Deep origins of eukaryotic multicellularity revealed by the Acrasis kona genome and developmental transcriptomes

Abstract

Abstract Acrasids are large, fast-moving, omnivorous amoebae. However, under certain conditions, they can also cooperate to form multicellular fruiting bodies in a process known as aggregative multicellularity (AGM). This makes acrasids the only known example of multicellularity among the earliest branches of eukaryotes (formerly superkingdom Excavata) and thus the outgroup to all other known multicellular eukaryotes. We have sequenced the genome of Acrasis kona, along with transcriptomes from cells in pre-, mid- and post-development. We find the A. kona genome to be rich in novelty, genes acquired by horizontal transfer and, especially, multigene families. The latter include nearly half of the amoeba’s protein coding capacity, and many of these families show differential expression among life cycle stages. Development in A. kona appears to be molecularly simple, requiring substantial upregulation of only 449 genes compared to 2762 in the only other AGM model, Dictyostelium discoideum. However, unlike the dictyostelid, developing A. kona also does not appear to be starving, being instead very metabolically active and inducing neither autophagy nor increasing ubiquitin-tagged proteolysis. Thus, contrary to current expectations, starvation does not appear to be essential for AGM development. Moreover, despite the ~ 2 billion years of evolution separating the two amoebae, their development appears to employ remarkably similar pathways for signaling, motility and construction of an extracellular matrix surrounding the developing cell mass. In addition, much of this similarity is shared with the clonal multicellularity of animals. This makes the acrasid something of a “bare bones” developmental model and suggests that much of the basic tool kit for multicellular development arose very early in eukaryotic evolution.