Decoupling of the nuclear division cycle and cell size control in the coenocytic cycle of the ichthyosporean Sphaeroforma arctica

Abstract

Coenocytes (multinucleated cells formed by sequential nuclear divisions without cytokinesis) are commonly found across the eukaryotic kingdom, including in animals, plants and several lineages of unicellular eukaryotes. Despite their commonality, little is known about how cell growth, nuclear divisions and cell divisions are coordinated in coenocytes. Among the unicellular eukaryotes that form coenocytes are ichthyosporeans, a lineage of unicellular holozoans that are of significant interest due to their phylogenetic placement as one of the closest relatives to animals. Here, we characterize the coenocytic cell division cycle in the ichthyosporean Sphaeroforma arctica. In laboratory conditions, we observed that S. arctica cells undergo a highly regular periodic coenocytic cell cycle. Nuclear division cycles occur synchronously within the coenocyte and in regular time intervals (~11 hours per nuclear cycle) until reaching 64-128 nuclei and releasing daughter cells. The duration of the nuclear division cycles is constant across a wide range of nutrient concentration. In contrast, the volume of the coenocytes increase more slowly in lower nutrient concentration, which also results in smaller newborn daughter cells. This suggests that S. arctica cells are capable to adapt the cell growth rate to nutrient concentration while maintaining the timing of nuclear division cycles, suggesting that in ichthyosporeans the mechanisms regulating highly periodic nuclear division cycles operate independently from mechanisms sensing the cell size.