Archaeal origin of tubulin

Abstract

Tubulins are a family of GTPases that are key components of the cytoskeleton in all eukaryotes and are distantly related to the FtsZ GTPase that is involved in cell division in most bacteria and many archaea. Among prokaryotes, bona fide tubulins have been identified only in bacteria of the genus Prosthecobacter. These bacterial tubulin genes appear to have been horizontally transferred from eukaryotes. Here we describe tubulins encoded in the genomes of thaumarchaeota of the genus Nitrosoarchaeum that we denote artubulins Phylogenetic analysis results are compatible with the origin of eukaryotic tubulins from artubulins. These findings expand the emerging picture of the origin of key components of eukaryotic functional systems from ancestral forms that are scattered among the extant archaea.

Figure 1

Conserved sequence blocks in the tubulin/FtsZ superfamily. The conserved blocks are separated by numbers which indicate the length of less well conserved sequence segments that are not shown (see Additional File 1). The alignment columns are colored on the basis of the respective position conservation throughout the superfamily: yellow background indicates hydrophobic residues (ACFILMVWY), red letters indicate polar residues (DEHKNQR), and green background indicates small residues (ACGNPSTV). Asterisks indicate amino acid residues that are conserved in the majority of the tubulins including artubulins but not in the majority of the FtsZ sequences. Each sequence is denoted by the corresponding taxon abbreviation followed by the species abbreviation and GenBank Identification (GI) number. Taxa abbreviations: A, Archaea; B, Bacteria; E, Eukaryota; Ac, Crenarchaeota; Ae, Euryarchaeota; An, Nanoarchaeota; At, Thaumarchaeota; Bv, Verrucomicrobia; Ec, Alveolata; Ek, Euglenozoa; El, Fungi/Metazoa group; Ep, Viridiplantae; Eq, Heterolobosea. Species abbreviations: Arath, Arabidopsis thaliana; Chlre, Chlamydomonas reinhardtii; Danre, Danio rerio; Drome, Drosophila melanogaster; Galga, Gallus gallus; Mondo, Monodelphis domestica; Musmu, Mus musculus; Naegr, Naegleria gruberi; Naneq, Nanoarchaeum equitans Kin4-M; Nemve, Nematostella vectensis; Ornan, Ornithorhynchus anatinus; Parte, Paramecium tetraurelia; Phypa, Physcomitrella patens; Plakn, Plasmodium knowlesi strain H; Plavi, Plasmodium vivax SaI-1; Prodeb, Prosthecobacter debontii; Prodej, Prosthecobacter dejongeii; Prova, Prosthecobacter vanneervenii; Sacce, Saccharomyces cerevisiae S288c; Strpu, Strongylocentrotus purpuratus; Tetth, Tetrahymena thermophila; Triad, Trichoplax adhaerens; Trycr, Trypanosoma cruzi; Xenla, Xenopus laevis.

Figure 2

Archaeal, bacterial and eukaryotic tubulins. (A) Phylogenetic tree of the FtsZ-tubulin superfamily. The tree is rooted by FtsZ proteins; TreeFinder/Molphy bootstrap values are indicated for major branches. The sequences are denoted as in Figure 1. Asterisks mark diverged ciliate tubulins [12]. (B) Genome neighborhood of bacterial and thaumarchaeal tubulins. Genes are marked as follows: A, bacterial tubulin A; B, bacterial tubulin B; C, tetratricopeptide repeat protein referred to as bacterial kinesin light chain in ref (PMIDS 12486237 and 17942428); T, thaumarchaeal tubulin; S, Snf7; 1, putative serine/threonine kinase; 2, pyruvate phosphate dikinase; 3, aspartate aminotransferase; 4, response regulator with a HTH DNA-binding domain; 5, glucose/sorbose dehydrogenase; 6, cysteine synthase; 7, DEAD/DEAH box helicase; 8, Major facilitator superfamily MFS 1; 9, TATA-box binding protein; 10, zinc-binding CMP/dCMP deaminase; 11, DNA polymerase I; 12, conserved hypothetical protein; 13, triosephosphate isomerase; and 14, AsnC family transcriptional regulator. Syntenic regions between Nitrosarachaeum koreensis and Nitrosopumilis maritimus are shaded.