How did animal multicellularity emerge from a single-celled ancestor?
How multicellular animals or metazoans emerged from a unicellular eukaryote, evolving into the highly-variable complex body plans we see today, is a major evolutionary question. However, the lack of fossil evidence of this ancestor compels the pursuit for novel ways of tracing the identity of this protist ancestor.
This fact has unavoidably led to focus the efforts in the study of early-branching animals. However, even though early-branching animals (such as ctenophores and poriferans) might provide insights on the multicellular ancestor of animals, the question on how it had become multicellular remains unanswered.
Therefore, to address this transition, we focus on comparing the genomes of animals to those of their closest unicellular relatives, namely filastereans (Capsaspora owczarzaki and Ministeria vibrans), ichthyosporeans (Sphaeroforma arctica, Creolimax fragrantissima, Abeoforma whisleri and Pirum gemmata) and chorallochytreans (Corallochytrium limacisporum). The study of these extant organisms allows us, on the one hand, to understand to what extent the evolution of animal multicellularity implied genetic innovation, and on the other hand, to reveal how the ancestor was and what genes did it count with.
So far, results have proven that the ancestor already counted with a complex repertoire of genes which play a key role in animal multicellularity -cell adhesion, signaling and communication.
How did animals “recycle” ancestral genes into new functions?
If gene innovation itself does not explain how animal multicellularity evolved, what was the key that drove this amazing transition? This question led us to analyse the role that these genes -those involved in cell signaling, adhesion and communication- are playing in our unicellular relatives, and how they were co-opted to the new functions in metazoans.
By elucidating the “ancestral function” of these genes, we will provide significant insights into the role they played in the development of animal multicellularity. In order to understand its role, we are developing some molecular and genetic tools, such as immunostaining, transfection, and CRISPR/cas9. Results suggest that the co-option of these ancestral genes might have taken place by a change in its regulation.
New model organisms to understand the origin of Metazoa
Although comparative genomics is a powerful methodology, it can not answer all questions. Some specific questions, such as how some genes or gene networks were co-opted at the origin of animals, can not be addressed without experimentally tractable organisms.
None of the model organisms available in Biology is appropriate to analyze the unicellular-to-multicellular transition that gave rise to animals. Thus, we are currently trying to develop at least one of the closest unicellular relatives of animals as a “model organism” to understand the origin of animals.
Currently, we are working with the filasterean Capsaspora owczarzaki; the ichthyosporeans Creolimax fragrantissima, Sphaeroforma arctica, Abeoforma whisleri, and Pirum gemmata; and the corallochytrean Corallochytrium limacisporum. So far, we have developed transfection protocols in Capsaspora owczarzaki, Creolimax fragrantissima, Abeoforma whisleri and Corallochytrium limacisporum.
This project counts with the collaboration of Elena Casacuberta. The labs of Hiroshi Suga and Duojia Pan are also working to develop Capsaspora owczarzaki as a model organism.
Searching for new animal and microbial opisthokont lineages
As mentioned above, the foundation of animal multicellularity can only be inferred by comparing animals with their closest unicellular relatives. However, molecular data from environmental surveys evidences many undescribed taxa, even whole lineages, in different habitats. Therefore, we are looking for novel unicellular lineages, closely related to animals, by analysing the molecular data of environmental samplings. These will not only become relevant to understand the unicellular-to-multicellular transition, but also help draw a more realistic image of the tree of life.
Lab website: Multicelgenome Lab
Rafels-Ybern, A.; Torres, A.G.; Grau-Bove, X.; Ruiz-Trillo, I.; Ribas de Pouplana, L. 2018. Codon adaptation to tRNAs with Inosine modification at position 34 is widespread among Eukaryotes and present in two Bacterial phyla. RNA Biology, DOI: 10.1080/15476286.2017.1358348
López-Escardó, D.; López-García, P.; Moreira, D.; Ruiz-Trillo, I.; Torruella, G. 2018. Parvularia atlantis gen. et sp. nov., a Nucleariid Filose Amoeba (Holomycota, Opisthokonta). Eukaryotic Microbiology. 65(2):170-179 DOI: 10.1111/jeu.12450
Leonard, G.; Labarre, A.; Milner, D.S.; Monier, A.; Soanes, D.; Wideman, J.G.; Maguire, F.; Stevens, S.; Sain, D.; Grau-Bové, X.; Sebé-Pedrós, A.; Stajich, J.E.; Paszkiewicz, K.; Brown, M.W.; Hall, N.; Wickstead, B.; Richards, T.A. 2018. Comparative genomic analysis of the 'pseudofungus' Hyphochytrium catenoides. Open Biology. 8(1):170184 doi: 10.1098/rsob.170184.
Cetkovic, H.; Bosnar, M.H.; Perina, D.; Mikoc, A.; Dezeljin, M.; Beluzic, R.; Bilandzija, H.; Ruiz-Trillo, I.; Harcet M. 2018. Characterization of a group i Nme protein of Capsaspora owczarzaki - A close unicellular relative of animals. Laboratory Investigation. 98(3):304-314 doi: 10.1038/labinvest.2017.134
27th April 2018:
On the appointment of Iñaki Ruiz-Trillo as new EMBO member:
- 21st, June 2017. Portal PRBB. "IBE (CSIC-UPF): Iñaki Ruiz-Trillo elected as new EMBO member"
- 19th, June 2017. IM Médico. "El investigador del CSIC-UPF Iñaki Ruiz-Trillo se convierte en nuevo miembro de la EMBO"
- 16th, June 2017. AlphaGalileo. "EMBO welcomes 65 new members"
- 16th, June 2017. EMBO. "EMBO welcomes 65 new members"
26th March, 2017. Cadena SER. "A vivir que son dos días: Burque al cubo" (with the participation of Iñaki Ruiz-Trillo).