Asgard archaea shed light on the evolutionary origins of the eukaryotic ubiquitin-ESCRT machinery

Tomoyuki Hatano, Saravanan Palani, Dimitra Papatziamou, Ralf Salzer, Diorge P. Souza, Daniel Tamarit, Mehul Makwana, Antonia Potter, Alexandra Haig, Wenjue Xu, David Townsend, David Rochester, Dom Bellini, Hamdi M. A. Hussain, Thijs J. G. Ettema, Jan Löwe, Buzz Baum (), Nicholas P. Robinson () and Mohan Balasubramanian ()
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Tomoyuki Hatano: University of Warwick
Saravanan Palani: University of Warwick
Dimitra Papatziamou: Lancaster University
Ralf Salzer: MRC Laboratory of Molecular Biology
Diorge P. Souza: MRC Laboratory of Molecular Biology
Daniel Tamarit: Wageningen University
Mehul Makwana: Lancaster University
Antonia Potter: Lancaster University
Alexandra Haig: Lancaster University
Wenjue Xu: Lancaster University
David Townsend: Lancaster University
David Rochester: Lancaster University
Dom Bellini: MRC Laboratory of Molecular Biology
Hamdi M. A. Hussain: University of Warwick
Thijs J. G. Ettema: Wageningen University
Jan Löwe: MRC Laboratory of Molecular Biology
Buzz Baum: MRC Laboratory of Molecular Biology
Nicholas P. Robinson: Lancaster University
Mohan Balasubramanian: University of Warwick

Nature Communications, 2022, vol. 13, issue 1, 1-16

Abstract: Abstract The ESCRT machinery, comprising of multiple proteins and subcomplexes, is crucial for membrane remodelling in eukaryotic cells, in processes that include ubiquitin-mediated multivesicular body formation, membrane repair, cytokinetic abscission, and virus exit from host cells. This ESCRT system appears to have simpler, ancient origins, since many archaeal species possess homologues of ESCRT-III and Vps4, the components that execute the final membrane scission reaction, where they have been shown to play roles in cytokinesis, extracellular vesicle formation and viral egress. Remarkably, metagenome assemblies of Asgard archaea, the closest known living relatives of eukaryotes, were recently shown to encode homologues of the entire cascade involved in ubiquitin-mediated membrane remodelling, including ubiquitin itself, components of the ESCRT-I and ESCRT-II subcomplexes, and ESCRT-III and Vps4. Here, we explore the phylogeny, structure, and biochemistry of Asgard homologues of the ESCRT machinery and the associated ubiquitylation system. We provide evidence for the ESCRT-I and ESCRT-II subcomplexes being involved in ubiquitin-directed recruitment of ESCRT-III, as it is in eukaryotes. Taken together, our analyses suggest a pre-eukaryotic origin for the ubiquitin-coupled ESCRT system and a likely path of ESCRT evolution via a series of gene duplication and diversification events.

Date: 2022
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DOI: 10.1038/s41467-022-30656-2

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