Stable transfection in protist Corallochytrium limacisporum identifies novel cellular features among unicellular animals relatives

• Published in: Current biology 2021-09, Vol.31 (18), p.4104-4110.e5
• Main Authors: Kożyczkowska, Aleksandra, Najle, Sebastián R., Ocaña-Pallarès, Eduard, Aresté, Cristina, Shabardina, Victoria, Ara, Patricia S., Ruiz-Trillo, Iñaki, Casacuberta, Elena
• Format: Article
• Language: English
• Subjects: Corallochytrea, unicellular Holozoa, binary fission, genetic tools, stable transfection, binucleated cells, coenocyte, non-linear life cycle, decoupled karyokinesis and cytokinesis
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2021.06.061

The evolutionary path from protists to multicellular animals remains a mystery. Recent work on the genomes of several unicellular relatives of animals has shaped our understanding of the genetic changes that may have occurred in this transition.1–3 However, the specific cellular modifications that took place to accommodate these changes remain unclear. To address this, we need to compare metazoan cells with those of their extant relatives, which are choanoflagellates, filastereans, ichthyosporeans, and corallochytreans/pluriformeans. Interestingly, these lineages display a range of developmental patterns potentially homologous to animal ones. Genetic tools have already been established in three of those lineages.4–7 However, there are no genetic tools available for Corallochytrea. We here report the development of stable transfection in the corallochytrean Corallochytrium limacisporum. Using these tools, we discern previously unknown biological features of C. limacisporum. In particular, we identify two different paths for cell division—binary fission and coenocytic growth—that reveal a non-linear life cycle. Additionally, we found that C. limacisporum is binucleate for most of its life cycle, and that, contrary to what happens in most eukaryotes, nuclear division is decoupled from cellular division. Moreover, its actin cytoskeleton shares characteristics with both fungal and animal cells. The establishment of these tools in C. limacisporum fills an important gap in the unicellular relatives of animals, opening up new avenues of research to elucidate the specific cellular changes that occurred in the evolution of animals. [Display omitted] •Stable transfection is established for the first time in the lineage Corallochytrea•C. limacisporum reproduces by either binary fission or coenocytic growth•Binary fission in C. limacisporum is decoupled from nuclear division•C. limacisporum actin cytoskeleton has features of both fungal and animal cells Kożyczkowska et al. develop stable transfection in Corallochytrium limacisporum, a close unicellular relative to animals. This will allow taxon-rich comparative analyses of the evolution of cell biological features from protists to metazoans. The results reveal C. limacisporum has a combination of fungal-like and animal-like cell traits.