Transcriptomic responses to thermal stress and varied phosphorus conditions in Symbiodinium kawagutii

Abstract

Symbiodinium species are essential symbionts of tropical reef-building corals and the disruption of their symbiosis with corals as a consequence of seawater warming and other stress conditions leads to the globally widespread coral bleaching. As coral reefs live in the oligotrophic environment, Symbiodinium photosynthesis can also face nutrient stress. How metabolic pathways in Symbiodinium respond to thermal stress and phosphate depletion is poorly understood and underexplored for many species. Here we conducted RNA-seq analysis to investigate transcriptomic responses to thermal stress, phosphate deprivation and glycerol-3-phosphate (Gro3P) replacement in S. kawagutii. RNA-seq and bioinformatic analysis were conducted for the above-mentioned three treatments and a control. We identified 221 (2.04%) genes showing no significant differential expression among all conditions, and defined them as \"core\" genes of S. kawagutii, which mostly were in the Gene Ontology terms of catalytic activity and binding. Using algorithms edgeR and NOIseq in combination, we identified a set of differentially expressed genes (DEGs) for each treatment relative to the control. Under heat stress 357 (4.42%) DEGs were found, with predicted roles in active molecular (protein-protein/RNA/DNA) interaction, cell wall modulation and transport (including nutrients, iron, and oxygen). About as many DEGs (396, 4.73%) were identified under P deprivation while nearly double of that (671, 8.05%) were detected under Gro3P utilization; in both cases most of the DEGs were up-regulated and predicted to function in photosystem and defensome. Further KEGG pathway comparison revealed different molecular responses between phosphate deprivation and Gro3P utilization. Catalytic activity and binding seem to be two important core functions in S. kawagutii. The most significant transcriptional response in S. kawagutii to heat stress was regulation of molecular interaction, cell wall modulation, and transport of iron, oxygen, and major nutrients, suggesting that this species uses a unique mechanism to cope with heat stress, possibly conferring thermal tolerance. The greatest transcriptomic impact of phosphate deprivation and Gro3P replacement were the up-regulation of photosystem and defense. This study provides new clues about molecular mechanisms underpinning responses in Symbiodinium to temperature and nutrient stresses, which will generate new hypotheses and set a new framework for future investigations.