Molecular Phylogeny of Unikonts: New Insights into the Position of Apusomonads and Ancyromonads and the Internal Relationships of Opisthokonts

Abstract

The eukaryotic supergroup Opisthokonta includes animals (Metazoa), fungi, and choanoflagellates, as well as the lesser known unicellular lineages Nucleariidae, Fonticula alba, Ichthyosporea, Filasterea and Corallochytrium limacisporum. Whereas the evolutionary positions of the well-known opisthokonts are mostly resolved, the phylogenetic relationships among the more obscure lineages are not. Within the Unikonta (Opisthokonta and Amoebozoa), it has not been determined whether the Apusozoa (apusomonads and ancyromonads) or the Amoebozoa form the sister group to opisthokonts, nor to which side of the hypothesized unikont/bikont divide the Apusozoa belong. Aiming at elucidating the evolutionary tree of the unikonts, we have assembled a dataset with a large sampling of both organisms and genes, including representatives from all known opisthokont lineages. In addition, we include new molecular data from an additional ichthyosporean (Creolimax fragrantissima) and choanoflagellate (Codosiga botrytis). Our analyses show the Apusozoa as a paraphyletic assemblage within the unikonts, with the Apusomonadida forming a sister group to the opisthokonts. Within the Holozoa, the Ichthyosporea diverge first, followed by C. limacisporum, the Filasterea, the Choanoflagellata, and the Metazoa. With our data enriched tree, it is possible to pinpoint the origin and evolution of morphological characters. As an example, we discuss the evolution of the unikont kinetid.

Exploring the evolutionary history of centrosomes

“…This led to the hypothesis, already formulated in the late 1800s by both James Clark and Haeckel, that animals evolved from a colonial choanoflagellate [66,91,92]. In support of it, molecular phylogenies have consistently found the choanoflagellates to be the sister group to Metazoa [45,47,[49][50][51] and sponges are often considered the most basal animal taxon-although this is still highly debated [43,93,94]. The hypothesis that our unicellular ancestors were choanoflagellate-like seems hard to reconcile with the idea that the common ancestor was also capable of amoeboid motility.…”

“…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].…”

“…There is a general consensus that the supergroup Amoebozoa is the sister group to Opisthokonta [42,47,[57][58][59]. Amoebozoa constitute a large ensemble of amoebae and flagellates that includes Entamoeba histolytica, a pathogen responsible for amoebic dysentery, and slime moulds such as D. discoideum and P. polycephalum.…”

“…In addition, they form pseudopodia from their ventral surface, which are involved in prey capture but not motility [66]. Recent molecular phylogenies support that either the whole phylum, which comprises the genera Apusomonadida and Ancyromonadida, or Apusomonadida only, is the sister group to Opisthokonta, and hence that they branched off of the main amorphean lineage later than Amoebozoa [47,53,81] ( figure 1). This suggests that the last common ancestor of Apusozoa and opisthokonts was itself an excavate-like biflagellate, and hence that Amoebozoa and opisthokonts evolved from two different flagellated ancestors.…”

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

“…In addition to those mentioned (the different Hacrobia), the microkingdoms include Apusomonadida and Breviatea (recently united with Opisthokonta as a new major eukaryotic grouping dubbed Obazoa) (125), Ancyromonadida (=Planomonadida), Mantamonadida, Rigifilida, and Collodictyonida (=Diphyllatea). The latter four groups appear to be deeply diverged lineages branching close to Obazoa and the supergroup Amoebozoa (126)(127)(128)(129), but their exact position is not known. Other such minor deep groups will surely be described, as their existence is suggested by culturing-independent environmental surveys of small subunit rRNA genes, such as the NAMAKO-1 and -2 lineages found in anoxic habitats (130).…”