Symbiosis with Dinoflagellates Alters Cnidarian Cell-Cycle Gene Expression

Abstract

In the cnidarian-dinoflagellate symbiosis, hosts show altered expression of genes involved in growth and proliferation when in the symbiotic state, but little is known about the molecular mechanisms that underlie the host’s altered growth rate. Using tissue-specific transcriptomics, we determined how symbiosis affects expression of cell cycle-associated genes, in the model symbiotic cnidarian Exaiptasia diaphana (Aiptasia). The presence of symbionts within the gastrodermis elicited cell-cycle arrest in the G1 phase in a larger proportion of host cells compared with the aposymbiotic gastrodermis. The symbiotic gastrodermis also showed a reduction in the amount of cells synthesizing their DNA and progressing through mitosis when compared with the aposymbiotic gastrodermis. Host apoptotic inhibitors (Mdm2) were elevated, while host apoptotic sensitizers (c-Myc) were depressed, in the symbiotic gastrodermis when compared with the aposymbiotic gastrodermis and epidermis of symbiotic anemones, respectively. This indicates that the presence of symbionts negatively regulates host apoptosis, possibly contributing to their persistence within the host. Transcripts (ATM/ATR) associated with DNA damage were also downregulated in symbiotic gastrodermal tissues. In epidermal cells, a single gene (Mob1) required for mitotic completion was upregulated in symbiotic compared with aposymbiotic anemones, suggesting that the presence of symbionts in the gastrodermis stimulates host cell division in the epidermis. To further corroborate this hypothesis, we performed microscopic analysis using an S-phase indicator (EdU), allowing us to evaluate cell cycling in host cells. Our results confirmed that there were significantly more proliferating host cells in both the gastrodermis and epidermis in the symbiotic state compared with the aposymbiotic state. Furthermore, when comparing between tissue layers in the presence of symbionts, the epidermis had significantly more proliferating host cells than the symbiont-containing gastrodermis. These results contribute to our understanding of the influence of symbionts on the mechanisms of cnidarian cell proliferation and mechanisms associated with symbiont maintenance.

Unlocking the Complex Cell Biology of Coral–Dinoflagellate Symbiosis: A Model Systems Approach

“…When mTOR signaling is inhibited, the LAMP1 niche is not established and symbiosis breaks down-a mechanism that is conserved in the coral A. tenuis (157). Symbiosis positively influences host cell proliferation in both endodermal and ectodermal tissues in Aiptasia larvae and adults, depending on symbiont strain and host nutritional status (47,147,157). Taken together, cellular and organismal responses to nutrient fluxes, including by mTOR signaling, are key for symbiont-derived nutrient integration in symbiotic cnidarians.…”

Rapid shifts in thermal reaction norms and tolerance of brooded coral larvae following parental heat acclimation

“…Therefore, our results indicate that the concerted and strong transcriptional HSR in larvae from heat‐acclimated adults could have been effective in rescuing host cells from stress, hence favouring cell cycle transitions and division (Figure 6). Cell division is the fundamental process that allows eukaryotic organisms to renew, repair and grow their tissues, and host cell cycle regulation has been suggested as a primary mechanism to govern symbiont density and sustain symbiosis in cnidarians (Gorman et al, 2022; Rivera & Davies, 2021; Tivey et al, 2020). The transcriptional signatures of accelerated host cell cycle and mitosis not only imply a faster self‐renewal and turnover of host cells but also a potentially greater capacity to maintain symbiosis, which is further reflected in the enhanced heat tolerance and the maintenance of symbiont population in A32 larvae.…”

Help Me, Symbionts, You’re My Only Hope: Approaches to Accelerate Our Understanding of Coral Holobiont Interactions

“…The answer most likely lies in nutritional benefits provided to the host by the symbiont under ambient conditions. After establishment of symbiosis, the host exerts control over Symbiodiniaceae cell density and proliferation through regulation of the cell cycle and nitrogen cycling (Gorman et al, 2022;Rivera & Davies, 2021).…”