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Unravelling the unicellular prehistory of metazoans with functional analyses and single-cell genomics

Final Report Summary - PREMETAZOANEVOLUTION (Unravelling the unicellular prehistory of metazoans with functional analyses and single-cell genomics)

The goal of the project was to better understand how multicellular animals emerged from their unicellular ancestor. Previous data from our and other labs, had already shown that the unicellular ancestor of animals already had a complex repertoire of genes involved in “multicellular” functions, such as cell adhesion, cell signaling, and transcriptional regulation. In this grant, we wanted to have a better understanding of the gene repertoire at the unicellular ancestor by sequencing taxa that we can not culture (using single-cell genomics). We also wanted to elucidate whether the unicellular ancestor had animal-like mechanisms of cell differentiation and gene and genomic regulation. Finally, we wanted to have an understanding of the potential ancestral role of those proteins that are key to animal multicellularity and that are present in the closest unicellular relatives of animals. To tackle all these questions, we work with some of the closest unicellular relatives of animals, some of which we are pushing to become model systems to understand the unicellular-to-multicellular transition that gave rise to animals.

Thanks to the data generated during this project, we have a much clear picture of animals origins. To start with, we have generated new genome data from organisms that were before unaccessible for genome sequencing because they can not be cultured. Using single-cell genomics, we sequenced different uncultured unicellular organisms closely related to animals and inferred the evolutionary history of “multicellular” genes, detecting genes that were previously thought to be exclusive to animals. We also inferred the potential ancestral function of some genes that are now key to animal multicellularity (such as integrins and the transcription factors Myc or Brachyury). This experiments revealed an unexpected conservation of transcription factor regulatory networks between animals and their unicellular relatives, something that challenges previous assumptions about the role of those gene regulatory networks in animal origins. Quite surprisingly, We also found animal-like mechanisms of cell differentiation and genomic regulation in a close unicellular relative of animals, which implies those mechanisms of cell differentiation were already present before animal origins, pushing much earlier their origin. Overall, we have been able to generate a lot of new data in unicellular relatives of animals that are challenging our previous view of animal origins and picturing, instead, a complex unicellular ancestor of animals already pre-equipped with genes and molecular mechanisms to be a complex animal. How specifically the transition took place remains unanswered, but, thanks to this grant, we know much more about the ancestor of animals, and we have put the basis to tackle this question in a more informative way.