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

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Asgard archaea shed light on the evolutionary origins of the eukaryotic ubiquitin-ESCRT machinery. / Hatano, Tomoyuki; Palani, Saravanan; Papatziamou, Dimitra et al.
In: Nature Communications, Vol. 13, No. 1, 3398, 13.06.2022.

Research output: Contribution to Journal/MagazineJournal articlepeer-review

Harvard

Hatano, T, Palani, S, Papatziamou, D, Salzer, R, Souza, DP, Tamarit, D, Makwana, M, Potter, A, Haig, A, Xu, W, Townsend, D, Rochester, D, Bellini, D, Hussain, HMA, Ettema, TJG, Löwe, J, Baum, B, Robinson, NP & Balasubramanian, M 2022, 'Asgard archaea shed light on the evolutionary origins of the eukaryotic ubiquitin-ESCRT machinery', Nature Communications, vol. 13, no. 1, 3398. https://doi.org/10.1038/s41467-022-30656-2

APA

Hatano, T., Palani, S., Papatziamou, D., Salzer, R., Souza, D. P., Tamarit, D., Makwana, M., Potter, A., Haig, A., Xu, W., Townsend, D., Rochester, D., Bellini, D., Hussain, H. M. A., Ettema, T. J. G., Löwe, J., Baum, B., Robinson, N. P., & Balasubramanian, M. (2022). Asgard archaea shed light on the evolutionary origins of the eukaryotic ubiquitin-ESCRT machinery. Nature Communications, 13(1), Article 3398. https://doi.org/10.1038/s41467-022-30656-2

Vancouver

Hatano T, Palani S, Papatziamou D, Salzer R, Souza DP, Tamarit D et al. Asgard archaea shed light on the evolutionary origins of the eukaryotic ubiquitin-ESCRT machinery. Nature Communications. 2022 Jun 13;13(1):3398. doi: 10.1038/s41467-022-30656-2

Author

Hatano, Tomoyuki ; Palani, Saravanan ; Papatziamou, Dimitra et al. / Asgard archaea shed light on the evolutionary origins of the eukaryotic ubiquitin-ESCRT machinery. In: Nature Communications. 2022 ; Vol. 13, No. 1.

Bibtex

@article{2e62bbeea0564711b9ab369baf4488e6,
title = "Asgard archaea shed light on the evolutionary origins of the eukaryotic ubiquitin-ESCRT machinery",
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.",
keywords = "Article, /631/45/535/1266, /631/45/612/1237, /631/326/26/2524, /631/80/313/2155, /45/111, /82/16, /82/83, /101, /145, /9, /45/43, article",
author = "Tomoyuki Hatano and Saravanan Palani and Dimitra Papatziamou and Ralf Salzer and Souza, {Diorge P.} and Daniel Tamarit and Mehul Makwana and Antonia Potter and Alexandra Haig and Wenjue Xu and David Townsend and David Rochester and Dom Bellini and Hussain, {Hamdi M. A.} and Ettema, {Thijs J. G.} and Jan L{\"o}we and Buzz Baum and Robinson, {Nicholas P.} and Mohan Balasubramanian",
year = "2022",
month = jun,
day = "13",
doi = "10.1038/s41467-022-30656-2",
language = "English",
volume = "13",
journal = "Nature Communications",
issn = "2041-1723",
publisher = "Nature Publishing Group",
number = "1",

}

RIS

TY - JOUR

T1 - Asgard archaea shed light on the evolutionary origins of the eukaryotic ubiquitin-ESCRT machinery

AU - Hatano, Tomoyuki

AU - Palani, Saravanan

AU - Papatziamou, Dimitra

AU - Salzer, Ralf

AU - Souza, Diorge P.

AU - Tamarit, Daniel

AU - Makwana, Mehul

AU - Potter, Antonia

AU - Haig, Alexandra

AU - Xu, Wenjue

AU - Townsend, David

AU - Rochester, David

AU - Bellini, Dom

AU - Hussain, Hamdi M. A.

AU - Ettema, Thijs J. G.

AU - Löwe, Jan

AU - Baum, Buzz

AU - Robinson, Nicholas P.

AU - Balasubramanian, Mohan

PY - 2022/6/13

Y1 - 2022/6/13

N2 - 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.

AB - 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.

KW - Article

KW - /631/45/535/1266

KW - /631/45/612/1237

KW - /631/326/26/2524

KW - /631/80/313/2155

KW - /45/111

KW - /82/16

KW - /82/83

KW - /101

KW - /145

KW - /9

KW - /45/43

KW - article

U2 - 10.1038/s41467-022-30656-2

DO - 10.1038/s41467-022-30656-2

M3 - Journal article

VL - 13

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

IS - 1

M1 - 3398

ER -