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: Different functional traits among closely related algal symbionts dictate stress endurance for vital Indo‐Pacific reef‐building corals
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
Award ID(s):
1719684 1635695
PAR ID:
10449620
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Global Change Biology
Volume:
27
Issue:
20
ISSN:
1354-1013
Page Range / eLocation ID:
p. 5295-5309
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. 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
  2. ABSTRACT As ocean warming threatens reefs worldwide, identifying corals with adaptations to higher temperatures is critical for conservation. Genetically distinct but morphologically similar (i.e. cryptic) coral populations can be specialized to extreme habitats and thrive under stressful conditions. These corals often associate with locally beneficial microbiota (Symbiodiniaceae photobionts and bacteria), obscuring the main drivers of thermal tolerance. Here, we leverage a holobiont (massivePorites) with high fidelity for C15 photobionts to investigate adaptive variation across classic (“typical” conditions) and extreme reefs characterized by higher temperatures and light attenuation. We uncovered three cryptic lineages that exhibit limited micro‐morphological variation; one lineage dominated classic reefs (L1), one had more even distributions (L2), and a third was restricted to extreme reefs (L3). L1 and L2 were more closely related to populations ~4300 km away, suggesting that some lineages are widespread. All corals harboredCladocopiumC15 photobionts; L1 and L2 shared a photobiont pool that differed in composition between reef types, yet L3 mostly harbored unique photobiont strains not found in the other lineages. Assemblages of bacterial partners differed among reef types in lineage‐specific ways, suggesting that lineages employ distinct microbiome regulation strategies. Analysis of light‐harvesting capacity and thermal tolerance revealed adaptive variation underpinning survival in distinct habitats: L1 had the highest light absorption efficiency and lowest thermal tolerance, suggesting that it is a classic reef specialist. L3 had the lowest light absorption efficiency and the highest thermal tolerance, showing that it is an extreme reef specialist. L2 had intermediate light absorption efficiency and thermal tolerance, suggesting that is a generalist lineage. These findings reveal diverging holobiont strategies to cope with extreme conditions. Resolving coral lineages is key to understanding variation in thermal tolerance among coral populations, can strengthen our understanding of coral evolution and symbiosis, and support global conservation and restoration efforts. 
    more » « less
  3. Abstract Coral bleaching events from thermal stress are increasing globally in duration, frequency, and intensity. While bleaching can cause mortality, some corals survive, reacquire symbionts, and recover. We experimentally bleachedMontipora capitatato examine molecular and physiological differences between corals that recover (resilient) and those that die (susceptible). Corals were collected and monitored for eight months post-bleaching to identify genets with long-term resilience. Using an integrated systems-biology approach that included quantitative proteomics, 16S rRNA sequencing to characterize the coral microbiome, total coral lipids, symbiont community composition and density, we explored molecular-level mechanisms of tolerance in corals pre- and post-bleaching. Prior to thermal stress, resilient corals have a more diverse microbiome and abundant proteins essential for carbon acquisition, symbiont retention, and pathogen resistance. Protein signatures of susceptible corals showed early symbiont rejection and utilized urea for carbon and nitrogen. Our results reveal molecular factors for surviving bleaching events and identify diagnostic protein biomarkers for reef management and restoration. 
    more » « less
  4. 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
  5. Abstract Filamentous viruses are hypothesized to play a role in stony coral tissue loss disease (SCTLD) through infection of the endosymbiotic dinoflagellates (Family Symbiodiniaceae) of corals. To evaluate this hypothesis, it is critical to understand the global distribution of filamentous virus infections across the genetic diversity of Symbiodiniaceae hosts. Using transmission electron microscopy, we demonstrate that filamentous virus-like particles (VLPs) are present in over 60% of Symbiodiniaceae cells (genusCladocopium) within Pacific corals (Acropora hyacinthus,Porites c.f. lobata); these VLPs are more prevalent in Symbiodiniaceae of in situ colonies experiencing heat stress. Symbiodiniaceae expelled fromA. hyacinthusalso contain filamentous VLPs, and these cells are more degraded than theirin hospitecounterparts. Similar to VLPs reported from SCTLD-affected Caribbean reefs, VLPs range from ~150 to 1500 nm in length and 16–37 nm in diameter and appear to constitute various stages in a replication cycle. Finally, we demonstrate that SCTLD-affected corals containing filamentous VLPs are dominated by diverse Symbiodiniaceae lineages from the generaBreviolum, Cladocopium, andDurusdinium. Although this study cannot definitively confirm or refute the role of filamentous VLPs in SCTLD, it demonstrates that filamentous VLPs are not solely observed in SCTLD-affected corals or reef regions, nor are they solely associated with corals dominated by members of a particular Symbiodiniaceae genus. We hypothesize that filamentous viruses are a widespread, common group that infects Symbiodiniaceae. Genomic characterization of these viruses and empirical tests of the impacts of filamentous virus infection on Symbiodiniaceae and coral colonies should be prioritized. 
    more » « less