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Characterisation of the Ubiquitin-ESCRT pathway in Asgard archaea sheds new light on origins of membrane trafficking in eukaryotes

Tomoyuki Hatano, View ORCID ProfileSaravanan Palani, Dimitra Papatziamou, Diorge P. Souza, Ralf Salzer, Daniel Tamarit, Mehul Makwana, Antonia Potter, Alexandra Haig, Wenjue Xu, David Townsend, David Rochester, Dom Bellini, Hamdi M. A. Hussain, Thijs Ettema, Jan Löwe, Buzz Baum, Nicholas P. Robinson, Mohan Balasubramanian
doi: https://doi.org/10.1101/2021.08.17.456605
Tomoyuki Hatano
1Centre for Mechanochemical Cell Biology, Division of Biomedical Sciences, Warwick Medical School, University of Warwick, Coventry CV4 7AL, United Kingdom
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Saravanan Palani
1Centre for Mechanochemical Cell Biology, Division of Biomedical Sciences, Warwick Medical School, University of Warwick, Coventry CV4 7AL, United Kingdom
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  • ORCID record for Saravanan Palani
Dimitra Papatziamou
2Division of Biomedical and Life Sciences, Faculty of Health and Medicine, Lancaster University, Lancaster LA1 4YG, United Kingdom
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Diorge P. Souza
3MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, United Kingdom
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Ralf Salzer
3MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, United Kingdom
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Daniel Tamarit
4Laboratory of Microbiology, Department of Agrotechnology and Food Sciences, Wageningen University, Wageningen 6708 WE, the Netherlands
5Department of Aquatic Sciences and Assessment, Swedish University of Agricultural Sciences, SE-75007 Uppsala, Sweden
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Mehul Makwana
2Division of Biomedical and Life Sciences, Faculty of Health and Medicine, Lancaster University, Lancaster LA1 4YG, United Kingdom
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Antonia Potter
2Division of Biomedical and Life Sciences, Faculty of Health and Medicine, Lancaster University, Lancaster LA1 4YG, United Kingdom
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Alexandra Haig
2Division of Biomedical and Life Sciences, Faculty of Health and Medicine, Lancaster University, Lancaster LA1 4YG, United Kingdom
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Wenjue Xu
2Division of Biomedical and Life Sciences, Faculty of Health and Medicine, Lancaster University, Lancaster LA1 4YG, United Kingdom
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David Townsend
6Department of Chemistry, Lancaster University, Lancaster LA1 4YB, United Kingdom
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David Rochester
6Department of Chemistry, Lancaster University, Lancaster LA1 4YB, United Kingdom
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Dom Bellini
3MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, United Kingdom
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Hamdi M. A. Hussain
1Centre for Mechanochemical Cell Biology, Division of Biomedical Sciences, Warwick Medical School, University of Warwick, Coventry CV4 7AL, United Kingdom
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Thijs Ettema
4Laboratory of Microbiology, Department of Agrotechnology and Food Sciences, Wageningen University, Wageningen 6708 WE, the Netherlands
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Jan Löwe
3MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, United Kingdom
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Buzz Baum
3MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, United Kingdom
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  • For correspondence: M.K.Balasubramanian@warwick.ac.uk n.robinson2@lancaster.ac.uk bbaum@mrc-lmb.cam.ac.uk
Nicholas P. Robinson
2Division of Biomedical and Life Sciences, Faculty of Health and Medicine, Lancaster University, Lancaster LA1 4YG, United Kingdom
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  • For correspondence: M.K.Balasubramanian@warwick.ac.uk n.robinson2@lancaster.ac.uk bbaum@mrc-lmb.cam.ac.uk
Mohan Balasubramanian
1Centre for Mechanochemical Cell Biology, Division of Biomedical Sciences, Warwick Medical School, University of Warwick, Coventry CV4 7AL, United Kingdom
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  • For correspondence: M.K.Balasubramanian@warwick.ac.uk n.robinson2@lancaster.ac.uk bbaum@mrc-lmb.cam.ac.uk
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SUMMARY

The ESCRT machinery performs a critical role in membrane remodelling events in all eukaryotic cells, including in membrane trafficking, membrane repair, cytokinetic abscission, in viral egress, and in the generation of extracellular vesicles. While the machinery is complex in modern day eukaryotes, where it comprises dozens of proteins, the system has simpler and more ancient origins. Indeed, homologues of ESCRT-III and the Vps4 ATPase, the proteins that execute the final membrane scission reaction, play analogous roles in cytokinesis and potentially in extracellular vesicle formation in TACK archaea where ESCRT-I and II homologues seem to be absent. Here, we explore the phylogeny, structure, and biochemistry of homologues of the ESCRT machinery and the associated ubiquitylation system found in genome assemblies of the recently discovered Asgard archaea. In these closest living prokaryotic relatives of eukaryotes, we provide evidence for the ESCRT-I and II sub-complexes being involved in the ubiquitin-directed recruitment of ESCRT-III,_as it is in eukaryotes. This analysis suggests a pre-eukaryotic origin for the Ub-coupled ESCRT system and a likely path of ESCRT evolution via a series of gene duplication and diversification events.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Characterisation of the Ubiquitin-ESCRT pathway in Asgard archaea sheds new light on origins of membrane trafficking in eukaryotes
Tomoyuki Hatano, Saravanan Palani, Dimitra Papatziamou, Diorge P. Souza, Ralf Salzer, Daniel Tamarit, Mehul Makwana, Antonia Potter, Alexandra Haig, Wenjue Xu, David Townsend, David Rochester, Dom Bellini, Hamdi M. A. Hussain, Thijs Ettema, Jan Löwe, Buzz Baum, Nicholas P. Robinson, Mohan Balasubramanian
bioRxiv 2021.08.17.456605; doi: https://doi.org/10.1101/2021.08.17.456605
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Characterisation of the Ubiquitin-ESCRT pathway in Asgard archaea sheds new light on origins of membrane trafficking in eukaryotes
Tomoyuki Hatano, Saravanan Palani, Dimitra Papatziamou, Diorge P. Souza, Ralf Salzer, Daniel Tamarit, Mehul Makwana, Antonia Potter, Alexandra Haig, Wenjue Xu, David Townsend, David Rochester, Dom Bellini, Hamdi M. A. Hussain, Thijs Ettema, Jan Löwe, Buzz Baum, Nicholas P. Robinson, Mohan Balasubramanian
bioRxiv 2021.08.17.456605; doi: https://doi.org/10.1101/2021.08.17.456605

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