Six Subgroups and Extensive Recent Duplications Characterize the Evolution of the Eukaryotic Tubulin Protein Family

Abstract

Tubulins belong to the most abundant proteins in eukaryotes providing the backbone for many cellular substructures like the mitotic and meiotic spindles, the intracellular cytoskeletal network, and the axonemes of cilia and flagella. Homologs have even been reported for archaea and bacteria. However, a taxonomically broad and whole-genome-based analysis of the tubulin protein family has never been performed, and thus, the number of subfamilies, their taxonomic distribution, and the exact grouping of the supposed archaeal and bacterial homologs are unknown. Here, we present the analysis of 3,524 tubulins from 504 species. The tubulins formed six major subfamilies, α to ζ. Species of all major kingdoms of the eukaryotes encode members of these subfamilies implying that they must have already been present in the last common eukaryotic ancestor. The proposed archaeal homologs grouped together with the bacterial TubZ proteins as sister clade to the FtsZ proteins indicating that tubulins are unique to eukaryotes. Most species contained α- and/or β-tubulin gene duplicates resulting from recent branch- and species-specific duplication events. This shows that tubulins cannot be used for constructing species phylogenies without resolving their ortholog–paralog relationships. The many gene duplicates and also the independent loss of the δ-, ε-, or ζ-tubulins, which have been shown to be part of the triplet microtubules in basal bodies, suggest that tubulins can functionally substitute each other.

Zeta-Tubulin Is a Member of a Conserved Tubulin Module and Is a Component of the Centriolar Basal Foot in Multiciliated Cells

“…The final member of the tubulin superfamily, zeta-tubulin, was identified in a recent evolutionary analysis showing that proteins annotated as zeta-tubulin, “cryptic tubulin”, and eta-tubulin form a single unique tubulin family [1, 8, 9]. Zeta-tubulins are present in many genomes, but are mostly unannotated or mis-annotated, and essentially uncharacterized.…”

“… SUMMARY There are six members of the tubulin superfamily in eukaryotes [1]. Alpha- and beta-tubulin form a heterodimer that polymerizes to form microtubules, and gamma-tubulin nucleates microtubules as a component of the gamma-tubulin ring complex.…”

Centriole triplet microtubules are required for stable centriole formation and inheritance in human cells

“…In the unicellular eukaryotes Chlamydomonas, Tetrahymena, Paramecium and Trypanosoma, mutations in delta-tubulin or epsilon-tubulin result in centrioles that lack triplet microtubules (Dupuis-Williams et al, 2002;Dutcher and Trabuco, 1998;Dutcher et al, 2002;Gadelha et al, 2006;Garreau de Loubresse et al, 2001;Goodenough and StClair, 1975;Ross et al, 2013). Humans and other placental mammals have delta-tubulin and epsilon-tubulin, but lack zeta-tubulin (Findeisen et al, 2014;Turk et al, 2015). Here, we show that human cells lacking delta-tubulin or epsilon-tubulin also lack triplets, that this results in unstable centrioles and initiation of a futile cycle of centriole formation and disintegration, and identify an interaction between deltatubulin and epsilon-tubulin.…”

Bacterial Tubulins A and B Exhibit Polarized Growth, Mixed-Polarity Bundling, and Destabilization by GTP Hydrolysis

“…BtubA/B have more sequence and structure in common with eukaryotic tubulins than any other bacterial tubulin, and the presence of both btubA and btubB genes suggests that the horizontal transfer event that is thought to have occurred not long after the initial duplication event created the ancestors of the A and B and ␣ and ␤ homolog pairs (7). The more evolutionarily distant phage tubulin PhuZ has been demonstrated to exhibit dynamic instability (32) and to segregate DNA (34).…”