Symbiodinium transcriptome and global responses of cells to immediate changes in light intensity when grown under autotrophic or mixotrophic conditions

Abstract

SummarySymbiosis between unicellular dinoflagellates (genus Symbiodinium) and their cnidarian hosts (e.g. corals, sea anemones) is the foundation of coral reef ecosystems. Dysfunction of this symbiosis under changing environmental conditions has led to global reef decline. Little information is known about Symbiodinium gene expression and mechanisms by which light impacts host–symbiont associations. To address these issues, we generated a transcriptome from axenic Symbiodinium strain SSB01. Here we report features of the transcriptome, including occurrence and length distribution of spliced leader sequences, the functional landscape of encoded proteins and the impact of light on gene expression. Expression of many Symbiodinium genes appears to be significantly impacted by light. Transcript encoding cryptochrome 2 declined in high light while some transcripts for Regulators of Chromatin Condensation (RCC1) declined in the dark. We also identified a transcript encoding a light harvesting AcpPC protein with homology to Chlamydomonas LHCSR2. The level of this transcript increased in high light autotrophic conditions, suggesting that it is involved in photo‐protection and the dissipation of excess absorbed light energy. The most extensive changes in transcript abundances occurred when the algae were transferred from low light to darkness. Interestingly, transcripts encoding several cell adhesion proteins rapidly declined following movement of cultures to the dark, which correlated with a dramatic change in cell surface morphology, likely reflecting the complexity of the extracellular matrix. Thus, light‐sensitive cell adhesion proteins may play a role in establishing surface architecture, which may in turn alter interactions between the endosymbiont and its host.

Glucose-Induced Trophic Shift in an Endosymbiont Dinoflagellate with Physiological and Molecular Consequences

“…Overall, the differences in levels of transcript accumulation that we observed were small, consistent with previous studies of gene-expression changes in SSB01 during exposure to different light intensities (Xiang et al, 2015). Only six transcripts exhibited a change in abundance of .10-fold at any time point following transfer to IMK+Glc medium (in either the light or the dark) but not when transferred to IMK medium (Supplemental Table S3).…”

“…Although this scoring is somewhat subjective, it was consistent in replicate trials in which individual images were scored without the observer's knowing in which medium the cells had been grown. A similar difference in surface structure was observed previously by SEM of cells grown in high light (typically more rough and convoluted) relative to cells grown in low light or maintained in the dark (typically smoother; Xiang et al, 2015). Differences in surface structures were also observed by TEM.…”

“…Transcript counts for all time points were compared to the timezero values (for the cells growing in IMK+Cas medium that were used to inoculate the three experimental cultures), but data from the experimental cultures at the same time points were also compared among themselves. From the 40 library samples analyzed (four replicates at time zero plus three replicates for each of the three conditions at each of the four subsequent time points; see Supplemental Table S1 for details), 687,443,214 reads were generated, mapped to the SSB01 transcriptome assembly symb6 (Xiang et al, 2015), and used to analyze differences in gene expression using DESeq2 as described in "Materials and Methods. "…”

Current Knowledge and Recent Advances in Marine Dinoflagellate Transcriptomic Research

“…While most of the studies on SOD and CAT enzymes in Symbiodinium suggested these enzymes play a major role in coping with an increase of sea temperature to prevent coral bleaching [91][92][93], a number of studies in other organisms revealed that these enzymes may act in response to other types of environmental stress such as salinity, exposure to hydrogen peroxide and drought conditions [94][95][96]. Apart from the antioxidative response, cell adhesion proteins also play a role in maintaining coral-Symbiodinium symbiosis interaction [9]. Genes encoding for cell surface molecules such as Sushi, Von Willebrand factor type A, EGF and pentraxin domain containing 1 (Svep1) were downregulated during the event of induced bleaching in their coral host.…”

“…Dinoflagellates are found in a range of marine ecosystems including estuaries, mangroves and deep-sea environments, and some exist as symbionts with other organism such as coral and epiphytes of seaweeds and seagrass [2][3][4][5][6]. Their lifestyle ranges from mixotrophic through to heterotrophic and autotrophic [7][8][9]. They also have been reported to be the major cause of the harmful algae blooms (HABs), sometimes referred to as 'red tide' events in the ocean, and may result in death of marine mammals and affect human health due to the accumulative effect of toxins moving throughout the food chain when contaminated seafood is consumed [10,11].…”