Genomics of soil depth niche partitioning in the Thaumarchaeota family Gagatemarchaeaceae

Paul O Sheridan, Yiyu Meng, Tom A Williams, Cécile Gubry-Rangin

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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.

Original languageEnglish
Article number7305
JournalNature Communications
Volume14
Issue number1
DOIs
Publication statusPublished - 11 Nov 2023

Bibliographical note

Acknowledgements
UKRI financially supported P.O.S. and Y.M. through the NERC grant (NE/R001529/1). In addition, C.G.-R. and T.A.W. were supported by Royal Society University Research Fellowships (URF150571 and UF140626, respectively). We thank Tony Travis for his support with Biolinux. The authors would also like to acknowledge the support of the Maxwell computer cluster funded by the University of Aberdeen.

Keywords

  • Soil
  • Ecosystem
  • Phylogeny
  • Archaea/metabolism
  • Genomics
  • Soil Microbiology
  • Oxidation-Reduction
  • Ammonia/metabolism

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