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.

Meta-analysis of the General Coral Stress Response:Acroporacorals show opposing responses depending on stress intensity

“…Although this may be due to lower samples size, repetition of Figure 2D. the random forest model revealed the type B response was less predictable than the type A response, with type B samples frequently misidentified as controls ( Figure 3B Cziesielski et al 2018;Aguilar et al 2019;Cziesielski et al 2019). We first examined differential expression values for all stressed type A samples compared to their controls.…”

“…Examining functional enrichment among heat stress genes in Acropora hyacinthus and in other coral studies, Barshis et al (2013) pointed out conspicuous overlap with the yeast ESR (Gasch et al 2000). Comparing heat stress responses among anemone strains, Cziesielski et al (2018) describe a "core Cnidarian response to heat stress" including protein folding and oxidative stress genes. The idea of a general stress response was also described by Aguilar et al (2019).…”

The past, present, and future of coral heat stress studies

“…The possibility of whole-mRNA sequencing propelled transcriptome studies in a variety of corals (Meyer et al, 2009;Schwarz et al, 2008;Traylor-Knowles et al, 2011) as well as in Symbiodiniaceae species (Barshis, Ladner, Oliver, & Palumbi, 2014;Bayer et al, 2012;Rosic et al, 2015). Though not comprehensively discussed in this review, a growing number of studies are applying proteomics in cnidarians (Barneah, Benayahu, & Weis, 2006;Cziesielski et al, 2018;Drake et al, 2013;Oakley et al, 2016;Ramos-Silva et al, 2013). Omics methods were previously only utilized in a handful of studies, but are currently one of the most common tools applied in the field (Figure 1) and thus the primary focus of the following sections.…”

With a Little Help From Friends—How Algae Help Corals Survive Temperature Stress

“…The stars between the temperatures of an anemone show where the change in ROS levels was strong. The data show that the algae that live in the Red Sea anemones had the least amount of ROS production in all conditions [2]. This means that the Red Sea anemone and algae were the least stressed when temperatures increased.…”

“…Shading around the line shows the maximum and minimum temperatures. This data shows that the Red Sea has the warmest waters [2] (temperature data obtained from www. seatemperature.org).…”