Rapid thermal adaptation in photosymbionts of reef‐building corals

Abstract

Climate warming is occurring at a rate not experienced by life on Earth for 10 s of millions of years, and it is unknown whether the coral-dinoflagellate (Symbiodinium spp.) symbiosis can evolve fast enough to ensure coral reef persistence. Coral thermal tolerance is partly dependent on the Symbiodinium hosted. Therefore, directed laboratory evolution in Symbiodinium has been proposed as a strategy to enhance coral holobiont thermal tolerance. Using a reciprocal transplant design, we show that the upper temperature tolerance and temperature tolerance range of Symbiodinium C1 increased after ~80 asexual generations (2.5 years) of laboratory thermal selection. Relative to wild-type cells, selected cells showed superior photophysiological performance and growth rate at 31°C in vitro, and performed no worse at 27°C; they also had lower levels of extracellular reactive oxygen species (exROS). In contrast, wild-type cells were unable to photosynthesise or grow at 31°C and produced up to 17 times more exROS. In symbiosis, the increased thermal tolerance acquired ex hospite was less apparent. In recruits of two of three species tested, those harbouring selected cells showed no difference in growth between the 27 and 31°C treatments, and a trend of positive growth at both temperatures. Recruits that were inoculated with wild-type cells, however, showed a significant difference in growth rates between the 27 and 31°C treatments, with a negative growth trend at 31°C. There were no significant differences in the rate and severity of bleaching in coral recruits harbouring wild-type or selected cells. Our findings highlight the need for additional Symbiodinium genotypes to be tested with this assisted evolution approach. Deciphering the genetic basis of enhanced thermal tolerance in Symbiodinium and the cause behind its limited transference to the coral holobiont in this genotype of Symbiodinium C1 are important next steps for developing methods that aim to increase coral bleaching tolerance.

Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility

“…For example, populations of two Breviolum B1 species ( B. antillogorgium and B. minutum ) from the same host species and reef site encompass standing genetic variation in heat and nutrient tolerance, as well as photosynthesis traits (Bayliss, Scott, Coffroth, & terHorst, ). Additionally, a monoclonal culture of Cladocopium C1 became adapted to elevated temperature within 2.5 years (~80 asexual generations) and tended to improve the outcomes for inoculated coral hosts under heat stress (Chakravarti, Beltran, & van Oppen, ; see also Chakravarti & van Oppen, ). While contemporary adaptation in natural Symbiodiniaceae populations remains to be demonstrated, fidelity for specific symbiont partners (i.e., putative species) does not negate the capacity for a symbiont role in coral adaptation.…”

Rapid adaptive responses to climate change in corals

“…The well-studied coral-Symbiodinium association best illustrates the potential of microbial symbionts to effect rapid phenotypic change at the level of the coral holobiont, either through their own evolution 70 or changes in community composition (Fig. 3).…”

Microbiome engineering: enhancing climate resilience in corals

“…; Chakravarti et al . ). Advances in coral ME for addressing climate‐change impacts may also focus on indirect selection.…”

“…Other researchers have begun to investigate the possibility of inoculating corals with heat‐selected members of the Symbiodiniaceae (Chakravarti et al . ) or communities of bacteria from “donor” heat‐resistant corals (Damjanovic et al . ), with the goal of increasing coral resilience to thermal stress.…”

“…; Chakravarti et al . ; Damjanovic et al . ), theoretical work – including the Coral Probiotic Hypothesis (Reshef et al .…”