Talin at the Root of the Eukaryotic Radiation and the Origins of Animal Multicellularity
A wealth of phylogenomic data has established the outline of the eukaryotic radiation, from the last eukaryotic common ancestor (LECA) through the terminal branches of extant eukaryotes. This consensus, derived from datasets of primarily “housekeeping” proteins, divides eukaryotes into two clades, bikonts [e.g. stramenopiles, alveolates, plants] and unikonts [Amoebozoa, opisthokonts (Fungi, choanoflagellates, Metazoa)]. Elucidation of the cellular differences between unikonts and bikonts is a major objective of Evolutionary Cell Biology. While the calculated phylogeny is robust, it has little to say about what made ancestral bikonts and unikonts different at the cellular level and how these differences led to current eukaryote diversity. This project is based on the molecular cell biology of one of the core proteins that composes the integrin adhesome: talin. The highly-conserved THATCH (Talin-Hip1Actin C-terminal Homology) domain is present in and diagnostic of all sequenced unikonts. Together, this multicomponent adhesome is essential for animal multicellularity, which is perhaps the exceptional distinction between the two clades. We will examine the interactions of recombinant talin proteins in model organisms representative of the bikont-unikont bifurcation (e.g. Thecamonas trahens, Capsaspora owczarzaki, Allomyces macrogynus) in order to provide a framework for elucidating original cellular characteristics that accompanied the divergence of eukaryotes into unikonts and bikonts. More specifically, our objectives are to: (1) identify and quantify protein-protein interactions that preadapted talin proteins in ancestral, largely unicellular unikonts for the leap to multicellularity; and (2) construct a model of integrin adhesome function that accounts for the emergence of the Metazoa at the cellular level. These complementary but independent aims will lead to a better insight into the fundamental differences of cell heredity and genome content that distinguish bikonts from unikonts. Furthermore, knowledge of how the individual components of the integrin adhesome coevolved from an “ancestral” to an apparently complex “modern” state will provide the framework for contributing to the understanding of eukaryotic evolution at the cellular level.
Carter, Elisabeth Ann