skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Thermotolerant coral–algal mutualisms maintain high rates of nutrient transfer while exposed to heat stress
Symbiotic mutualisms are essential to ecosystems and numerous species across the tree of life. For reef-building corals, the benefits of their association with endosymbiotic dinoflagellates differ within and across taxa, and nutrient exchange between these partners is influenced by environmental conditions. Furthermore, it is widely assumed that corals associated with symbionts in the genusDurusdiniumtolerate high thermal stress at the expense of lower nutrient exchange to support coral growth. We traced both inorganic carbon (H13CO3) and nitrate (15NO3) uptake by divergent symbiont species and quantified nutrient transfer to the host coral under normal temperatures as well as in colonies exposed to high thermal stress. Colonies representative of diverse coral taxa associated withDurusdinium trenchiiorCladocopiumspp. exhibited similar nutrient exchange under ambient conditions. By contrast, heat-exposed colonies withD. trenchiiexperienced less physiological stress than conspecifics withCladocopiumspp. while high carbon assimilation and nutrient transfer to the host was maintained. This discovery differs from the prevailing notion that these mutualisms inevitably suffer trade-offs in physiological performance. These findings emphasize that many host–symbiont combinations adapted to high-temperature equatorial environments are high-functioning mutualisms; and why their increased prevalence is likely to be important to the future productivity and stability of coral reef ecosystems.  more » « less
Award ID(s):
1719684 1635695
PAR ID:
10485401
Author(s) / Creator(s):
; ; ; ; ; ;
Publisher / Repository:
The Royal Society
Date Published:
Journal Name:
Proceedings of the Royal Society B: Biological Sciences
Volume:
290
Issue:
2007
ISSN:
0962-8452
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Reef‐building corals in the genusPoritesare one of the most important constituents of Indo‐Pacific reefs. Many species within this genus tolerate abnormally warm water and exhibit high specificity for particular kinds of endosymbiotic dinoflagellates that cope with thermal stress better than those living in other corals. Still, during extreme ocean heating, somePoritesexhibit differences in their stress tolerance. While corals have different physiological qualities, it remains unknown whether the stability and performance of these mutualisms is influenced by the physiology and genetic relatedness of their symbionts. We investigated two ubiquitous Pacific reef corals,Porites rusandPorites cylindrica, from warmer inshore and cooler offshore reef systems in Palau. While these corals harbored a similar kind of symbiont in the genusCladocopium(within the ITS2C15 subclade), rapidly evolving genetic markers revealed evolutionarily diverged lineages corresponding to eachPoritesspecies living in each reef habitat. Furthermore, these closely relatedCladocopiumlineages were differentiated by their densities in host tissues, cell volume, chlorophyll concentration, gross photosynthesis, and photoprotective pathways. When assessed using several physiological proxies, these previously undifferentiated symbionts contrasted in their tolerance to thermal stress. Symbionts withinP.cylindricawere relatively unaffected by exposure to 32℃ for 14 days, whereasP.ruscolonies lost substantial numbers of photochemically compromised symbionts. Heating reduced the ability of the offshore symbiont associated withP.rusto translocate carbon to the coral. By contrast, high temperatures enhanced symbiont carbon assimilation and delivery to the coral skeleton of inshoreP.cylindrica. This study indicates that large physiological differences exist even among closely related symbionts, with significant implications for thermal susceptibility among reef‐buildingPorites. 
    more » « less
  2. Abstract The susceptibility of corals to environmental stress is determined by complex interactions between host genetic variation and the Symbiodiniaceae family community. We exposed genotypes of Montipora capitata hosting primarily Cladocopium or Durusdinium symbionts to ambient conditions and an 8-day heat stress. Symbionts’ cell surface glycan composition differed between genera and was significantly affected by temperature and oxidative stress. The metabolic profile of coral holobionts was primarily shaped by symbionts identity, but was also strongly responsive to oxidative stress. At peak temperature stress, betaine lipids in Cladocopium were remodeled to more closely resemble the abundance and saturation state of Durusdinium symbionts, which paralleled a larger metabolic shift in Cladocopium. Exploring how Symbiodiniaceae members regulate stress and host-symbiont affinity helps identify the traits contributing to coral resilience under climate change. 
