Cargando…
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...
Autores principales: | , , , , , , , |
---|---|
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 |
_version_ | 1784832566177562624 |
---|---|
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. |
format | Online Article Text |
id | pubmed-9671500 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT pinskeyjustinem threedimensionalflagellastructuresfromanimalsclosestunicellularrelativesthechoanoflagellates AT lagisettyadhya threedimensionalflagellastructuresfromanimalsclosestunicellularrelativesthechoanoflagellates AT guilong threedimensionalflagellastructuresfromanimalsclosestunicellularrelativesthechoanoflagellates AT phannhan threedimensionalflagellastructuresfromanimalsclosestunicellularrelativesthechoanoflagellates AT reetzevan threedimensionalflagellastructuresfromanimalsclosestunicellularrelativesthechoanoflagellates AT tavakoliamirrasoul threedimensionalflagellastructuresfromanimalsclosestunicellularrelativesthechoanoflagellates AT fugang threedimensionalflagellastructuresfromanimalsclosestunicellularrelativesthechoanoflagellates AT nicastrodaniela threedimensionalflagellastructuresfromanimalsclosestunicellularrelativesthechoanoflagellates |