Asgard archaea shed light on the evolutionary origins of the eukaryotic ubiquitin-ESCRT machinery.
Hussain, Hamdi MA
Springer Science and Business Media LLC
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Hatano, T., Palani, S., Papatziamou, D., Salzer, R., Souza, D. P., Tamarit, D., Makwana, M., et al. (2022). Asgard archaea shed light on the evolutionary origins of the eukaryotic ubiquitin-ESCRT machinery.. Nat Commun, 13 (1) https://doi.org/10.1038/s41467-022-30656-2
Funder: Above funding attributed to the authors as follows (from paper acknowledgements): Computational analysis was facilitated by resources provided by the Swedish National Infrastructure for Computing (SNIC) at the Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX), partially funded by the Swedish Research Council through grant agreement no. 2018-05973. We thank the Warwick Proteomics RTP for mass spectrometry. MKB was supported by the Wellcome Trust (WT101885MA) and the European Research Council (ERC-2014-ADG No. 671083). Work by the NR laboratory was supported by start-up funds from the Division of Biomedical and Life Sciences (BLS, Lancaster University) and a Leverhulme Research Project Grant (RPG-2019-297). NR would like to thank Johanna Syrjanen for performing trial expressions of the Odinarchaeota ESCRT proteins, and Joseph Maman for helpful discussion regarding the SEC-MALS. NR, WX and AP would like to thank Charley Lai and Siu-Kei Yau for assistance with initial Odinarchaeota ESCRT protein purifications. DPS and BB would like to thank Chris Johnson at the MRC LMB Biophysics facility for performing the SEC-MALS assay on Heimdallarchaeotal Vps22. TH, HH, MB, RS, JL, D Tamarit, TE, DPS and BB received support from a Wellcome Trust collaborative award (203276/Z/16/Z). BB and DPS were supported by the MRC. D Tamarit was supported by the Swedish Research Council (International Postdoc grant 2018-06609).
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.
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
Wellcome Trust (Wellcome) (203276/Z/16/Z, WT101885MA)
Leverhulme Trust (RPG-2019-297)
Svenska Forskningsrådet Formas (Swedish Research Council Formas) (2018-06609, 2018-05973)
External DOI: https://doi.org/10.1038/s41467-022-30656-2
This record's URL: https://www.repository.cam.ac.uk/handle/1810/338086