Novel Predators Reshape Holozoan Phylogeny and Reveal the Presence of a Two-Component Signaling System in the Ancestor of Animals

• Published in: Current biology 2017-07, Vol.27 (13), p.2043-2050.e6
• Main Authors: Hehenberger, Elisabeth, Tikhonenkov, Denis V., Kolisko, Martin, del Campo, Javier, Esaulov, Anton S., Mylnikov, Alexander P., Keeling, Patrick J.
• Format: Article
• Language: English
• Subjects: Animals; Biological Evolution; Eukaryota - classification; Eukaryota - genetics; Eukaryota - physiology; Evolution, Molecular; Fetal Proteins - genetics; Fetal Proteins - metabolism; Holozoa; multicellularity; phylogenomics; Predatory Behavior; RNA, Ribosomal, 18S - genetics; Signal Transduction; T-Box Domain Proteins - genetics; T-Box Domain Proteins - metabolism; transcription factor; two-component signaling
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2017.06.006

Our understanding of the origin of animals has been transformed by characterizing their most closely related, unicellular sisters: the choanoflagellates, filastereans, and ichthyosporeans. Together with animals, these lineages make up the Holozoa [1, 2]. Many traits previously considered “animal specific” were subsequently found in other holozoans [3, 4], showing that they evolved before animals, although exactly when is currently uncertain because several key relationships remain unresolved [2, 5]. Here we report the morphology and transcriptome sequencing from three novel unicellular holozoans: Pigoraptor vietnamica and Pigoraptor chileana, which are related to filastereans, and Syssomonas multiformis, which forms a new lineage with Corallochytrium in phylogenomic analyses. All three species are predatory flagellates that feed on large eukaryotic prey, and all three also appear to exhibit complex life histories with several distinct stages, including multicellular clusters. Examination of genes associated with multicellularity in animals showed that the new filastereans contain a cell-adhesion gene repertoire similar to those of other species in this group. Syssomonas multiformis possessed a smaller complement overall but does encode genes absent from the earlier-branching ichthyosporeans. Analysis of the T-box transcription factor domain showed expansion of T-box transcription factors based on combination with a non-T-box domain (a receiver domain), which has not been described outside of vertebrates. This domain and other domains we identified in all unicellular holozoans are part of the two-component signaling system that has been lost in animals, suggesting the continued use of this system in the closest relatives of animals and emphasizing the importance of studying loss of function as well as gain in major evolutionary transitions. •New taxa restructure and stabilize the phylogenomic framework of Holozoa•A two-component signaling system is present in the ancestor of animals Hehenberger et al. describe three novel Holozoa and infer an updated phylogenomic framework for this group, in the course recovering a new lineage. Using comparative genomics, they show the presence of a two-component signaling system across all unicellular Holozoa and suggest the loss of this signaling system with the origin of animals.