Relationships Between Host and Symbiont Cell Cycles in Sea Anemones and Their Symbiotic Dinoflagellates

Abstract

The processes by which cnidarians and their algal endosymbionts achieve balanced growth and biomass could include coordination of host and symbiont cell cycles. We evaluated this theory with natural populations of sea anemones hosting symbiotic dinoflagellates, focusing on the temperate sea anemone Anthopleura elegantissima symbiotic with Symbiodinium muscatinei in Washington State, USA, and the tropical anemone Stichodactyla helianthus associating with unknown Symbiodinium spp. in Belize. By extruding symbiont-containing gastrodermal cells from the relatively large tentacles of these species and using nuclear staining and flow cytometry, we selectively analyzed cell cycle distributions of the symbionts and the host gastrodermal cells that house them. We found no indications of diel synchrony in host and symbiont G2/M phases, and we observed evidence of diel periodicity only in Symbiodinium spp. associated with S. helianthus but not in the anemone itself. Seasonally, S. muscatinei showed considerable G2/M phase variability among samples collected quarterly over an annual period, while the G2/M phase of its host varied much less. Within samples taken at different times of the year, correlations between host and symbiont G2/M phases ranged from very weakly to very strongly positive, with significant correlations in only half of the samples (two of four A. elegantissima samples and one of two S. helianthus samples). Overall, the G2/M phase relationships across species and sampling periods were positive. Thus, while we found no evidence of close cell cycle coupling, our results suggest a loose, positive relationship between cell cycle processes of the symbiotic partners.

Cell Cycle Dynamics of Cultured Coral Endosymbiotic Microalgae (Symbiodinium) Across Different Types (Species) Under Alternate Light and Temperature Conditions

“…Previous studies have identified phased division of Symbiodinium in hospite (Dimond et al. ; Fitt ; Hoegh‐Guldberg ; Hoegh‐Guldberg and Smith ; Wilkerson et al. ); however, almost all of these studies were based on a “mitotic index” (visual index of doublets or cells undergoing cytokinesis), providing only a narrow window of cell cycle progression.…”

“…), few studies have yet examined the Symbiodinium cell cycle to resolve premitotic control of Symbiodinium cell densities by their hosts (Dimond et al. ; Smith and Muscatine ). Growth status of Symbiodinium is important for maintaining a stable symbiosis with the host (e.g.…”

“…Cell cycle progression appears well-conserved across genetic types (species) and thus provides an improved baseline with which to consider cell cycle progression in hospite and hence better understand host control. Previous studies have identified phased division of Symbiodinium in hospite (Dimond et al 2013;Fitt 2000;Hoegh-Guldberg 1994;Hoegh-Guldberg and Smith 1989;Wilkerson et al 1983); however, almost all of these studies were based on a "mitotic index" (visual index of doublets or cells undergoing cytokinesis), providing only a narrow window of cell cycle progression. For example, previous studies showed an increase in the mitotic index of Symbiodinium in hospite during increases in water temperature (Bhagooli and Hidaka 2002;Strychar et al 2004b;Suharsono and Brown 1992).…”

Maintenance of algal endosymbionts in Paramecium bursaria: a simple model based on population dynamics

“…However, even under the normal light regime, the growth of the two organisms exhibited time lags, which were the main cause of the dynamic behaviours of the endosymbiont population size in the host cells. Moreover, the cell divisions of the hosts and the endosymbionts exhibited differences in dependence on the light-dark change, as the endosymbiont was coupled to the change, whereas the host was almost not (similarly to a sea anemone in Dimond et al, 2013). These results suggest both that there is only slight, if any, coupling between the cell cycles of the two organisms and that direct regulation of endosymbiont cell division plays only a limited role in P. bursaria, with the endosymbionts likely to be regulated by some indirect mechanism.…”

“…The coupling of cell cycles between the host and the endosymbiont may be an important factor in regulating endosymbiont population size, as it simply leads to coordinated growth of the two organisms and thereby the maintenance of endosymbiont number in the host. In some invertebrates, the relationships of cell cycle processes between the two organisms seem to be positive, whereas the degree of the coupling is variable depending on cells, species or environments (McAuley, 1982;1985;Fitt, 2000;Dimond et al, 2013). It has been suggested that in P. bursaria the cell cycle of the endosymbiont depends on that of the host (Kadono et al, 2004); however, close coupling of cell cycles between Chlorella-like algae and ciliates is likely to require complicated systems because of the differences in their respective cell division patterns.…”