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

Abstract

ABSTRACTOcean 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-typeC. proliferumstrain. Thermotolerance of SS8-corals was similar to that of coral fragments from the same colony hosting the homologous symbiont,Durusdiniumsp., 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 toDurusdinium-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-typeC. 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-evolvedC. proliferumremains in the corals in moderate abundance two years after its first inoculation, suggesting long-term stability of this novel symbiosis.