Abstract
BackgroundThe origin of animals from their unicellular ancestor was one of the most important events in evolutionary history, but the nature and the order of events leading up to the emergence of multicellular animals are still highly uncertain. The diversity and biology of unicellular relatives of animals have strongly informed our understanding of the transition from single-celled organisms to the multicellular Metazoa. Here, we analyze the cellular structures and complex life cycles of the novel unicellular holozoans Pigoraptor and Syssomonas (Opisthokonta), and their implications for the origin of animals.ResultsSyssomonas and Pigoraptor are characterized by complex life cycles with a variety of cell types including flagellates, amoeboflagellates, amoeboid non-flagellar cells, and spherical cysts. The life cycles also include the formation of multicellular aggregations and syncytium-like structures, and an unusual diet for single-celled opisthokonts (partial cell fusion and joint sucking of a large eukaryotic prey), all of which provide new insights into the origin of multicellularity in Metazoa. Several existing models explaining the origin of multicellular animals have been put forward, but these data are interestingly consistent with one, the “synzoospore hypothesis.”ConclusionsThe feeding modes of the ancestral metazoan may have been more complex than previously thought, including not only bacterial prey, but also larger eukaryotic cells and organic structures. The ability to feed on large eukaryotic prey could have been a powerful trigger in the formation and development of both aggregative (e.g., joint feeding, which also implies signaling) and clonal (e.g., hypertrophic growth followed by palintomy) multicellular stages that played important roles in the emergence of multicellular animals.
Highlights
The origin of animals from their unicellular ancestor was one of the most important events in evolutionary history, but the nature and the order of events leading up to the emergence of multicellular animals are still highly uncertain
Three novel holozoan taxa were isolated from a freshwater pool (Syssomonas multiformis) and the silty sand on the littoral of a freshwater lake (Pigoraptor vietnamica) in tropical Vietnam, and from the sediment of a freshwater temporary water body in Tierra del Fuego (Pigoraptor chileana)
As we acquire more information about the biology of known unicellular relatives of animals and, importantly, describe diverse new species of unicellular Holozoa, models for the evolutionary histories of specific characteristics that contributed to the emergence of multicellularity in animals can be evaluated more meaningfully
Summary
The origin of animals from their unicellular ancestor was one of the most important events in evolutionary history, but the nature and the order of events leading up to the emergence of multicellular animals are still highly uncertain. Information on the diversity and biology of the unicellular relatives of animals, their placement within the phylogenetic tree of opisthokonts, and the identification of molecular and morphological traits thought to be specific for animals within their unicellular sister lineages has all strongly informed our understanding of the transition from single-celled organisms to the multicellular Metazoa [15,16,17,18,19]. Only three unicellular lineages, the choanoflagellates, filastereans, and ichthyosporeans, as well as Corallochytrium limacisporum, a mysterious marine osmotrophic protist described in association with corals, have been described as collectively being sisters to animals Together with animals, they form the Holozoa within the Opisthokonta [19,20,21]. Molecular data predict a cryptic flagellated stage for Corallochytrium [19]
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