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

Abstract

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 protist relatives of animals, which have shown many “animal-specific” genes actually arose in protistan ancestors long before the emergence of animals. These genes have sometimes 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. But discoveries of new animal-related lineages are rare and biased to bacteriovores and parasites. Here, we characterize the morphology, life cycle and transcriptome content of a new animal-related lineage, represented by the predatory flagellate, Tunicaraptor unikontum. Although it survives by preying on other eukaryotes, Tunicaraptor is an extremely small (3-5 μm) and morphologically simple cell; closely resembling some fungal zoospores. The Tunicaraptor transcriptome encodes a full complement of flagellar genes, which are only common to predatory animal relatives and missing in microbial parasites and grazers. Tunicaraptor also encodes several major classes of animal cell adhesion molecules and transcription factors and 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.