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Genomics of soil depth niche partitioning in the Thaumarchaeota family Gagatemarchaeaceae

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  • Paul O. Sheridan

    (School of Biological Sciences, University of Aberdeen
    School of Biological and Chemical Sciences, University of Galway)

  • Yiyu Meng

    (School of Biological Sciences, University of Aberdeen)

  • Tom A. Williams

    (School of Biological Sciences, University of Bristol)

  • Cécile Gubry-Rangin

    (School of Biological Sciences, University of Aberdeen)

Abstract

Knowledge of deeply-rooted non-ammonia oxidising Thaumarchaeota lineages from terrestrial environments is scarce, despite their abundance in acidic soils. Here, 15 new deeply-rooted thaumarchaeotal genomes were assembled from acidic topsoils (0-15 cm) and subsoils (30-60 cm), corresponding to two genera of terrestrially prevalent Gagatemarchaeaceae (previously known as thaumarchaeotal Group I.1c) and to a novel genus of heterotrophic terrestrial Thaumarchaeota. Unlike previous predictions, metabolic annotations suggest Gagatemarchaeaceae perform aerobic respiration and use various organic carbon sources. Evolutionary divergence between topsoil and subsoil lineages happened early in Gagatemarchaeaceae history, with significant metabolic and genomic trait differences. Reconstruction of the evolutionary mechanisms showed that the genome expansion in topsoil Gagatemarchaeaceae resulted from extensive early lateral gene acquisition, followed by progressive gene duplication throughout evolutionary history. Ancestral trait reconstruction using the expanded genomic diversity also did not support the previous hypothesis of a thermophilic last common ancestor of the ammonia-oxidising archaea. Ultimately, this study provides a good model for studying mechanisms driving niche partitioning between spatially related ecosystems.

Suggested Citation

  • Paul O. Sheridan & Yiyu Meng & Tom A. Williams & Cécile Gubry-Rangin, 2023. "Genomics of soil depth niche partitioning in the Thaumarchaeota family Gagatemarchaeaceae," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43196-0
    DOI: 10.1038/s41467-023-43196-0
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    References listed on IDEAS

    as
    1. Paul O. Sheridan & Yiyu Meng & Tom A. Williams & Cécile Gubry-Rangin, 2022. "Recovery of Lutacidiplasmatales archaeal order genomes suggests convergent evolution in Thermoplasmatota," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. Benjamin J. Tully, 2019. "Metabolic diversity within the globally abundant Marine Group II Euryarchaea offers insight into ecological patterns," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    3. Paul O. Sheridan & Sebastien Raguideau & Christopher Quince & Jennifer Holden & Lihong Zhang & Tom A. Williams & Cécile Gubry-Rangin, 2020. "Gene duplication drives genome expansion in a major lineage of Thaumarchaeota," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    4. Joran Martijn & Max E. Schön & Anders E. Lind & Julian Vosseberg & Tom A. Williams & Anja Spang & Thijs J. G. Ettema, 2020. "Hikarchaeia demonstrate an intermediate stage in the methanogen-to-halophile transition," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    5. Zheng-Shuang Hua & Yan-Ni Qu & Qiyun Zhu & En-Min Zhou & Yan-Ling Qi & Yi-Rui Yin & Yang-Zhi Rao & Ye Tian & Yu-Xian Li & Lan Liu & Cindy J. Castelle & Brian P. Hedlund & Wen-Sheng Shu & Rob Knight & , 2018. "Genomic inference of the metabolism and evolution of the archaeal phylum Aigarchaeota," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    6. Metin Balaban & Niema Moshiri & Uyen Mai & Xingfan Jia & Siavash Mirarab, 2019. "TreeCluster: Clustering biological sequences using phylogenetic trees," PLOS ONE, Public Library of Science, vol. 14(8), pages 1-20, August.
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