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, 3 (5), e2098

Multigene Phylogeny of Choanozoa and the Origin of Animals

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Multigene Phylogeny of Choanozoa and the Origin of Animals

Kamran Shalchian-Tabrizi et al. PLoS One.

Abstract

Animals are evolutionarily related to fungi and to the predominantly unicellular protozoan phylum Choanozoa, together known as opisthokonts. To establish the sequence of events when animals evolved from unicellular ancestors, and understand those key evolutionary transitions, we need to establish which choanozoans are most closely related to animals and also the evolutionary position of each choanozoan group within the opisthokont phylogenetic tree. Here we focus on Ministeria vibrans, a minute bacteria-eating cell with slender radiating tentacles. Single-gene trees suggested that it is either the closest unicellular relative of animals or else sister to choanoflagellates, traditionally considered likely animal ancestors. Sequencing thousands of Ministeria protein genes now reveals about 14 with domains of key significance for animal cell biology, including several previously unknown from deeply diverging Choanozoa, e.g. domains involved in hedgehog, Notch and tyrosine kinase signaling or cell adhesion (cadherin). Phylogenetic trees using 78 proteins show that Ministeria is not sister to animals or choanoflagellates (themselves sisters to animals), but to Capsaspora, another protozoan with thread-like (filose) tentacles. The Ministeria/Capsaspora clade (new class Filasterea) is sister to animals and choanoflagellates, these three groups forming a novel clade (filozoa) whose ancestor presumably evolved filose tentacles well before they aggregated as a periciliary collar in the choanoflagellate/sponge common ancestor. Our trees show ichthyosporean choanozoans as sisters to filozoa; a fusion between ubiquitin and ribosomal small subunit S30 protein genes unifies all holozoa (filozoa plus Ichthyosporea), being absent in earlier branching eukaryotes. Thus, several successive evolutionary innovations occurred among their unicellular closest relatives prior to the origin of the multicellular body-plan of animals.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Phylogeny of the Choanozoa and other unikont eukaryotes reconstructed by the maximum likelihood method for 78 protein-coding genes.
Numbers beside the internal nodes are maximum likelihood bootstrap values obtained from RaxML and Bayesian MCMC posterior probabilities. Black circles indicate 100% bootstrap support and 1.00 posterior probability values.
Figure 2
Figure 2. Domain structure of selected annotated sequences.
A: hedgehog and B: Notch homologues. The illustrated domains are some of those found by searches against the Conserved Domain Database. Numbers at the species names are accession numbers, protein IDs from the Joint Genome Institute (JGI) and references where annotation recently have been presented. Domain structure identified in Ministeria is compared with animals - Porifera (Amphimedon and Oscarella), Cnidaria (Nematostella) and Chordata (Homo) - and the choanoflagellate Monosiga. Abbreviations: Hh-signal domain, N-terminal hedgehog domain; Hint cleavage site, cleavage site of the C-terminal hedgehog domain; Hint domain, C-terminal hedgehog domain; Notch(DSL), Notch domain also called Delta Serrate Ligand; EGF, epidermal growth factor domain; NL, domain found in Notch and Lin-12; NOD, NOD region; NODP, NODP region; ANK, ankyrin reapeats; PTP, protein tyrosine phosphatase.
Figure 3
Figure 3. Evolutionary relationships among animals and fungi and their closest unicellular relatives (Choanozoa, Protozoa).
The five choanozoan classes (bold) form at least four distinct clades, one probably related to fungi and the others to animals. Innovations in pseudopod character and their multiple losses with the origin of cell walls during nutritional shifts from engulfing prey (phagotrophy) to saprotrophy or parasitism are indicated by bars. In the common ancestor of animals and choanoflagellates a subset of the filozoan actin-supportd tentacles aggregated as a collar around the cilium ( = flagellum) for filter feeding. Epithelia and connective tissue made the first animals: the filter-feeding sponges.

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