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Three-dimensional flagella structures from animals’ closest unicellular relatives, the Choanoflagellates

In most eukaryotic organisms, cilia and flagella perform a variety of life-sustaining roles related to environmental sensing and motility. Cryo-electron microscopy has provided considerable insight into the morphology and function of flagellar structures, but studies have been limited to less than a...

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Autores principales: Pinskey, Justine M, Lagisetty, Adhya, Gui, Long, Phan, Nhan, Reetz, Evan, Tavakoli, Amirrasoul, Fu, Gang, Nicastro, Daniela
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9671500/
https://www.ncbi.nlm.nih.gov/pubmed/36384644
http://dx.doi.org/10.7554/eLife.78133
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author Pinskey, Justine M
Lagisetty, Adhya
Gui, Long
Phan, Nhan
Reetz, Evan
Tavakoli, Amirrasoul
Fu, Gang
Nicastro, Daniela
author_facet Pinskey, Justine M
Lagisetty, Adhya
Gui, Long
Phan, Nhan
Reetz, Evan
Tavakoli, Amirrasoul
Fu, Gang
Nicastro, Daniela
author_sort Pinskey, Justine M
collection PubMed
description In most eukaryotic organisms, cilia and flagella perform a variety of life-sustaining roles related to environmental sensing and motility. Cryo-electron microscopy has provided considerable insight into the morphology and function of flagellar structures, but studies have been limited to less than a dozen of the millions of known eukaryotic species. Ultrastructural information is particularly lacking for unicellular organisms in the Opisthokonta clade, leaving a sizeable gap in our understanding of flagella evolution between unicellular species and multicellular metazoans (animals). Choanoflagellates are important aquatic heterotrophs, uniquely positioned within the opisthokonts as the metazoans’ closest living unicellular relatives. We performed cryo-focused ion beam milling and cryo-electron tomography on flagella from the choanoflagellate species Salpingoeca rosetta. We show that the axonemal dyneins, radial spokes, and central pair complex in S. rosetta more closely resemble metazoan structures than those of unicellular organisms from other suprakingdoms. In addition, we describe unique features of S. rosetta flagella, including microtubule holes, microtubule inner proteins, and the flagellar vane: a fine, net-like extension that has been notoriously difficult to visualize using other methods. Furthermore, we report barb-like structures of unknown function on the extracellular surface of the flagellar membrane. Together, our findings provide new insights into choanoflagellate biology and flagella evolution between unicellular and multicellular opisthokonts.
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spelling pubmed-96715002022-11-18 Three-dimensional flagella structures from animals’ closest unicellular relatives, the Choanoflagellates Pinskey, Justine M Lagisetty, Adhya Gui, Long Phan, Nhan Reetz, Evan Tavakoli, Amirrasoul Fu, Gang Nicastro, Daniela eLife Structural Biology and Molecular Biophysics In most eukaryotic organisms, cilia and flagella perform a variety of life-sustaining roles related to environmental sensing and motility. Cryo-electron microscopy has provided considerable insight into the morphology and function of flagellar structures, but studies have been limited to less than a dozen of the millions of known eukaryotic species. Ultrastructural information is particularly lacking for unicellular organisms in the Opisthokonta clade, leaving a sizeable gap in our understanding of flagella evolution between unicellular species and multicellular metazoans (animals). Choanoflagellates are important aquatic heterotrophs, uniquely positioned within the opisthokonts as the metazoans’ closest living unicellular relatives. We performed cryo-focused ion beam milling and cryo-electron tomography on flagella from the choanoflagellate species Salpingoeca rosetta. We show that the axonemal dyneins, radial spokes, and central pair complex in S. rosetta more closely resemble metazoan structures than those of unicellular organisms from other suprakingdoms. In addition, we describe unique features of S. rosetta flagella, including microtubule holes, microtubule inner proteins, and the flagellar vane: a fine, net-like extension that has been notoriously difficult to visualize using other methods. Furthermore, we report barb-like structures of unknown function on the extracellular surface of the flagellar membrane. Together, our findings provide new insights into choanoflagellate biology and flagella evolution between unicellular and multicellular opisthokonts. eLife Sciences Publications, Ltd 2022-11-17 /pmc/articles/PMC9671500/ /pubmed/36384644 http://dx.doi.org/10.7554/eLife.78133 Text en © 2022, Pinskey et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Structural Biology and Molecular Biophysics
Pinskey, Justine M
Lagisetty, Adhya
Gui, Long
Phan, Nhan
Reetz, Evan
Tavakoli, Amirrasoul
Fu, Gang
Nicastro, Daniela
Three-dimensional flagella structures from animals’ closest unicellular relatives, the Choanoflagellates
title Three-dimensional flagella structures from animals’ closest unicellular relatives, the Choanoflagellates
title_full Three-dimensional flagella structures from animals’ closest unicellular relatives, the Choanoflagellates
title_fullStr Three-dimensional flagella structures from animals’ closest unicellular relatives, the Choanoflagellates
title_full_unstemmed Three-dimensional flagella structures from animals’ closest unicellular relatives, the Choanoflagellates
title_short Three-dimensional flagella structures from animals’ closest unicellular relatives, the Choanoflagellates
title_sort three-dimensional flagella structures from animals’ closest unicellular relatives, the choanoflagellates
topic Structural Biology and Molecular Biophysics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9671500/
https://www.ncbi.nlm.nih.gov/pubmed/36384644
http://dx.doi.org/10.7554/eLife.78133
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