Decoupling of Nuclear Division Cycles and Cell Size during the Coenocytic Growth of the Ichthyosporean Sphaeroforma arctica

Andrej Ondracka,Omaya Dudin,Iñaki Ruiz-Trillo

doi:10.1016/j.cub.2018.04.074

Abstract

SummaryCoordination of the cell division cycle with the growth of the cell is critical to achieve cell size homeostasis [1]. Mechanisms coupling the cell division cycle with cell growth have been described across diverse eukaryotic taxa [2, 3, 4], but little is known about how these processes are coordinated in organisms that undergo more complex life cycles, such as coenocytic growth. Coenocytes (multinucleate cells formed by sequential nuclear divisions without cytokinesis) are commonly found across the eukaryotic kingdom, including in animal and plant tissues and several lineages of unicellular eukaryotes [5]. Among the organisms 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 of animals [6]. Here, we characterize the coenocytic cell division cycle in the ichthyosporean Sphaeroforma arctica. We observe that, in laboratory conditions, S. arctica cells undergo a uniform and easily synchronizable coenocytic cell cycle, reaching up to 128 nuclei per cell before cellularization and release of daughter cells. Cycles of nuclear division occur synchronously within the coenocyte and in regular time intervals (11–12 hr). We find that the growth of cell volume is dependent on concentration of nutrients in the media; in contrast, the rate of nuclear division cycles is constant over a range of nutrient concentrations. Together, the results suggest that nuclear division cycles in the coenocytic growth of S. arctica are driven by a timer, which ensures periodic and synchronous nuclear cycles independent of the cell size and growth.

Highlights

We first characterized the life cycle of S. arctica in laboratory conditions by microscopy
Mechanisms coupling the cell division cycle with cell growth have been described across diverse eukaryotic taxa [2,3,4], but little is known about how these processes are coordinated in organisms that undergo more complex life cycles, such as coenocytic growth
Coenocytes are commonly found across the eukaryotic kingdom, including in animal and plant tissues and several lineages of unicellular eukaryotes [5]

Summary

Introduction

We first characterized the life cycle of S. arctica in laboratory conditions by microscopy. Pseudopodial cells and cells with large vacuoles have been observed in other closely related Sphaeroforma species [13], the majority of S. arctica cells grown in these conditions exhibit uniformly round morphology, no large vacuoles, and uniformly distributed nuclei within the multinucleate coenocyte (Figure 1B), which suggests a simple, linear coenocytic life cycle (Figure 1C). Newborn cells grow into a multinucleate coenocyte by rounds of synchronous nuclear divisions [9] followed by cellularization and release of the daughter cells (burst). We observed that newborn cells frequently contain two or even four nuclei (Figure 1B, fourth row, white arrow). This suggests that nuclear divisions already occur inside the cellularized coenocytes before the burst or that cellularization can occur around multiple nucle

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Discussion

Conclusion