New Lineage of Microbial Predators Adds Complexity to Reconstructing the Evolutionary Origin of Animals

The origin of animals is one of the most intensely studied evolutionary events, and our understanding of this transition was greatly advanced by analyses of unicellular relatives of animals, which have shown many “animal-specific” genes actually arose in protistan ancestors long before the emergence of animals [1–3]. These genes have complex distributions, and the protists have diverse lifestyles, so understanding their evolutionary significance requires both a robust phylogeny of animal relatives and a detailed understanding of their biology [4, 5]. But discoveries of new animal-related lineages are rare and historically biased to bacteriovores and parasites. Here, we characterize the morphology and transcriptome content of a new animal-related lineage, predatory flagellate Tunicaraptor unikontum. Tunicaraptor is an extremely small (3–5 μm) and morphologically simple cell superficially resembling some fungal zoospores, but it survives by preying on other eukaryotes, possibly using a dedicated but transient “mouth,” which is unique for unicellular opisthokonts. The Tunicaraptor transcriptome encodes a full complement of flagellar genes and the flagella-associated calcium channel, which is only common to predatory animal relatives and missing in microbial parasites and grazers. Tunicaraptor also encodes several major classes of animal cell adhesion molecules, as well as transcription factors and homologs of proteins involved in neurodevelopment that have not been found in other animal-related lineages. Phylogenomics, including Tunicaraptor, challenges the existing framework used to reconstruct the evolution of animal-specific genes and emphasizes that the diversity of animal-related lineages may be better understood only once the smaller, more inconspicuous animal-related lineages are better studied. [Display omitted] •New predatory protist (Tunicaraptor) with unique morphology is related to animals•Tunicaraptor calls into question many of the well-accepted relationships in Holozoa•Tunicaraptor possesses a unique combination of “animal-specific” gene products•Eukaryovorous flagellates may represent a major share of unicellular animal relatives Tikhonenkov et al. report a new lineage of predatory protists (Tunicaraptor) related to animals, challenging the existing phylogenomic framework used to reconstruct the evolution of “animal-specific” genes. This protist highlights the notion that eukaryovorous flagellates may represent a major fraction of the unicellu