Physiological dynamics of cnidarian-dinoflagellate symbioses under climate change
Date
2022
Authors
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Publisher
University of Delaware
Abstract
Mutualistic symbioses between tropical cnidarian hosts and dinoflagellate symbionts are critical to the ecological success and function of coral reefs. Unfortunately, these symbioses are susceptible to climate change stressors, and extreme stress causes bleaching or the loss of symbionts from the host tissue. Thermal anomalies that cause bleaching are increasing in severity and frequency, and many studies have quantified the effects of extreme thermal stress on cnidarian symbioses. However, our understanding of how these relationships will acclimatize and adapt to future environmental conditions is lacking. My first experiment characterizes the physiological and molecular homeostasis reached by three asexual generations of Exaiptasia diaphana after 345 days of sublethal acidification and heating. Physiological acclimation was generation-specific, with later generations recovering or even improving function lost during acclimation in the first generation. However, asexual reproduction declined with acidification and heating in the first two generations suggesting that future environmental conditions could negatively affect anemone reproductive fitness. Unlike the generation-specific physiological response, anemone gene expression responded similarly to acidification and heating across generations. Acclimation to ocean acidification and heating required nuanced transcriptomic regulation that differed from patterns seen in acute stress experiments and were only identified using a novel analysis pipeline. Anemones in the acidification and heating treatment downregulated genes typically upregulated in response to acute stress, including immune signaling, protein folding, and programmed cell death, while upregulating genes associated with biogenesis and metabolism. Together this indicates that the sublethal stress treatment was sufficiently moderate to avoid the coral environmental stress response and suggests that elevated inorganic carbon availability and thermally-induced metabolic increases could support biosynthetic processes. ☐ Dinoflagellate adaptation will also play a role in how symbiotic cnidarians respond to climate change; thus, I investigated the adaptive potential in closely related dinoflagellate strains and assessed their impact on holobiont (host + symbiont) thermal performance. To engineer thermally selected algal populations, I employed a ratchet experimental design to maximize the potential for beneficial mutations to enter the gene pool, followed by a growth period for mutations to become fixed in the population. Only two of four genotypes (G1 and G2) showed trait-based adaptations following 80 generations of growth at elevated temperatures indicating that adaptive potential varies on extremely fine genetic scales. Furthermore, the two adapted genotypes used different mechanisms to support physiological function at elevated temperatures. G1 increased carbon fixation and had lower gross photoinhibition and lower photo-repair than thermally naïve counterparts growing at ambient temperature. In contrast, G2 had higher gross and net photoinhibition rates without a concomitant increase in carbon fixation to support cellular repair. These two adaptive strategies highlight differences in resource allocation between thermally selected algae that likely affected their performance in symbiosis. Indeed, each algal genotype produced a distinct holobiont phenotype in symbiosis with E. diaphana. Interestingly, while G2 had a smaller physiological response to selection, it conferred greater thermal tolerance to its anemone host than G1. Anemones hosting thermally selected G2 symbionts maintained higher photochemical efficiency and photosynthetic oxygen production than anemones hosting thermally naïve G2 symbionts. Conversely, anemones hosting G1 symbionts had high thermal tolerance regardless of symbiont selection. The disparity between the physiological response of G1 symbionts in vitro versus in hospite suggests that the intracellular host environment significantly modulated symbiont’s response to thermal stress. While symbiont adaptive potential differs on fine genetic scales, increased thermal tolerance in vitro is not necessarily conferred to intact symbiosis, and other host-related factors also contribute significantly to the holobiont thermal stress response. ☐ Finally, I investigated the thermal tolerance of natural coral populations to assess how different tolerant symbionts and life-history traits affect thermal tolerance. In Palau, and on reefs around the world, corals either acquire symbionts with each generation from environmental sources (horizontally) and harbor host-generalist symbionts, or they acquire symbionts from the maternal line (vertically) and harbor highly co-evolved specialist symbionts. I compared the thermal response of two corals, Pocillopora verrucosa, a vertical transmitter that hosts specialist symbionts, and Psammocora digitata, a horizontal transmitter that hosts generalist symbionts. Corals were collected from inshore and offshore reefs where corals hosted different thermally tolerant Durusdinium and thermally sensitive Cladocopium symbionts, respectively. While experimental thermal stress confirmed higher thermal tolerance in inshore versus offshore corals of both species, the vertically transmitting P. verrucosa demonstrated greater physiological stability than P. digitata. P. verrucosa from both reefs maintained the ability to assimilate carbon (13C) and nitrogen (15NO3–) when heated. In contrast, heated P. digitata from both locations experienced greater physiological variability and greater loss in the ability to assimilate carbon (13C) and nitrogen (15NO3–). Partner co-evolution could facilitate metabolic stability in reef-building coral symbioses as sea surface temperatures continue to rise.
Description
Keywords
Cnidarian, Coral, Physiology, Symbiodiniaceae, Symbiosis