Inference and reconstruction of the heimdallarchaeial ancestry of eukaryotes

Laura Eme, Daniel Tamarit, Eva F. Caceres, Courtney W. Stairs, Valerie Anda, Max E. Schön, Kiley W. Seitz, Nina Dombrowski, William H. Lewis, Felix Homa, Jimmy H. Saw, Jonathan Lombard, Takuro Nunoura, Wen-Jun Li, Zheng-Shuang Hua, Lin-Xing Chen, Jillian F. Banfield, Emily St John, Anna-Louise Reysenbach, Matthew B. Stott, Andreas Schramm, Kasper U. Kjeldsen, Andreas P. Teske, Brett J. Baker and Thijs J. G. Ettema ()
Additional contact information
Laura Eme: Uppsala University
Daniel Tamarit: Uppsala University
Eva F. Caceres: Uppsala University
Courtney W. Stairs: Uppsala University
Valerie Anda: University of Texas Austin
Max E. Schön: Uppsala University
Kiley W. Seitz: University of Texas Austin
Nina Dombrowski: University of Texas Austin
William H. Lewis: Uppsala University
Felix Homa: Wageningen University and Research
Jimmy H. Saw: Uppsala University
Jonathan Lombard: Uppsala University
Takuro Nunoura: Japan Agency for Marine-Earth Science and Technology (JAMSTEC)
Wen-Jun Li: Sun Yat-Sen University
Zheng-Shuang Hua: University of Science and Technology of China
Lin-Xing Chen: University of California
Jillian F. Banfield: University of California
Emily St John: Portland State University
Anna-Louise Reysenbach: Portland State University
Matthew B. Stott: University of Canterbury
Andreas Schramm: Aarhus University
Kasper U. Kjeldsen: Aarhus University
Andreas P. Teske: University of North Carolina
Brett J. Baker: University of Texas Austin
Thijs J. G. Ettema: Uppsala University

Nature, 2023, vol. 618, issue 7967, 992-999

Abstract: Abstract In the ongoing debates about eukaryogenesis—the series of evolutionary events leading to the emergence of the eukaryotic cell from prokaryotic ancestors—members of the Asgard archaea play a key part as the closest archaeal relatives of eukaryotes1. However, the nature and phylogenetic identity of the last common ancestor of Asgard archaea and eukaryotes remain unresolved2–4. Here we analyse distinct phylogenetic marker datasets of an expanded genomic sampling of Asgard archaea and evaluate competing evolutionary scenarios using state-of-the-art phylogenomic approaches. We find that eukaryotes are placed, with high confidence, as a well-nested clade within Asgard archaea and as a sister lineage to Hodarchaeales, a newly proposed order within Heimdallarchaeia. Using sophisticated gene tree and species tree reconciliation approaches, we show that analogous to the evolution of eukaryotic genomes, genome evolution in Asgard archaea involved significantly more gene duplication and fewer gene loss events compared with other archaea. Finally, we infer that the last common ancestor of Asgard archaea was probably a thermophilic chemolithotroph and that the lineage from which eukaryotes evolved adapted to mesophilic conditions and acquired the genetic potential to support a heterotrophic lifestyle. Our work provides key insights into the prokaryote-to-eukaryote transition and a platform for better understanding the emergence of cellular complexity in eukaryotic cells.

Date: 2023
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DOI: 10.1038/s41586-023-06186-2

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