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, 280 (1769), 20131755

Phylogenomics Demonstrates That Breviate Flagellates Are Related to Opisthokonts and Apusomonads

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Phylogenomics Demonstrates That Breviate Flagellates Are Related to Opisthokonts and Apusomonads

Matthew W Brown et al. Proc Biol Sci.

Abstract

Most eukaryotic lineages belong to one of a few major groups. However, several protistan lineages have not yet been robustly placed in any of these groups. Both the breviates and apusomonads are two such lineages that appear to be related to the Amoebozoa and Opisthokonta (i.e. the 'unikonts' or Amorphea); however, their precise phylogenetic positions remain unclear. Here, we describe a novel microaerophilic breviate, Pygsuia biforma gen. nov. sp. nov., isolated from a hypoxic estuarine sediment. Ultrastructurally, this species resembles the breviate genera Breviata and Subulatomonas but has two cell morphologies, adherent and swimming. Phylogenetic analyses of the small sub-unit rRNA gene show that Pygsuia is the sister to the other breviates. We constructed a 159-protein supermatrix, including orthologues identified in RNA-seq data from Pygsuia. Phylogenomic analyses of this dataset show that breviates, apusomonads and Opisthokonta form a strongly supported major eukaryotic grouping we name the Obazoa. Although some phylogenetic methods disagree, the balance of evidence suggests that the breviate lineage forms the deepest branch within Obazoa. We also found transcripts encoding a nearly complete integrin adhesome from Pygsuia, indicating that this protein complex involved in metazoan multicellularity may have evolved earlier in eukaryote evolution than previously thought.

Keywords: animal–fungal clade; eukaryote evolution; integrin; mitochondria; protist.

Figures

Figure 1.
Figure 1.
Micrographs of P. biforma. (a) Differential interference contrast micrograph (DIC) of an adherent amoeboid cell with a long apical flagellum, af, and prominent filose pseudopodia, f, (arrowheads) projecting from one side. (b) DIC of an adherent amoeboid cell showing the inconspicuous posteriorly directed flagellum, pf, running along the cell surface. (c) DIC of a swimming cell with two long opposed flagella. (d) Scanning election micrograph of an adherent cell with a filose pseudopodium. (e) Transmission electron micrograph (TEM) of a whole cell. (f) TEM showing the flagellar apparatus of the cell shown in (c), four serial sections deeper into the cell. Note the microtubular dorsal fan, d, closely associated with the anterior basal body, ab. (g) TEM of the pf projecting from the posterior basal body, pb. Same cell as shown in (c,d), three sections deeper than (c). (h) TEM of the mitochondrion-related organelle (m) closely associated with, d. n, nucleus; s, starch-like body; fv, food vacuole; g, Golgi apparatus. Scale bars: (b) 10 µm, (c) 10 µm (a scaled to c), (d) 2.5 µm, (e) 2 µm, (f,g) 0.5 µm, (h) 0.5 µm.
Figure 2.
Figure 2.
Phylogenetic tree estimated from the 159-protein dataset, inferred by Phylobayes-mpi under the CAT-GTR + Γ4 model. Posterior probabilities (PPs) are shown under branches. ML bootstrap support was also estimated under the LG + Γ4 + F model (upper value). Black dots indicate 100% bootstrap support and PPs of 1.0. Topologies not recovered in the ML analyses are denoted by asterisks (*).
Figure 3.
Figure 3.
Sites were sorted based on their rates of evolution and removed from the dataset from highest to lowest rate. The bootstrap values for each bipartition of interest are plotted. The dataset with 18 000 sites removed (grey bar) was analysed further; see the electronic supplementary material, figure S5. O, Opisthokonta; B, Breviatea; A, Apusomonadida.
Figure 4.
Figure 4.
(a) Domain architecture of ITA from P. biforma (Pb) compared to a canonical ITA of Homo sapiens (Hs) (ITGA5, GenBank NP_002196) and the ITA in Thecamonas trahens (Tt) [26]. (b) Domain architecture of ITB of Pb compared to a canonical ITB of Hs (ITGB1, GenBank NP_391988) and the ITB in Tt [26]. SP, signal peptide (SignalP-NN(euk)); ITA head, integrin α, β-propeller (IPR013519); FG, FG-gap (PS51470); ITA leg, integrin α-2 (IPR013649); TM, transmembrane domain; ITB head, integrin β chain (PF00362); EGF, epidermal growth factor; extracellular (IPR013111); BT, integrin-B tail (PF07965); BC, integrin-B cytoplasmic region (PF08725). Vertical purple lines represent cysteine-rich repeats (CxCxxCxC) (PS00243). The number of EGF and CxCxxCxC are indicated. (c) Phylogenetic distribution of IMAC. The inset depicts IMAC coloured in accordance with the distributions shown in the tree. Circle, innovation/gain; bar, loss. Abbreviations: vin, vinculin; pax, paxillin; tal, talin; par, parvin; pin, particularly interesting new cysteine-histidine-rich protein; FAK, focal adhesion kinase; ILK, integrin-linked kinase; αA, alpha-actinin; α, α-integrin; β, β-integrin; IP, Interpro; PF, Pfam; PS, ProSite.

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