Genome-Wide Analysis of Cell Cycle-Regulating Genes in the Symbiotic Dinoflagellate Breviolum minutum

Abstract

A delicate relationship exists between reef-building corals and their photosynthetic endosymbionts. Unfortunately, this relationship can be disrupted, with corals expelling these algae when temperatures rise even marginally above the average summer maximum. Interestingly, several studies indicate that failure of corals to regulate symbiont cell divisions at high temperatures may underlie this disruption; increased proliferation of symbionts may stress host cells by over-production of reactive oxygen species or by disrupting the flow of nutrients. This needs to be further investigated, so to begin deciphering the molecular mechanisms controlling the cell cycle in these organisms, we used a computational approach to identify putative cell cycle-regulating genes in the genome of the dinoflagellate Breviolum minutum. This species is important as an endosymbiont of Aiptasia pallida—an anemone that is used as a model for studying coral biology. We then correlated expression of these putative cell cycle genes with cell cycle phase in diurnally growing B. minutum in culture. This approach allowed us to identify a cyclin/cyclin-dependent kinase pair that may function in the G1/S transition—a likely point for coral cells to exert control over algal cell divisions.

Mutual antagonism between Hippo signaling and cyclin E drives intracellular pattern formation

“…Nonciliate alveolates (Apicomplexa and dinoflagellates) lack cyclin E ( Fig. S1 B ), as reported earlier ( Alvarez and Suvorova, 2017 ; Cato et al, 2019 ). Overall, cyclin E is present in Holozoa, an apusozoan Thecamonas trahens , and ciliates ( Cao et al, 2014 ; Stover and Rice, 2011 ; Suga et al, 2013 ; this study).…”

Phylogenetic analysis of cell-cycle regulatory proteins within the Symbiodiniaceae

“…S3). This finding agrees with the previous study 20 , which found P-type cyclins in B. minutum. Genes within these groups were related to the S. cerevisiae Pho80p cyclin.…”

“…Amongst transcriptional roles, the CDK10/11 subfamily has also been proposed to have roles in cellcycle progression during the G 2 /M phase (Table S1) 57 . However, in B. minutum, CDK20, CDK9 and CDK11 expression did not change with cell-cycle phase 20 , highlighting their similarity to metazoan CDK20, CDK9 and CDK11, which are predominantly transcriptional CDKs and indirectly related to the cell cycle 58 . Previous studies 20 have reported an absence of CDK7 in B. minutum, however this study found a CDK7-related gene (confirmed via BLAST searches on the NCBI nr database) across 13 different Symbiodiniaceae species ( Supplementary Fig.…”

“…2). A previous study 20 investigating Symbiodiniaceae cell-cycle proteins found four B. minutum-specific CDKs. Here we show that three of those four CDKs are also present across other Symbiodiniaceae species (alveolate-specific CDKG/H/J- Table 1; Supplementary Fig.…”

“…S3). Two cyclins previously reported to be B. minutum-specific 20 were found in other Symbiodiniaceae species and belong to the "Plant Cyclin D-like" grouping (Table 3; Supplementary Fig. S3).…”