology, Nanjing Agricultural UniversityDepartment of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life SciencesAgResearch Limited, Grasslands Research CentreRuminant Nutrition and Feed Engineering Technology Research Center, College of Animal Science and Technology, Nanjing Agricultural UniversityRuminant Nutrition and Feed Engineering Technology Research Center, College of Animal Science and Technology, Nanjing Agricultural UniversityAbstract Background Methanomassiliicoccales are a recently identified order of methanogens that are diverse across global environments particularly the gastrointestinal tracts of animals; however, their metabolic capacities are defined via a limited number of cultured strains. Results Here, we profile and analyze 243 Methanomassiliicoccales genomes assembled from cultured representatives and uncultured metagenomes recovered from various biomes, including the gastrointestinal tracts of different animal species. Our analyses reveal the presence of numerous undefined genera and genetic variability in metabolic capabilities within Methanomassiliicoccales lineages, which is essential for adaptation to their ecological niches. In particular, gastrointestinal tract Methanomassiliicoccales demonstrate the presence of co-diversified members with their hosts over evolutionary timescales and likely originated in the natural environment. We highlight the presence of diverse clades of vitamin transporter BtuC proteins that distinguish Methanomassiliicoccales from other archaeal orders and likely provide a competitive advantage in efficiently handling B12. Furthermore, genome-centric metatranscriptomic analysis of ruminants with varying methane yields reveal elevated expression of select Methanomassiliicoccales genera in low methane animals and suggest that B12 exchanges could enable them to occupy ecological niches that possibly alter the direction of H2 utilization. Conclusions We provide a comprehensive and updated account of divergent Methanomassiliicoccales lineages, drawing from numerous uncultured genomes obtained from various habitats. We also highlight their unique metabolic capabilities involving B12, which could serve as promising targets for mitigating ruminant methane emissions by altering H2 flow.https://doi.org/10.1186/s13059-024-03167-0MethanomassiliicoccalesComparative genomicsRuminantsMethane emissionsB12 |
| spellingShingle | Fei Xie Shengwei Zhao Xiaoxiu Zhan Yang Zhou Yin Li Weiyun Zhu Phillip B. Pope Graeme T. Attwood Wei Jin Shengyong Mao Unraveling the phylogenomic diversity of Methanomassiliicoccales and implications for mitigating ruminant methane emissions Genome Biology Methanomassiliicoccales Comparative genomics Ruminants Methane emissions B12 |
| title | Unraveling the phylogenomic diversity of Methanomassiliicoccales and implications for mitigating ruminant methane emissions |
| title_full | Unraveling the phylogenomic diversity of Methanomassiliicoccales and implications for mitigating ruminant methane emissions |
| title_fullStr | Unraveling the phylogenomic diversity of Methanomassiliicoccales and implications for mitigating ruminant methane emissions |
| title_full_unstemmed | Unraveling the phylogenomic diversity of Methanomassiliicoccales and implications for mitigating ruminant methane emissions |
| title_short | Unraveling the phylogenomic diversity of Methanomassiliicoccales and implications for mitigating ruminant methane emissions |
| title_sort | unraveling the phylogenomic diversity of methanomassiliicoccales and implications for mitigating ruminant methane emissions |
| topic | Methanomassiliicoccales Comparative genomics Ruminants Methane emissions B12 |
| url | https://doi.org/10.1186/s13059-024-03167-0 |
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