The opisthokont tree of life. Who are the closest unicellular relatives of animals and fungi?
The Opisthokonta clade is the group of eukaryotes that comprises animals, fungi, and several unicellular taxa. By obtaining genomic and transcriptomic data from different opisthokont taxa and performing phylogenomic analyses our lab has defined (and continues to define) a well resolved phylogenetic tree of the opisthokonts.
Such a tree provides the adequate phylogenetic backbone in which to ask different evolutionary questions. Our current view of the opisthokonts is depicted in the schematic tree shown in the figure. There are two major clades: the Holozoa and the Holomycota. The Holozoa includes Teretosporea (Corallochytrea and Ichthyosporea), Filasterea, Choanoflagellata, and Metazoa. The Holomycota includes Nucleariidae, Opisthosporidia, and Fungi.
Our current view of Opisthokonts
–Torruella, G., de Mendoza, A., Grau-Bové, X., Antó, M., A. Chaplin, M., del Campo, J., Eme, L., Pérez-Cordón, G., M. Whipps, C., M. Nichols, K., Paley, R., Roger, A.J., Sitjà-Bobadilla, A., Donachie, S., and Ruiz-Trillo, I. (2015). Phylogenomics reveals convergent evolution of lifestyles in close relatives of animals and fungi. Current Biology 25(18):2404-10.
–Torruella, G., Derelle, R., Paps, J., Lang, B. F., Roger, A. J., Shalchian-Tabrizi, K. & Ruiz-Trillo, I. (2012) Phylogenetic relationships within the Opisthokonta based on phylogenomic analyses of conserved single copy protein domains. Molecular Biology and Evolution 29(2): 531-544.
–Ruiz-Trillo, I., Roger, A. J., Burger, G., Gray, M. W. & Lang, B F. (2008) A phylogenomic investigation into the origin of Metazoa. Molecular Biology and Evolution 25 (4): 664-672.
The unicellular ancestor of animals had a rich repertoire of genes involved in multicellular functions
By comparing the genomes of animals with the genomes of their closest unicellular relatives we have been able to infer the gene content of the unicellular ancestor of animals. Interestingly, we found that this ancestor already had a rich repertoire of genes key to multicellular function and animal development.
Among the genes present in the ancestor are some that were previously believed to be exclusive to animals, such as integrins, protein tyrosine kinases, and several transcription factors such as Runx, NFKappa, T-box, or Grainyhead. Interestingly, some of those genes were secondarily lost in choanoflagellates, which indicates that a complete taxon sampling is key when addressing evolutionary questions.
The unicellular ancestor of animals had a complex regulatory genome.
By analyzing the epigenome of Capsaspora (one of the closest unicellular relatives of animals), we have shown that the unicellular ancestor of animals already had a complex regulatory genome. In particular that ancestor already had the capacity to regulate temporal cell types along its life cycle via regulation of gene expression and differential histone marks. It also had animal-like long non-coding RNAs, as well as conserved transcription factor regulatory networks (such as the network of Brachyury, a gene involved in gastrulation in Bilateria).
One important difference between animals and Capsaspora, though, is the lack of distal enhancer regulation. Capsaspora has proximal cis-regulation, but it lacks the distal regulatory regions, known as enhancers, of animals. This may indeed be a key acquisition that allowed animals to have a more specific regulation of the different cell types.
The last common eukaryotic ancestor (LECA) was already complex
By analyzing several gene families we have shown that the last common eukaryotic ancestor (LECA) had a rich repertoire of genes involved in cytoskeleton (myosins) and regulation (HECT, ubiquitin signaling, transcription factors, and GPCRs). Most of those were also subsequently expanded in lineages with complex multicellularity, such as in animals and plants.
-de Mendoza, A., Sebe-Pedros, A., Sestak, M. S., Matejcic, M., Torruella, G., Domazet-Loso, T., & Ruiz-Trillo, I. (2013). Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages. Proc Natl Acad Sci U S A, 110(50), E4858–66. https://doi.org/10.1073/pnas.1311818110
-de Mendoza, A., Sebe-Pedros, A., & Ruiz-Trillo, I. (2014). The Evolution of the GPCR Signaling System in Eukaryotes: Modularity, Conservation, and the Transition to Metazoan Multicellularity. Genome Biol Evol, 6(3), 606–619. https://doi.org/10.1093/gbe/evu038
-Grau-Bove, X., Sebe-Pedros, A., & Ruiz-Trillo, I. (2013). A Genomic Survey of HECT Ubiquitin Ligases in Eukaryotes Reveals Independent Expansions of the HECT System in Several Lineages. Genome Biol Evol, 5(5), 833–847. https://doi.org/10.1093/gbe/evt052 -Grau-Bové, X., Sebé-Pedrós, A., & Ruiz-Trillo, I. (2015). The eukaryotic ancestor had a complex ubiquitin signaling system of archaeal origin. Mol Biol Evol, 32(3), 726–739. https://doi.org/10.1093/molbev/msu334 -Sebe-Pedros, A., Grau-Bove, X., Richards, T. A., & Ruiz-Trillo, I. (2014). Evolution and classification of myosins, a paneukaryotic whole-genome approach. Genome Biol Evol, 6(2), 290–305. https://doi.org/10.1093/gbe/evu013