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

Akıl, Caner; Ali, Samson; Tran, Linh Thuoc; Gaillard, Jérémie; Li, Wenfei; Hayashida, Kenichi; Hirose, Mika; Kato, Takayuki; Oshima, Atsunori; Fujishima, Kosuke; Blanchoin, Laurent; Narita, Akihiro; Robinson, Robert

doi:10.1126/sciadv.abm2225

Cited by 18 publications

(31 citation statements)

References 48 publications

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“…These differences could be due to different parameters of the reconstructions (taxonomic sampling, the use of different outgroups, or different methods for the MSA trimming), showing the phylogenetic instability of these prokaryotic tubulins and, therefore, the difficulty in inferring their evolutionary placement. Nevertheless, from our reconstructions, it is clear that OdinTubulins and BtubA/B are closer to α- and β-tubulins, in agreement with recent analyses ( Akıl et al, 2022 ).…”

Section: Resultssupporting

confidence: 92%

“…Despite the possible incompleteness of the Asgardarchaeota metagenomes, the sequencing of several Asgardarchaeota clades ( Liu et al, 2021 ) confirmed that this OdinTubulin is still uniquely found in this archaeon. In vitro and at high temperatures, this OdinTubulin forms tubules with short curved protofilaments coiling around the tubule circumference, more similar to FtsZ, rather than running parallel to its length as in eukaryotic microtubules ( Akıl et al, 2022 ). Nevertheless, the genome context of this OdinTubulin displays interesting features related to eukaryotes.…”

Section: Resultsmentioning

confidence: 99%

“…To provide a global overview of the evolution of the FtsZ/tubulin protein family, we reconstructed a phylogeny of representative sequences representing the diversity of subfamilies, their relationships, and their domain architecture ( Figure 1 ). The FtsZ/tubulin protein family is mainly composed of prokaryotic FtsZ [including mitochondrial ( Leger et al, 2015 ) and chloroplastic ( TerBush et al, 2013 ) ones], eukaryotic tubulins [including prokaryotic sequences from Asgardarchaeota ( Akıl et al, 2022 ) and Verrucomicrobia ( Schlieper et al, 2005 )], archaeal paralogs closely related to tubulins [including CetZ ( Duggin et al, 2015 ), artubulins ( Yutin and Koonin, 2012 ), and other bacterial and archaeal sequences not included in this tree such as the plasmidic TubZ found in Firmicutes ( Larsen et al, 2007 )], and divergent homologs bearing the tubulin_2 Pfam domain, which were used to root the tree. This latter group, here called FtsZ-like, displayed diverse domain composition and poorly aligned positions, and given its sparse distribution in prokaryotes, domain architecture, and genomic synteny, its evolutionary history is unlikely to be directly related to the one of the FtsZ/tubulin protein family ( Makarova and Koonin, 2010 ).…”

Section: Introductionmentioning

confidence: 99%

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Early origin and evolution of the FtsZ/tubulin protein family

2023

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The origin of the FtsZ/tubulin protein family was extremely relevant for life since these proteins are present in nearly all organisms, carrying out essential functions such as cell division or forming a major part of the cytoskeleton in eukaryotes. Therefore, investigating the early evolution of the FtsZ/tubulin protein family could reveal crucial aspects of the diversification of the three domains of life. In this study, we revisited the phylogenies of the FtsZ/tubulin protein family in an extensive prokaryotic diversity, focusing on the main evolutionary events that occurred during its evolution. We found evidence of its early origin in the last universal common ancestor since FtsZ was present in the last common ancestor of Bacteria and Archaea. In bacteria, ftsZ genes are genomically associated with the bacterial division gene cluster, while in archaea, ftsZ duplicated prior to archaeal diversification, and one of the copies is associated with protein biosynthesis genes. Archaea have expanded the FtsZ/tubulin protein family with sequences closely related to eukaryotic tubulins. In addition, we report novel CetZ-like groups in Halobacterota and Asgardarchaeota. Investigating the C-termini of prokaryotic paralogs basal to eukaryotic tubulins, we show that archaeal CetZ, as well as the plasmidic TubZ from Firmicutes, most likely originated from archaeal FtsZ. Finally, prokaryotic tubulins are restricted to Odinarchaeaota and Prosthecobacter species, and they seem to belong to different molecular systems. However, their phylogenies suggest that they are closely related to α/β-tubulins pointing to a potential ancestrality of these eukaryotic paralogs of tubulins.

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Section: Resultssupporting

confidence: 92%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Early origin and evolution of the FtsZ/tubulin protein family

2023

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“…Prokaryotic homologs are called FtsZ, and form structure like a contraction ring in eukaryotes. Recently, we analyzed the tubulin homolog from the archaea Odin, determined the polymerization conditions, and performed cryo-EM analysis [17]. The results were surprising.…”

Section: The Archaea Tubulin Homologmentioning

confidence: 99%

Structural analysis of filamentous complexes by cryo-electron microscopy

Narita

2022

Translational and Regulatory Sciences

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Cryo-electron microscopy (cryo-EM) has become one of the main tools in structural biology over the last decade. Nonetheless, the details of cryo-EM remain unknown to many researchers. Cryo-electron microscopes are very expensive. Therefore, owning, maintaining, or renewing a cryo-EM instrument in a single laboratory or university is often challenging. As has been done for synchrotrons, it is rational to introduce cryo-EM in shared facilities and allocate cryo-EM beamtimes to research teams. Shared cryo-EM systems have been established in several countries. However, sound knowledge of sample preparation is essential for achieving results using shared facilities, where the availability of beamtime is limited. In this review, we present the current state of cryo-EM for general users who do not have direct access to a cryo-electron microscope by reviewing the achieved structures (mainly filamentous complexes) and the ways to determine them.

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“…(A–D) Scheme of the main conformational changes in tubulin and MTs. ,,, (E) Prokaryotic tubulins described in the manuscript. , …”

Section: Introductionmentioning

confidence: 99%

Alternative Approaches to Understand Microtubule Cap Morphology and Function

et al. 2023

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Microtubules (MTs) are essential cellular machines built from concatenated αβ-tubulin heterodimers. They are responsible for two central and opposite functions from the dynamic point of view: scaffolding (static filaments) and force generation (dynamic MTs). These roles engage multiple physiological processes, including cell shape, polarization, division and movement, and intracellular long-distance transport. At the most basic level, the MT regulation is chemical because GTP binding and hydrolysis have the ability to promote assembly and disassembly in the absence of any other constraint. Due to the stochastic GTP hydrolysis, a chemical gradient from GTP-bound to GDP-bound tubulin is created at the MT growing end (GTP cap), which is translated into a cascade of structural regulatory changes known as MT maturation. This is an area of intense research, and several models have been proposed based on information mostly gathered from macromolecular crystallography and cryo-electron microscopy studies. However, these classical structural biology methods lack temporal resolution and can be complemented, as shown in this mini-review, by other approaches such as time-resolved fiber diffraction and computational modeling. Together with studies on structurally similar tubulins from the prokaryotic world, these inputs can provide novel insights on MT assembly, dynamics, and the GTP cap.

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

Cited by 18 publications

References 48 publications

Early origin and evolution of the FtsZ/tubulin protein family

Early origin and evolution of the FtsZ/tubulin protein family

Structural analysis of filamentous complexes by cryo-electron microscopy

Alternative Approaches to Understand Microtubule Cap Morphology and Function

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