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Link to original content: https://pubmed.ncbi.nlm.nih.gov/26832778/
A paneukaryotic genomic analysis of the small GTPase RABL2 underscores the significance of recurrent gene loss in eukaryote evolution - PubMed Skip to main page content
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. 2016 Feb 2;11(1):5.
doi: 10.1186/s13062-016-0107-8.

A paneukaryotic genomic analysis of the small GTPase RABL2 underscores the significance of recurrent gene loss in eukaryote evolution

Marek Eliáš  1 , Vladimír Klimeš  2 , Romain Derelle  3 , Romana Petrželková  4 , Jan Tachezy  5
Affiliations

A paneukaryotic genomic analysis of the small GTPase RABL2 underscores the significance of recurrent gene loss in eukaryote evolution

Marek Eliáš et al. Biol Direct. .

Abstract

Background: The cilium (flagellum) is a complex cellular structure inherited from the last eukaryotic common ancestor (LECA). A large number of ciliary proteins have been characterized in a few model organisms, but their evolutionary history often remains unexplored. One such protein is the small GTPase RABL2, recently implicated in the assembly of the sperm tail in mammals.

Results: Using the wealth of currently available genome and transcriptome sequences, including data from our on-going sequencing projects, we systematically analyzed the phylogenetic distribution and evolutionary history of RABL2 orthologs. Our dense taxonomic sampling revealed the presence of RABL2 genes in nearly all major eukaryotic lineages, including small "obscure" taxa such as breviates, ancyromonads, malawimonads, jakobids, picozoans, or palpitomonads. The phyletic pattern of RABL2 genes indicates that it was present already in the LECA. However, some organisms lack RABL2 as a result of secondary loss and our present sampling predicts well over 30 such independent events during the eukaryote evolution. The distribution of RABL2 genes correlates with the presence/absence of cilia: not a single well-established cilium-lacking species has retained a RABL2 ortholog. However, several ciliated taxa, most notably nematodes, some arthropods and platyhelminths, diplomonads, and ciliated subgroups of apicomplexans and embryophytes, lack RABL2 as well, suggesting some simplification in their cilium-associated functions. On the other hand, several algae currently unknown to form cilia, e.g., the "prasinophytes" of the genus Prasinoderma or the ochrophytes Pelagococcus subviridis and Pinguiococcus pyrenoidosus, turned out to encode not only RABL2, but also homologs of some hallmark ciliary proteins, suggesting the existence of a cryptic flagellated stage in their life cycles. We additionally obtained insights into the evolution of the RABL2 gene architecture, which seems to have ancestrally consisted of eight exons subsequently modified not only by lineage-specific intron loss and gain, but also by recurrent loss of the terminal exon encoding a poorly conserved C-terminal extension.

Conclusions: Our comparative analysis supports the notion that RABL2 is an ancestral component of the eukaryotic cilium and underscores the still underappreciated magnitude of recurrent gene loss, or reductive evolution in general, in the history of eukaryotic genomes and cells.

