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

ABSTRACT 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 chemically bleached adult fragments of the scleractinian coral, Galaxea fascicularis . The new symbionts persisted for the five 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. Our findings show that adult coral thermotolerance can be enhanced via the uptake of exogenously supplied, heat-evolved symbionts, without a trade-off against growth under ambient temperature. Heat-evolved C. proliferum remains in the corals in moderate abundance two years after its first inoculation, suggesting long-term stability of this novel symbiosis.