Chemical factors induce aggregative multicellularity in a close unicellular relative of animals
Núria Ros-Rocher, Ria Q. Kidner, Catherine Gerdt, +2, and Joseph P. Gerdt
Authors Info & Affiliations
Edited by Joan Strassmann, Washington University in St. Louis, St. Louis, MO; received November 30, 2022; accepted February 14, 2023
April 24, 2023
120 (18) e2216668120
https://doi.org/10.1073/pnas.2216668120
Significance
Whether the first multicellular animals utilized chemical cues to regulate cellular aggregation remains poorly studied. We discovered that aggregation of a unicellular close animal relative is induced by chemical cues, as observed in some animals and other unicellular species. This discovery expands the prevalence of chemically regulated multicellularity in unicellular animal relatives, which suggests that this trait may have been common in the close unicellular ancestors of animals. Our findings also yield a biochemical tool to further dissect the stages of aggregation in an emerging unicellular model and determine the extent of their homology to aggregation mechanisms in animals.
Abstract
Regulated cellular aggregation is an essential process for development and healing in many animal tissues. In some animals and a few distantly related unicellular species, cellular aggregation is regulated by diffusible chemical cues. However, it is unclear whether regulated cellular aggregation was part of the life cycles of the first multicellular animals and/or their unicellular ancestors. To fill this gap, we investigated the triggers of cellular aggregation in one of animals’ closest unicellular living relatives—the filasterean Capsaspora owczarzaki. We discovered that Capsaspora aggregation is induced by chemical cues, as observed in some of the earliest branching animals and other unicellular species. Specifically, we found that calcium ions and lipids present in lipoproteins function together to induce aggregation of viable Capsaspora cells. We also found that this multicellular stage is reversible as depletion of the cues triggers disaggregation, which can be overcome upon reinduction. Our finding demonstrates that chemically regulated aggregation is important across diverse members of the holozoan clade. Therefore, this phenotype was plausibly integral to the life cycles of the unicellular ancestors of animals.
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