The Capsaspora genome reveals a complex unicellular prehistory of animals

Abstract

To reconstruct the evolutionary origin of multicellular animals from their unicellular ancestors, the genome sequences of diverse unicellular relatives are essential. However, only the genome of the choanoflagellate Monosiga brevicollis has been reported to date. Here we completely sequence the genome of the filasterean Capsaspora owczarzaki, the closest known unicellular relative of metazoans besides choanoflagellates. Analyses of this genome alter our understanding of the molecular complexity of metazoans’ unicellular ancestors showing that they had a richer repertoire of proteins involved in cell adhesion and transcriptional regulation than previously inferred only with the choanoflagellate genome. Some of these proteins were secondarily lost in choanoflagellates. In contrast, most intercellular signalling systems controlling development evolved later concomitant with the emergence of the first metazoans. We propose that the acquisition of these metazoan-specific developmental systems and the co-option of pre-existing genes drove the evolutionary transition from unicellular protists to metazoans.

Exploring the evolutionary history of centrosomes

“…Major changes in cytoskeleton architecture can nevertheless result from adaptation to different ecological niches, in particular with respect to motility and feeding modes. For instance, centrioles and cilia are entirely missing in Filasteria and Nucleariida, which use actin-based filopodia to crawl along a substrate (figure 1) [45,51,52,55,56,63]. A possible scenario is that the last common ancestor of all Amorphea or even of all eukaryotes was capable of both flagellar and actin-based motility, and different lineages lost one or the other (or both) while adapting to their specific environment [26,27,[64][65][66].…”

“…Among them, the most robustly predicted by phylogenetic analyses is the supergroup Opisthokonta, which comprises animals, fungi and the smaller groups Choanoflagellatea, Filasterea, Ichthyosporea and Nucleariida [44][45][46][47]. Choanoflagellates, which are unicellular or colonial free-living uniflagellates, are considered the closest living relatives of animals [45,[47][48][49][50][51]. Filasterea comprise only two known species of filose amoebae completely lacking centrioles and cilia: the free-living marine protist Ministeria vibrans and Capsaspora owczarzaki, an endosymbiont of Biomphalaria glabrata, the intermediate snail host for intestinal schistosomiasis [46,[51][52][53].…”

“…Choanoflagellates, which are unicellular or colonial free-living uniflagellates, are considered the closest living relatives of animals [45,[47][48][49][50][51]. Filasterea comprise only two known species of filose amoebae completely lacking centrioles and cilia: the free-living marine protist Ministeria vibrans and Capsaspora owczarzaki, an endosymbiont of Biomphalaria glabrata, the intermediate snail host for intestinal schistosomiasis [46,[51][52][53]. Ichthyosporeans comprises unicellular species living in parasitic or commensal relationships with animals, mostly fish.…”

Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life

“…It includes the parabasalid Trichomonas vaginalis (43), the heterolobosean Naegleria gruberi (44), various trebouxiophyte green algae (45), Microsporidia (Opisthosporidia) (46), Glomeromycota (arbuscular mycorrhizal fungi) (47,48), and the naked foraminiferan Reticulomyxa filosa (Rhizaria) (49). It also comprises the amoeba Capsaspora owczarzaki, representing Filasterea, a small lineage related to multicellular animals and choanoflagellates, which have far more diverse proteins for cell adhesion and transcriptional regulation than encoded by the choanoflagellate genome (50). These gene sets probably allowed the transition from unicellular organisms to metazoans.…”

Phylogenetic evidence for the modular evolution of metazoan signalling pathways

“…Now known to be unique to Metazoa [24 -26], a full complement of TGF-b signalling components (TGF-b and BMP ligands, their receptors, and numerous SMAD cofactors) has been found in cnidarians [27 -29], placozoans [15], sponges [30] and, most recently, the ctenophores Mnemiopsis leidyi [31] and Pleurobrachia bachei (table 1). Non-metazoan unikonts lack not only the ligands, receptors and SMAD cofactors [17,[24][25][26], but also most of the inhibitors. This pathway is a clear example of a metazoan innovation [25], and the presence of all elements together in ctenophores suggests that this system was actively transducing extracellular signals into transcriptional responses in the ancestral metazoan.…”