The Acrasis kona genome and developmental transcriptomes reveal deep origins of eukaryotic multicellular pathways

• Published in: Nature communications 2024-11, Vol.15 (1), p.10197-19, Article 10197
• Main Authors: Sheikh, Sanea, Fu, Cheng-Jie, Brown, Matthew W., Baldauf, Sandra L.
• Format: Article
• Language: English
• Subjects: 38/22; 38/23; 38/90; 38/91; 45/88; 631/181/2806; 631/181/735; 631/208/212/2304; Amoeba; Amoeba - genetics; Autophagy; Developmental stages; Dictyostelium - genetics; Dictyostelium - growth & development; Eukaryotes; Evolutionary genetics; Extracellular matrix; Fruit bodies; Gene Transfer, Horizontal; Genes; Genome; Genome, Protozoan; Genomes; Horizontal transfer; Humanities and Social Sciences; multidisciplinary; Nucleotide sequence; Phylogeny; Proteasomes; Proteome - genetics; Proteome - metabolism; Proteomes; Protozoan Proteins - genetics; Protozoan Proteins - metabolism; Science; Science (multidisciplinary); Similarity; Transcriptome; Transcriptomes
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-54029-z

Acrasids are amoebae with the capacity 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 (the former Excavata). Here, we report the Acrasis kona genome sequence plus transcriptomes from pre-, mid- and post-developmental stages. The genome is rich in novelty and genes with strong signatures of horizontal transfer, and multigene families encode nearly half of the amoeba’s predicted proteome. Development in A. kona appears molecularly simple relative to the AGM model, Dictyostelium discoideum . However, the acrasid also differs from the dictyostelid in that it does not appear to be starving during development. Instead, developing A. kona appears to be very metabolically active, does not induce autophagy and does not up-regulate its proteasomal genes. Together, these observations strongly suggest that starvation is not essential for AGM development. Nonetheless, development in the two amoebae appears to employ remarkably similar pathways for signaling, motility and, potentially, construction of an extracellular matrix surrounding the developing cell mass. Much of this similarity is also shared with animal development, suggesting that much of the basic tool kit for multicellular development arose early in eukaryote evolution. Acrasis kona is a solitary amoeba which builds a multicellular fruiting body, despite being a distant relative of other multicellular eukaryotes. This study analysed A. kona’s genome and developmental transcriptomes and find extensive similarity with common developmental pathways of other multicellular taxa.