MULTICELLEXPEVO · Reconstructing the origins of animal multicellularity using experimental evolution

Reconstructing the origins of animal multicellularity using experimental evolution

All living animals evolved from a single-celled ancestor. Understanding how this ancestor evolved to become the first multicellular animal is crucial to trace our origins. To date comparative genomic and phylogenetic comparisons of meta-zoans genomes with their closest unicellular relatives was the unique research strategy to unravel animal origins of mul-ticellularity. Phylogenomic analyses have shown that animals are closely related to three unicellular lineages: choanoflagellates, filastereans and ichthyosporeans, which together form the Holozoa clade. Each lineage uses a distinct developmental mode that includes transient simple multicellular forms. Choanoflagellates undergo colo-nial clonal development; the filasterean Capsaspora owczarzaki has an aggregative multicellular stage; and most ichthyosporeans form multinucleated coenocytes. To date, it is still unknown from which developmental mode animals emerged. Both choanoflagellates and filastereans are highly studied and genetic tools are currently in development in order to answer this question. However, ichthyosporeans have received less attention despite their attractive coenocytic lifecycle. This developmental mode comprises a growth stage in which nuclei divide synchronously within a common cytoplasm. The coenocyte then undergoes plasma membrane cleavage followed by release of new-born cells. By better understanding the cell biology of these interesting organisms, we were hoping to better understand how ancestral developmental mechanisms first evolved and how these compare with animal developmental processus. Such project is important for society because it would allow us better to understand the evolution of animals inclduing us humans. It would also allow us to unravel the ancestral mechanism of transition between unicellular organisms and multicellular ones. More specifically, the MULTICELLEXPEVO project aimed to better understand requirements needed for the unicellular to multicellular transition. It clearly focused on investigating the role of actin and microtubule cytoskeletons in the formation of the aggregative stage as well as the development of genetic tools through experimental evolution and random mutagenesis using Capsaspora owczarzaki as a model. Despite being focalized on Capsaspora owczarzaki , many aspects of this project were done using the ichthyosporean Sphaeroforma arctica for several technical reasons explained below. However, our project concluded in general that unicellular holozoan use similar morphological processes during their transient multicellular stage. More specifically, we showed that S. arctica undergo cellularization using plasma membrane invagination forming a transinet epithelium-like layer of cells. Such cellularization ressembled the cellularization of the Drosophila embryo.

Data: CORDIS, © European Union