L’origen de la multicel·lularitat en animals: una aproximació genòmica the origin of multicellularity in animals: a genomic approach
- Autores: Xavier Grau Bové
- Directores de la Tesis: Iñaki Ruiz Trillo (dir. tes.), Marta Riutort Leon (tut. tes.)
- Lectura: En la Universitat de Barcelona ( España ) en 2017
- Idioma: español
- Tribunal Calificador de la Tesis: Pedro Martínez Serra (presid.), Elena Casacuberta Suñer (secret.), Daniel J. Richter (voc.)
- Programa de doctorado: Programa de Doctorado en Genética por la Universidad de Barcelona
- Materias:
- Enlaces
- Tesis en acceso abierto en: TESEO
- Resumen
The origin of multicellularity in animals is a hallmark event in evolution, that was accompanied by profound changes in the genomes, development and cell biology processes of the animal ancestors. I here analyze the origin of animals from the point of view of comparative genomics and phylogenomics, aiming to reconstruct the key innovations behind the transition to multicellularity by taking advantage of comparative analyses with the closest unicellular relatives of animals within the Holozoa clade.
This project has been carried out in a two-fold approach. First, I aimed to establish the taxonomy and phylogenetic relationships between animals and unicellular holozoan lineages using phylogenomic approaches – with particular interest in the placement of the enigmatic protist Corallochytrium limacisporum in the opisthokont tree of life. Second, reconstructing the genomic content of key ancestral nodes, before and after the advent of multicellularity, in order to pinpoint the specific changes that underpinned the origin of Metazoa.
Our phylogenomic analyses resulted in the establishment of four clades in Holozoa: Teretosporea (containing C. limacisporum and ichthyosporean protists), Filasterea (2 amoebas, including Capsaspora owczarzaki) and Choanoflagellata (flagellated protists, sometimes colonial), as well as multicellular Metazoa. Using this robust phylogenetic framework, we could then interrogate the genome content of extant organisms in order to confidently reconstruct ancestral characters. The reconstructions of ancestral gene contents were focused on the ubiquitin signaling tool-kit---a set of gene families involved in post-translational protein modification in eukaryotes---, myosin molecular motors and transcription factors. For all these genetic tool-kits, we uncovered a continued state of innovation in terms of de novo gene origin, protein diversification and massive paralogy before in pre-metazoan lineages. These evolutionary trajectories can sometimes be associated with co-option of ancestral gene tool-kits for animal-specific functions, and reinforce the idea that the holozoan unicellular ancestor from which animals evolved was not a genetically simple organism as initially proposed – rather, it already possessed a remarkably complex ubiquitin signaling tool-kit and more myosin orthologous families than extant animals, in line with previous reports highlighting the premetazoan origin of cell-to-cell adhesion mechanisms and developmental transcription factors and signaling systems.
In order to expand the outlook of comparative genomic analyses of Holozoa, I then aimed to establish the evolution of genome architecture in premetazoan lineages. Thus, we sequenced, annotated and analyzed the genomes of 6 ichthyosporeans (Creolimax fragrantissima, Chromosphaera perkinsii, Sphaeroforma arctica, Ichthyophonus hoferi, Abeoforma whisleri and Pirum gemmata) and the corallochytrean C. limacisporum; and compared them to other unicellular holozoans (C. owczarzaki and the choanoflagellates Monosiga brevicollis and Salpingoeca rosetta) and animals. As mentioned above, analyses of animal unicellular relatives uncovered the premetazoan origin of many genes with multicellularity-related functions, e.g. developmental transcription factors or cell adhesion proteins. Here we show that genome architecture evolution was equally dynamic: an early burst of gene diversity in the holozoan ancestor, enriched in signaling genes, transcription factors and extracellular-matrix adhesion genes, was followed by independent episodes of synteny disruption, intron gain, and genome expansions in both unicellular and multicellular lineages.
Finally, we correlated the evolution of alternative splicing-based transcriptome regulation with the evolution of exon/intron gene structure in holozoans. We unraveled a universal code of alternative splicing determination that determines the frequency of animal-like exon skipping patterns whenever large and intron-rich genomes are a product of neutral or adaptive evolution. We can thus associate ancestral reconstructions of genome architecture with a key source of phenotypic innovation at the transcriptome regulatory level, and date the origin of alternative splicing-rich animals at the last common ancestor of Bilateria within metazoans. This result highlights how the analysis of genome architecture can reveal the evolutionary pressures faced by ancestral lineages, as well as enabling the inference of ancestral states of transcriptome regulation such as AS.
These results demonstrate that comparative genomics and ancestral reconstructions constitute a powerful tool for evolutionary analysis of ancestral eukaryotes: not only it allows to uncover the primary composition of ancestral genomes; it can also fuel inferences regarding their transcriptomic regulation and the role played by non-genomic sources of evolutionary innovation.
