Free‐living and symbiotic lifestyles of a thermotolerant coral endosymbiont display profoundly distinct transcriptomes under both stable and heat stress conditions

Reef-building corals depend upon a nutritional endosymbiosis with
photosynthetic dinoflagellates of the family Symbiodiniaceae for the
majority of their energetic needs. While this mutualistic relationship is
impacted by numerous stressors, warming oceans are a predominant threat to
coral reefs, placing the future of the world’s reefs in peril. Some
Symbiodiniaceae species exhibit tolerance to thermal stress, but the in
hospite symbiont response to thermal stress is underexplored. To describe
the underpinnings of symbiosis and heat stress response, we compared in
hospite and free-living transcriptomes of Durusdinium trenchii, a
pan-tropical heat-tolerant Symbiodiniaceae species, under stable
temperature conditions and acute hyperthermal stress. We discovered that
symbiotic state was a larger driver of the transcriptional landscape than
heat stress. The majority of differentially expressed transcripts between
in hospite and free-living cells were downregulated, suggesting the in
hospite condition is associated with the shutdown of numerous processes
uniquely required for a free-living lifestyle. In the free-living state,
we identified enrichment for numerous cell signaling pathways and other
functions related to detecting and responding to a changing environment,
as well as transcripts relating to mitosis, meiosis, and motility. In
contrast, in hospite cells exhibited enhanced transcriptional activity for
photosynthesis and carbohydrate transport as well as chromatin
modifications and a disrupted circadian clock. Hyperthermal stress induced
drastic alteration of transcriptional activity in hospite, suggesting
symbiotic engagement with the host elicited an exacerbated stress response
when compared to free-living D. trenchii. Altogether, the dramatic
differences in gene expression between in hospite and free-living D.
trenchii indicate the importance of considering symbiotic state in
investigations of symbiosis and hyperthermal stress in Symbiodiniaceae.