Heat-evolved algal symbionts enhance bleaching tolerance of adult corals without trade-off against growth.

Ocean warming has caused coral mass bleaching and mortality worldwide and the persistence of symbiotic reef-building corals requires rapid acclimation or adaptation. Experimental evolution of the coral's microalgal symbionts followed by their introduction into coral is one potential method to enhance coral thermotolerance. Heat-evolved microalgal symbionts of the generalist species, Cladocopium proliferum (strain SS8), were exposed to elevated temperature (31°C) for ~10 years, and were introduced into four genotypes of chemically bleached adult fragments of the scleractinian coral, Galaxea fascicularis. Two of the four coral genotypes acquired SS8. The new symbionts persisted for the 5 months of the experiment and enhanced adult coral thermotolerance, compared with corals that were inoculated with the wild-type C. proliferum strain. Thermotolerance of SS8-corals was similar to that of coral fragments from the same colony hosting the homologous symbiont, Durusdinium sp., which is naturally heat tolerant. However, SS8-coral fragments exhibited faster growth and recovered cell density and photochemical efficiency more quickly following chemical bleaching and inoculation under ambient temperature relative to Durusdinium-corals. Mass spectrometry imaging suggests that algal pigments involved in photobiology and oxidative stress were the greatest contributors to the thermotolerance differences between coral hosting heat-evolved versus wild-type C. proliferum. These pigments may have increased photoprotection in the heat-evolved symbionts. This is the first laboratory study to show that thermotolerance of adult corals (G. fascicularis) can be enhanced via the uptake of exogenously supplied, heat-evolved symbionts, without a trade-off against growth under ambient temperature. Importantly, heat-evolved C. proliferum remained in the corals in moderate abundance 2 years after first inoculation, suggesting long-term stability of this novel symbiosis and potential long-term benefits to coral thermotolerance.

The use of experimentally evolved coral photosymbionts for reef restoration.

The heat tolerance of corals is largely determined by their microbial photosymbionts (Symbiodiniaceae, colloquially known as zooxanthellae). Therefore, manipulating symbiont communities may enhance the ability of corals to survive summer heatwaves. Although heat-tolerant and -sensitive symbiont species occur in nature, even corals that harbour naturally tolerant symbionts have been observed to bleach during summer heatwaves. Experimental evolution (i.e., laboratory selection) of Symbiodiniaceae cultures under elevated temperatures has been successfully used to enhance their upper thermal tolerance, both in vitro and, in some instances, following their reintroduction into corals. In this review, we present the state of this intervention and its potential role within coral reef restoration, and discuss the next critical steps required to bridge the gap to implementation.

Comparing the Role of ROS and RNS in the Thermal Stress Response of Two Cnidarian Models, Exaiptasia diaphana and Galaxea fascicularis.

Coral reefs are threatened by climate change, because it causes increasingly frequent and severe summer heatwaves, resulting in mass coral bleaching and mortality. Coral bleaching is believed to be driven by an excess production of reactive oxygen (ROS) and nitrogen species (RNS), yet their relative roles during thermal stress remain understudied. Here, we measured ROS and RNS net production, as well as activities of key enzymes involved in ROS scavenging (superoxide dismutase and catalase) and RNS synthesis (nitric oxide synthase) and linked these metrics to physiological measurements of cnidarian holobiont health during thermal stress. We did this for both an established cnidarian model, the sea anemone Exaiptasia diaphana, and an emerging scleractinian model, the coral Galaxea fascicularis, both from the Great Barrier Reef (GBR). Increased ROS production was observed during thermal stress in both species, but it was more apparent in G. fascicularis, which also showed higher levels of physiological stress. RNS did not change in thermally stressed G. fascicularis and decreased in E. diaphana. Our findings in combination with variable ROS levels in previous studies on GBR-sourced E. diaphana suggest G. fascicularis is a more suitable model to study the cellular mechanisms of coral bleaching.