Open Access

Genome Biology

, volume 25 , issue 1 , publication number 32

Unraveling the phylogenomic diversity of Methanomassiliicoccales and implications for mitigating ruminant methane emissions

Fei Xie ^{1, 2}

Shengwei Zhao ^{1, 2}

Xiaoxiu Zhan ^{1, 2}

Zhou Yang ^{1, 2}

Li Yin ^{1, 2}

Weiyun Zhu ^{1, 2}

Phillip B Pope ^{3, 4}

Graeme T. Attwood ⁵

Wei Jin ^{1, 2}

Shengyong Mao ^{1, 2}

Hide authors affiliations Show authors affiliations: 5 affiliations

Ruminant Nutrition and Feed Engineering Technology Research Center, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, China |

Laboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, National Center for International Research on Animal Gut Nutrition, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, China |

Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, Ås, Norway |

⁴

Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Ås, Norway |

⁵

AgResearch Limited, Grasslands Research Centre, Palmerston North, New Zealand |

Publication type: Journal Article

Publication date: 2024-01-23

Springer Nature

Genome Biology

scimago Q1

wos Q1

SJR: 5.710

CiteScore: 17.5

Impact factor: 9.4

ISSN: 14747596, 14656906, 1474760X

DOI: 10.1186/s13059-024-03167-0

Copy DOI

PubMed ID: 38263062

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.

Found

1 citation

Kravchishina Marina

148 publications, 1 219 citations, 18 reviews

h-index: 17

P. P. Shirshov Institute of Oceanology of the Russian Academy of Sciences

Research interests

Biogeochemistry

Sedimentology

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GOST Copy

Xie F. et al. Unraveling the phylogenomic diversity of Methanomassiliicoccales and implications for mitigating ruminant methane emissions // Genome Biology. 2024. Vol. 25. No. 1. 32

GOST all authors (up to 50) Copy

Xie F., Zhao S., Zhan X., Zhou Yang, Li Yin, Zhu W., Pope P. B., Attwood G. T., Jin W., Mao S. Unraveling the phylogenomic diversity of Methanomassiliicoccales and implications for mitigating ruminant methane emissions // Genome Biology. 2024. Vol. 25. No. 1. 32

RIS |

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RIS Copy

TY - JOUR

DO - 10.1186/s13059-024-03167-0

UR - https://doi.org/10.1186/s13059-024-03167-0

TI - Unraveling the phylogenomic diversity of Methanomassiliicoccales and implications for mitigating ruminant methane emissions

T2 - Genome Biology

AU - Xie, Fei

AU - Zhao, Shengwei

AU - Zhan, Xiaoxiu

AU - Zhou Yang

AU - Li Yin

AU - Zhu, Weiyun

AU - Pope, Phillip B

AU - Attwood, Graeme T.

AU - Jin, Wei

AU - Mao, Shengyong

PY - 2024

DA - 2024/01/23

PB - Springer Nature

IS - 1

VL - 25

PMID - 38263062

SN - 1474-7596

SN - 1465-6906

SN - 1474-760X

ER -

BibTex

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BibTex (up to 50 authors) Copy

@article{2024_Xie,

author = {Fei Xie and Shengwei Zhao and Xiaoxiu Zhan and Zhou Yang and Li Yin and Weiyun Zhu and Phillip B Pope and Graeme T. Attwood and Wei Jin and Shengyong Mao},

title = {Unraveling the phylogenomic diversity of Methanomassiliicoccales and implications for mitigating ruminant methane emissions},

journal = {Genome Biology},

year = {2024},

volume = {25},

publisher = {Springer Nature},

month = {jan},

url = {https://doi.org/10.1186/s13059-024-03167-0},

number = {1},

pages = {32},

doi = {10.1186/s13059-024-03167-0}

}

Publisher

Springer Nature

Journal

Genome Biology

scimago Q1

wos Q1

SJR

5.710

CiteScore

17.5

Impact factor

9.4

ISSN

14747596 (Print)

14656906 (Print)

1474760X (Electronic)