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

Abstract

BackgroundThe 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.ResultsUsing 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.ConclusionsOur 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.ReviewersThis article was reviewed by Berend Snel and James O. McInerney.Electronic supplementary materialThe online version of this article (doi:10.1186/s13062-016-0107-8) contains supplementary material, which is available to authorized users.

The CEP19-RABL2 GTPase Complex Binds IFT-B to Initiate Intraflagellar Transport at the Ciliary Base

“…Rab-like protein 2 (RABL2) is a small GTPase not belonging to any subfamily within the small GTPase superfamily (Diekmann et al, 2011), but is thought to be an ancestral GTPase that exists in the last eukaryotic common ancestor (Elias et al, 2016). Although Rab-like proteins (RABL2-6) have little sequence similarity, two out of five RABL proteins, RABL4/IFT27 and RABL5/IFT22, are highly conserved components of the IFT-B complex.…”

“…Given the importance of RABL2B in cilium formation and its highly conserved G1-G5 GTPase domains (Elias et al, 2016), we hypothesized that RABL2B engages in a conserved GTPase cycle critical for cilium assembly. To understand the RABL2B GTPase cycle, we first constructed classical alleles disrupting the GTPase and exchange activities.…”

“…Since the rice and thale cress sequences aligned better with FOPNL (PTHR15431), orthology for these two genes reported in OG5_133356 was manually removed. Data from (Elias et al, 2016) for RABL2, in addition to the first 51 results of an NCBI BLAST search of the Nematostella vectensis sequences for FOP, CEP19, and CEP350 using default parameters, were used to identify additional orthologs to include in the table.…”

The plastid genome of some eustigmatophyte algae harbours a bacteria-derived six-gene cluster for biosynthesis of a novel secondary metabolite

“…These form part of a separate, broader EboF clade that also includes sequences from two unrelated eukaryotic groups, the so-called PX clade of ochrophyte algae (Phaeophyceae, Schizocladia ischiensis , Phaeothamnion confervicola , Vaucheria litorea ) and the rhizarian P. brassicae (figure 8). An EboF sequence from strain RCC2339 (an unidentified organism that appears to be a green alga representing the ‘prasinophyte’ clade VIIB) may also be affiliated with this broader eukaryotic clade, but statistical support for this is lacking and the authenticity of this sequence is uncertain, as it is derived from a large transcriptome project known to be plagued with contaminations [74]. The final eukaryotic EboF sequence in our analysis came from a transcriptome assembly of the liverwort Frullania sp.…”

The Trypanosome Exocyst: A Conserved Structure Revealing a New Role in Endocytosis

“…The intervening period of over a billion years subsequently moulded these ancestral transport systems by both losses and gains to those now present in living cells [60]. Secondary loss of ancestral components is quite common,and likely a response to the requirements of individual organisms or lineages, and are reasonably easy to identify by comparative genomics [61]. By contrast, lineage-specific modifications, which are potentially very common, are difficult to identify in silico .…”