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Structure and dynamics of Odinarchaeota tubulin and the implications for eukaryotic microtubule evolution

Tubulins are critical for the internal organization of eukaryotic cells, and understanding their emergence is an important question in eukaryogenesis. Asgard archaea are the closest known prokaryotic relatives to eukaryotes. Here, we elucidated the apo and nucleotide-bound x-ray structures of an Asg...

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Autores principales: Akıl, Caner, Ali, Samson, Tran, Linh T., Gaillard, Jérémie, Li, Wenfei, Hayashida, Kenichi, Hirose, Mika, Kato, Takayuki, Oshima, Atsunori, Fujishima, Kosuke, Blanchoin, Laurent, Narita, Akihiro, Robinson, Robert C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Association for the Advancement of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8956254/
https://www.ncbi.nlm.nih.gov/pubmed/35333570
http://dx.doi.org/10.1126/sciadv.abm2225
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author Akıl, Caner
Ali, Samson
Tran, Linh T.
Gaillard, Jérémie
Li, Wenfei
Hayashida, Kenichi
Hirose, Mika
Kato, Takayuki
Oshima, Atsunori
Fujishima, Kosuke
Blanchoin, Laurent
Narita, Akihiro
Robinson, Robert C.
author_facet Akıl, Caner
Ali, Samson
Tran, Linh T.
Gaillard, Jérémie
Li, Wenfei
Hayashida, Kenichi
Hirose, Mika
Kato, Takayuki
Oshima, Atsunori
Fujishima, Kosuke
Blanchoin, Laurent
Narita, Akihiro
Robinson, Robert C.
author_sort Akıl, Caner
collection PubMed
description Tubulins are critical for the internal organization of eukaryotic cells, and understanding their emergence is an important question in eukaryogenesis. Asgard archaea are the closest known prokaryotic relatives to eukaryotes. Here, we elucidated the apo and nucleotide-bound x-ray structures of an Asgard tubulin from hydrothermal living Odinarchaeota (OdinTubulin). The guanosine 5′-triphosphate (GTP)–bound structure resembles a microtubule protofilament, with GTP bound between subunits, coordinating the “+” end subunit through a network of water molecules and unexpectedly by two cations. A water molecule is located suitable for GTP hydrolysis. Time course crystallography and electron microscopy revealed conformational changes on GTP hydrolysis. OdinTubulin forms tubules at high temperatures, with short curved protofilaments coiling around the tubule circumference, more similar to FtsZ, rather than running parallel to its length, as in microtubules. Thus, OdinTubulin represents an evolutionary stage intermediate between prokaryotic FtsZ and eukaryotic microtubule-forming tubulins.
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spelling pubmed-89562542022-04-04 Structure and dynamics of Odinarchaeota tubulin and the implications for eukaryotic microtubule evolution Akıl, Caner Ali, Samson Tran, Linh T. Gaillard, Jérémie Li, Wenfei Hayashida, Kenichi Hirose, Mika Kato, Takayuki Oshima, Atsunori Fujishima, Kosuke Blanchoin, Laurent Narita, Akihiro Robinson, Robert C. Sci Adv Biomedicine and Life Sciences Tubulins are critical for the internal organization of eukaryotic cells, and understanding their emergence is an important question in eukaryogenesis. Asgard archaea are the closest known prokaryotic relatives to eukaryotes. Here, we elucidated the apo and nucleotide-bound x-ray structures of an Asgard tubulin from hydrothermal living Odinarchaeota (OdinTubulin). The guanosine 5′-triphosphate (GTP)–bound structure resembles a microtubule protofilament, with GTP bound between subunits, coordinating the “+” end subunit through a network of water molecules and unexpectedly by two cations. A water molecule is located suitable for GTP hydrolysis. Time course crystallography and electron microscopy revealed conformational changes on GTP hydrolysis. OdinTubulin forms tubules at high temperatures, with short curved protofilaments coiling around the tubule circumference, more similar to FtsZ, rather than running parallel to its length, as in microtubules. Thus, OdinTubulin represents an evolutionary stage intermediate between prokaryotic FtsZ and eukaryotic microtubule-forming tubulins. American Association for the Advancement of Science 2022-03-25 /pmc/articles/PMC8956254/ /pubmed/35333570 http://dx.doi.org/10.1126/sciadv.abm2225 Text en Copyright © 2022 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). https://creativecommons.org/licenses/by-nc/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license (https://creativecommons.org/licenses/by-nc/4.0/) , which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
spellingShingle Biomedicine and Life Sciences
Akıl, Caner
Ali, Samson
Tran, Linh T.
Gaillard, Jérémie
Li, Wenfei
Hayashida, Kenichi
Hirose, Mika
Kato, Takayuki
Oshima, Atsunori
Fujishima, Kosuke
Blanchoin, Laurent
Narita, Akihiro
Robinson, Robert C.
Structure and dynamics of Odinarchaeota tubulin and the implications for eukaryotic microtubule evolution
title Structure and dynamics of Odinarchaeota tubulin and the implications for eukaryotic microtubule evolution
title_full Structure and dynamics of Odinarchaeota tubulin and the implications for eukaryotic microtubule evolution
title_fullStr Structure and dynamics of Odinarchaeota tubulin and the implications for eukaryotic microtubule evolution
title_full_unstemmed Structure and dynamics of Odinarchaeota tubulin and the implications for eukaryotic microtubule evolution
title_short Structure and dynamics of Odinarchaeota tubulin and the implications for eukaryotic microtubule evolution
title_sort structure and dynamics of odinarchaeota tubulin and the implications for eukaryotic microtubule evolution
topic Biomedicine and Life Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8956254/
https://www.ncbi.nlm.nih.gov/pubmed/35333570
http://dx.doi.org/10.1126/sciadv.abm2225
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