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Research reveals clues to the elusive ‘Hello World’ moment of multicellular life

Becoming multicellular was a major transition in evolution, but it may have been different than originally thought. Growing evidence suggests that sophisticated genetic machinery needed to create more complex forms of life may have existed in several unicellular organisms before the first multicellular animals emerged.

Fundamental Research

All animals evolved from a single-celled ancestor millions of years ago. Understanding how life made this spectacular leap from unicellular simplicity to multicellular complexity is one of the major evolutionary puzzles of our time. Scientists are just beginning to come up with key pieces as to what actually happened in the first place. Reconstructing events that happened in the very distant past is difficult. The single-celled ancestor of all animals is extinct. “Recent phylogenomic studies suggest that choanoflagellates, filastereans and ichthyosporeans are amongst the closest living single-celled relatives of animals in the same way chimpanzees are humans’ closest cousins in the animal kingdom,” notes Omaya Dudin, coordinator of the EU-funded MULTICELLEXPEVO project that received funding under the Marie Skłodowska-Curie programme.

Fascinating yet forgotten organisms

The Marie-Curie fellow was awarded an Ambizione grant from the Swiss National Research Foundation that allowed him to start his own lab at the Swiss Federal Institute of Technology in Lausanne (EPFL). He specifically focused on ichthyosporeans as he felt that they have grabbed the least attention so far. Amongst holozoans, this group of unicellular eukaryotes is the only lineage that forms coenocytes during their life cycle. A coenocyte is a cell that undergoes multiple rounds of nuclear divisions without their accompanying cytokinesis. The ichthyosporean cell that initially has a single nucleus can grow to reach 128 nuclei sharing the same cytoplasm before undergoing cellularisation. What is also special about ichthyosporeans is that their cultures can be easily synchronised, which means that scientists can obtain cells in the same growth stage. “As a biologist with a background on cytoskeleton dynamics, the first question that crossed my mind is how a big multinucleated cell leads to the formation of hundreds of uninucleated cells,” adds Dudin.

Beautiful actin networks shrouded in mystery

The researcher employed live and fixed cell imaging and inhibitors in an effort to study and localise proteins inside the cell. He turned to Sphaeroforma arctica (S. arctica), an ichthyosporean that appeared more robust and uniform than other species. The team showed that cellularisation in S. arctica depends on actin and myosin networks that generate contractile forces within cells. The nucleus of a single cell divides repeatedly to form a polarised epithelial layer, which then gives rise to multiple cells as the plasma membrane undergoes coordinated invaginations. The actin network takes around nine hours to form on the coenocyte surface. With the help of Arp2/3 complexes, formins and myosin II, which proved essential in the cellularisation process, the network undergoes a transient multicellular stage. “Regulating these proteins is a complex developmental feat for a unicellular organism. Importantly, the cellularisation process allows the formation of a self-organised layer of clonal cells,” explains Dudin. “Small RNA and microRNA analyses associate the cellularisation process with the simultaneous expression of cell-adhesion genes, giving rise to proteins such as integrins and catenins. These proteins might have a prominent role in animal development and spatial organisation of animal cells.” The implications of this finding are dramatic, changing our mindset about animal development. “If this is indeed valid, it could mean that the epithelial-like structure we see in unicellular organisms was present before animals evolved. Relating this situation to the ‘egg and chicken’ question, it could mean that eggs arrived first – the developmental mechanisms of spatial organisation and cell differentiation were somehow already present in the unicellular ancestor of all animals,” concludes Dudin.

Keywords

MULTICELLEXPEVO, unicellular, multicellular, ichthyosporean, cellularisation, actin, Sphaeroforma arctica

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