Multi-omics analysis of thermal stress response in a zooxanthellate cnidarian reveals the importance of associating with thermotolerant symbionts

Abstract

Corals and their endosymbiotic dinoflagellates of the genus Symbiodinium have a fragile relationship that breaks down under heat stress, an event known as bleaching. However, many coral species have adapted to high temperature environments such as the Red Sea (RS). To investigate mechanisms underlying temperature adaptation in zooxanthellate cnidarians we compared transcriptome- and proteome-wide heat stress response (24 h at 32°C) of three strains of the model organism Aiptasia pallida from regions with differing temperature profiles; North Carolina (CC7), Hawaii (H2) and the RS. Correlations between transcript and protein levels were generally low but inter-strain comparisons highlighted a common core cnidarian response to heat stress, including protein folding and oxidative stress pathways. RS anemones showed the strongest increase in antioxidant gene expression and exhibited significantly lower reactive oxygen species (ROS) levels in hospite However, comparisons of antioxidant gene and protein expression between strains did not show strong differences, indicating similar antioxidant capacity across the strains. Subsequent analysis of ROS production in isolated symbionts confirmed that the observed differences of ROS levels in hospite were symbiont-driven. Our findings indicate that RS anemones do not show increased antioxidant capacity but may have adapted to higher temperatures through association with more thermally tolerant symbionts.

Keywords: Aiptasia; heat stress; oxidative stress; proteomics; thermotolerance; transcriptomics.

Figure 1.

Annual average temperature profiles of sampling locations of the three investigated Aiptasia strains originating from North Carolina (Wilmington), Hawaii (Kāne'ohe Bay) and the Red Sea (Al Lith). The average monthly temperature is denoted by a solid line. Shading around lines represent maximum and minimum temperature (temperature data taken for closest location to sampling area from www.seatemperature.org).

Figure 2.

Correlation of protein abundance with mRNA expression at control (25°C) and heat stress (32°C) for each biological replicate. Expression values were log₂-transformed to better approximate normal distributions. Linear regressions were calculated for control and stress conditions across all replicates of a given strain. Darker colours represent heat stress; lighter ones represent control. SCPM, spectral counts per million; TPM, transcripts per million.

Figure 3.

Heatmap of GO terms related to unfolded protein response, metabolism and oxidative stress from three Aiptasia pallida transcriptomes. Selected terms illustrate strain-specific differential transcriptomic responses to heat stress (p < 0.05). Empty boxes denote differences that were not significant (p ≥ 0.05).

Figure 4.

ROS produced by Symbiodinium (a) in hospite and (b) in isolate. ROS was measured for control (25°C) and heat stress (32°C) conditions and normalized against total symbiont counts. Error bars denote ±1 standard errors. *p < 0.05; n.s., not significant.