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Figures

Fig. 1
Fig. 1
Annotated multiple alignment of representative RABL2 proteins sequences. The figure shows a subset of RABL2 sequences from a complete alignment provided as Additional file 3. The five conserved functionally important motifs of the Ras superfamily (G1 to G5 [45]) are marked on the top. Regions corresponding to secondary structure elements – α-helices and β-sheets – predicted for the RABL2 GTPase are indicated by series of letters “h” and “e”, respectively. The figure shows the prediction of α-helices and β-sheets as provided by PROMALS [113], but predictions using other tools were generally congruent with some differences in exact delimitation of the different elements. Note the predicted extra helix at the C-terminus that does not belong to the conserved core of a GTPase domain (comprised of the region from strand 1 to helix 5). The seven intron positions inferred to be ancestral for the RABL2 gene (see main text) are marked by consecutive numbers above the amino acid residues whose codon is located immediately upstream of the intron (phase 0) or is interrupted by the intron at the second or third position (phases 2 and 3). The phase of each intron is indicated by the number in superscript. The sequences of the extremely variable C-terminal tail encoded by the terminal ancestral exon (downstream of the 7th ancestral intron) are not aligned, as no meaningful alignment can be produced for the sequences from different major eukaryotic groups. Species abbreviations used to label the RABL2 sequences: Hsa – Homo sapiens; Bde – Batrachochytrium dendrobatidis; Ttr – Thecamonas trahens; Mba – Mastigamoeba balamuthi; Pmi – Planomonas micra; Mca – Malawimonas californiana; Tva – Trichomonas vaginalis; Ngr – Naegleria gruberi; Cre – Chlamydomonas reinhardtii; Cpx – Cyanophora paradoxa; Gth – Guillardia theta; Ehu – Emiliania huxleyi; Pso – Phytophthora sojae; Otr – Oxytricha trifallax; Bna – Bigelowiella natans. Sequence identifiers are available in Additional file 1: Table S1
Fig. 2
Fig. 2
Maximum likelihood phylogenetic tree of RABL2 protein sequences. The tree was constructed from an alignment of complete or nearly complete RABL2 sequences (158 amino acid positions) using RAxML and the LG + Γ + F substitution model. Bootstrap support values are shown when higher than 50 %. Sequence identifiers are provided in Additional file 1: Table S1. Sequences representing the same major eukaryotic group (not necessarily monophyletic in the tree) are indicated with the same colour, sequences revealed as apparent contaminations (see main text and Additional file 2) are shown in black
Fig. 3
Fig. 3
Occurrence of RABL2 genes in major eukaryotic lineages. The dendrogram showing the phylogenetic relationships among the taxa is drawn on the basis of current phylogenetic and phylogenomic literature. Multifurcations in the tree indicate lack of consensus on the topology in particular phylogenetic areas. The root of the tree is placed according to the most recent rooting hypothesis [53]. The position of Metamonada with respect to the root is unclear; sometimes they are placed sister to the group Discoba, while other analyses suggest metamonads may be sister to malawimonads or represent a deep group with unresolved affiliation. However, the unsettled position of metamonads, as well as alternative root positions suggested by other authors, do not change the inference on the occurrence of a RABL2 gene already in the LECA. For several eukaryotic lineages sufficiently complete genome or transcriptome data are still not available, so the presence or absence of RABL2 genes in them cannot be ascertained (indicated by the question marks)
Fig. 4
Fig. 4
A fine-scale map of the phylogenetic distribution and losses of RABL2 genes in eukaryotes. The dendrogram indicating the relationships among the taxa was drawn with the same rationale as the one on Fig. 3. For each taxon the presence/absence of a RABL2 ortholog and of a cilium is indicated on the right (evidence for the presence of absence of a cilium for the different taxa is based an extensive literature survey complemented for some taxa with checking the presence of homologs of cilium-specific genes in their genome or transcriptome sequences). Well established (named) clades, where all species analyzed either possessed or lacked a RABL2 ortholog, were collapsed and displayed as a single terminal branch. The metazoan clade, which includes both RABL2-possessing and RABL2-lacking species, was also collapsed and is shown in detail in a separate scheme (Fig. 5). The number of the species representing the clade in our sample (see Additional file 1: Table S1 for their identity) is indicated in square brackets. The meaning of the symbols used for indicating the distribution and loss of RABL2 and the cilium is explained in Fig. 5. The position of the fungus Olpidium bornovanus is shown sister to all traditionally defined Eumycota (paraphyletic “Zygomycota” plus Dikarya) to conservatively indicate only a single unique loss of RABL2 in this group, but the dashed lines indicate that Olpidium may be specifically related to some “zygomycetes”, which would increase the number of RABL2 losses in Fungi (see main text for details)
Fig. 5
Fig. 5
A fine-scale map of the phylogenetic distribution and losses of RABL2 genes in Metazoa. The figure was rendered using the same convention as Fig. 4
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