    more » « less
  3. Abstract Algal symbiont shuffling in favour of more thermotolerant species has been shown to enhance coral resistance to heat‐stress. Yet, the mechanistic underpinnings and long‐term implications of these changes are poorly understood. This work studied the modifications in coral DNA methylation, an epigenetic mechanism involved in coral acclimatization, in response to symbiont manipulation and subsequent heat stress exposure. Symbiont composition was manipulated in the great star coralMontastraea cavernosathrough controlled thermal bleaching and recovery, producing paired ramets of three genets dominated by either their native symbionts (genusCladocopium) or the thermotolerant species (Durusdinium trenchi). Single‐base genome‐wide analyses showed significant modifications in DNA methylation concentrated in intergenic regions, introns and transposable elements. Remarkably, DNA methylation changes in response to heat stress were dependent on the dominant symbiont, with twice as many differentially methylated regions found in heat‐stressed corals hosting different symbionts (Cladocopiumvs.D.trenchii) compared to all other comparisons. Interestingly, while differential gene body methylation was not correlated with gene expression, an enrichment in differentially methylated regions was evident in repetitive genome regions. Overall, these results suggest that changes in algal symbionts favouring heat tolerant associations are accompanied by changes in DNA methylation in the coral host. The implications of these results for coral adaptation, along with future avenues of research based on current knowledge gaps, are discussed in the present work. 
    more » « less
  4. Abstract Coral reefs are declining globally as climate change and local water quality press environmental conditions beyond the physiological tolerances of holobionts—the collective of the host and its microbial symbionts. To assess the relationship between symbiont composition and holobiont stress tolerance, community diversity metrics were quantified for dinoflagellate endosymbionts (Family: Symbiodiniaceae) from eightAcropora milleporagenets that thrived under or responded poorly to various stressors. These eight selected genets represent the upper and lower tails of the response distribution of 40 coral genets that were exposed to four stress treatments (and control conditions) in a 10‐day experiment. Specifically, four ‘best performer’ coral genets were analyzed at the end of the experiment because they survived high temperature, highpCO2, bacterial exposure, or combined stressors, whereas four ‘worst performer’ genets were characterized because they experienced substantial mortality under these stressors. At the end of the experiment, seven of eight coral genets mainly hostedCladocopiumsymbionts, whereas the eighth genet was dominated by bothCladocopiumandDurusdiniumsymbionts. Symbiodiniaceae alpha and beta diversity were higher in worst performing genets than in best performing genets. Symbiont communities in worst performers also differed more after stress exposure relative to their controls (based on normalized proportional differences in beta diversity), than did best performers. A generalized joint attribute model estimated the influence of host genet and treatment on Symbiodiniaceae community composition and identified strong associations among particular symbionts and host genet performance, as well as weaker associations with treatment. Although dominant symbiont physiology and function contribute to host performance, these findings emphasize the importance of symbiont community diversity and stochasticity as components of host performance. Our findings also suggest that symbiont community diversity metrics may function as indicators of resilience and have potential applications in diverse disciplines from climate change adaptation to agriculture and medicine. 
    more » « less
  5. Abstract While the presence of morphologically cryptic species is increasingly recognized, we still lack a useful understanding of what causes and maintains co‐occurring cryptic species and its consequences for the ecology, evolution, and conservation of communities. We sampled 724Pocilloporacorals from five habitat zones (the fringing reef, back reef, and fore reef at 5, 10, and 20 m) at four sites around the island of Moorea, French Polynesia. Using validated genetic markers, we identified six sympatric species ofPocillopora, most of which cannot be reliably identified based on morphology:P. meandrina(42.9%),P. tuahiniensis(25.1%),P. verrucosa(12.2%),P. acuta(10.4%),P. grandis(7.73%), andP.cf.effusa(2.76%). For 423 colonies (58% of the genetically identified hosts), we also usedpsbAncror ITS2 markers to identify symbiont species (Symbiodiniaceae). The relative abundance ofPocilloporaspecies differed across habitats within the reef. Sister taxaP. verrucosaandP. tuahiniensishad similar niche breadths and hosted the same specialist symbiont species (mostlyCladocopium pacificum) but the former was more common in the back reef and the latter more common deeper on the fore reef. In contrast, sister taxaP. meandrinaandP. grandishad the highest niche breadths and overlaps and tended to host the same specialist symbiont species (mostlyC. latusorum).Pocillopora acutahad the narrowest niche breadth and hosted the generalist, and more thermally tolerant,Durusdinium gynnii. Overall, there was a positive correlation between reef habitat niche breadth and symbiont niche breadth—Pocilloporaspecies with a broader habitat niche also had a broader symbiont niche. Our results show how fine‐scale variation within reefs plays an important role in the generation and coexistence of cryptic species. The results also have important implications for how niche differences affect community resilience, and for the success of coral restoration practices, in ways not previously appreciated. 
    more » « less