Contrasting heat stress response patterns of coral holobionts across the Red Sea suggest distinct mechanisms of thermal tolerance

Abstract

Corals from the northern Red Sea, in particular the Gulf of Aqaba (GoA), have exceptionally high bleaching thresholds approaching >5°C above their maximum monthly mean (MMM) temperatures. These elevated thresholds are thought to be due to historical selection, as corals passed through the warmer Southern Red Sea during re-colonization from the Arabian Sea. To test this hypothesis, we determined thermal tolerance thresholds of GoA versus Central Red Sea (CRS) Stylophora pistillata corals using the Coral Bleaching Automated Stress System (CBASS) to run a series of standardized acute thermal stress assays. Relative thermal thresholds of GoA and CRS corals were indeed similar and exceptionally high (~7°C above MMM). However, absolute thermal thresholds of CRS corals were on average 3°C above those of GoA corals. To explore the mechanistic underpinnings, we determined gene expression response and microbiome dynamics of coral holobiont compartments. Transcriptomic responses differed markedly, with a strong response to the thermal stress in GoA corals versus a remarkably muted response in corals from the CRS. This pattern was recapitulated in the algal symbionts that showed site-specific genetic differentiation. Concomitant to this, a subset of coral and algal genes showed temperature-induced expression in GoA corals, while exhibiting fixed high expression, i.e. front-loading, in CRS corals. Bacterial community composition of GoA corals changed dramatically under heat stress, whereas CRS corals displayed consistent assemblages, indicating distinct microbial response patterns. Our work demonstrates distinct patterns underlying thermal tolerance across spatial scales, even for the same species and ocean basin. We interpret the response of GoA corals as that of a resilient population approaching a tipping point in contrast to a pattern of consistently elevated thermal resistance in CRS corals that cannot further attune. Such response differences suggest distinct thermal tolerance mechanisms that affect the response of coral populations to ocean warming.

Remarkably high and consistent tolerance of a Red Sea coral to acute and chronic thermal stress exposures

“…The Fv/Fm ED 50 is not an absolute measure of thermal tolerance, as the absolute thermal tolerance of a coral is likely to be affected by the prospective diel/seasonal heating and light regime among other factors. Still, our results, along with those from Voolstra et al (2020a) and Morikawa and Palumbi (2019), indicate some consistency in the response of corals to acute thermal assays and more prolonged thermal exposures and serve as evidence that acute thermal assays could provide realistic assessments of natural variance in the thermal tolerance of coral populations (Voolstra et al 2020b). As such, this approach could hold great promise as a standardized diagnostic to empirically assess environmental and evolutionary drivers of thermal tolerance across large scales and identify coral populations with the greatest chance of surviving future impacts of global warming.…”

Fast and pervasive transcriptomic resilience and acclimation of extremely heat-tolerant coral holobionts from the northern Red Sea

“…It did, however, decrease at 34.5°C, especially in the long-term experiments (Fig. 3B), indicating a sharp transition in resilience of the symbiont population, similar to the coral host, between 32°C and 34.5°C (41). In addition, 414 DEGs appeared in the 32°C treatment at T2 in the short-term experiment (Dataset S3), mainly as a down-regulation of genes involved in photosynthesis, indicating that reduced photosynthetic activity might be beneficial to the symbionts immediately after thermal stress, possibly to reduce the abundance of reactive oxygen species.…”

Flexibility in Red Sea Tridacna maxima‐Symbiodiniaceae associations supports environmental niche adaptation

“…In corals, fine-scale resolutions of Symbiodiniaceae assemblages often strongly correlate to host genotype (Gardner et al, 2019;Howells et al, 2020;Hume, D'Angelo, et al, 2018;Hume et al, 2020). However, if the Red Sea T. maxima populations are assumed to be a single well-connected, yet diverse population, this would suggest that the prevailing environmental conditions, which are also known to strongly influence coral-Symbiodiniaceae associations (Hume et al, 2020;LaJeunesse et al, 2010;Oliver & Palumbi, 2009;Smith et al, 2020;Terraneo et al, 2019;Varasteh et al, 2017;Voolstra, Valenzuela, et al, 2020;Ziegler et al, 2015), are the driving forces of the observed structure. Whether this relatively high clam-symbiont flexibility is a product of the location in which the algal symbionts reside within the host tissue (i.e., extracellularly in clams vs. intracellularly in corals) remains to be investigated.…”