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1. Thermotolerant coral symbionts modulate heat stress‐responsive genes in their hosts

   https://doi.org/10.1111/mec.15526  

   Cunning, Ross ; Baker, Andrew C. ( July 2020 , Molecular Ecology)

   Some corals may become more resistant to bleaching by shuffling their Symbiodiniaceae communities toward thermally tolerant species, and manipulations to boost the abundance of these symbionts in corals may increase resilience in warming oceans. However, the thermotolerant symbiontDurusdinium trenchiimay reduce growth and fecundity in Caribbean corals, and these tradeoffs need to be better understood as this symbiont spreads through the region. We sought to understand howD. trenchiimodulates coral gene expression by manipulating symbiont communities inMontastraea cavernosato produce replicate ramets containingD. trenchiitogether with paired ramets of these same genets (n = 3) containingCladocopiumC3 symbionts. We then examined differences in global gene expression between corals hostingDurusdiniumandCladocopiumunder control temperatures, and in response to short‐term heat stress. We identified numerous transcriptional differences associated with symbiont identity, which explained 2%–14% of the transcriptional variance. Corals withD. trenchiiupregulated genes related to translation, ribosomal structure and biogenesis, and downregulated genes related to extracellular structures, and carbohydrate and lipid transport and metabolism, relative to corals withCladocopium. Unexpectedly, these changes were similar to those observed inCladocopium‐dominated corals in response to heat stress, suggesting that thermotolerantD. trenchiimay cause corals to increase expression of heat stress‐responsive genes, explaining both the increased heat tolerance and the associated energetic tradeoffs in corals containingD. trenchii. These findings provide insight into the ecological changes occurring on contemporary coral reefs in response to climate change, and the diverse ways in which different symbionts modulate emergent phenotypes of their hosts.

    

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2. Different functional traits among closely related algal symbionts dictate stress endurance for vital Indo‐Pacific reef‐building corals

   https://doi.org/10.1111/gcb.15799  

   Hoadley, Kenneth D. ; Pettay, Daniel. T. ; Lewis, Allison ; Wham, Drew ; Grasso, Chris ; Smith, Robin ; Kemp, Dustin W. ; LaJeunesse, Todd ; Warner, Mark E. ( August 2021 , Global Change Biology)

   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.

    

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3. The role of the endolithic alga Ostreobium spp. during coral bleaching recovery

   https://doi.org/10.1038/s41598-022-07017-6  

   Galindo-Martínez, Claudia Tatiana ; Weber, Michele ; Avila-Magaña, Viridiana ; Enríquez, Susana ; Kitano, Hiroaki ; Medina, Mónica ; Iglesias-Prieto, Roberto ( February 2022 , Scientific Reports)

   In this study, we explore how the Caribbean coral Orbicella faveolata recovers after bleaching, using fragments from 13 coral colonies exposed to heat stress (32 °C) for ten days. Biological parameters and coral optical properties were monitored during and after the stress. Increases in both, the excitation pressure over photosystem II (Qm) and pigment specific absorption (a*_Chla) were observed in the stressed corals, associated with reductions in light absorption at the chlorophyll a red peak (D_e675) and symbiont population density. All coral fragments exposed to heat stress bleached but a fraction of the stressed corals recovered after removing the stress, as indicated by the reductions in Q_m and increases in D_e675 and the symbiont population observed. This subsample of the experimentally bleached corals also showed blooms of the endolithic algae Ostreobium spp. underneath the tissue. Using a numerical model, we quantified the amount of incident light reflected by the coral, and absorbed by the different pigmented components: symbionts, host-tissue and Ostreobiumspp. Our study supports the key contribution of Ostreobiumspp. blooms near the skeletal surface, to coral recovery after bleaching by reducing skeleton reflectance. Endolithic blooms can thus significantly alleviate the high light stress that affects the remaining symbionts during the stress or when the coral has achieved the bleached phenotype.

    

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4. Symbiont shuffling induces differential DNA methylation responses to thermal stress in the coral Montastraea cavernosa

   https://doi.org/10.1111/mec.16246  

   Rodriguez‐Casariego, Javier A. ; Cunning, Ross ; Baker, Andrew C. ; Eirin‐Lopez, Jose M. ( November 2021 , Molecular Ecology)

   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.

    

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5. Symbiont community diversity is more variable in corals that respond poorly to stress

   https://doi.org/10.1111/gcb.14999  

   Howe‐Kerr, Lauren I. ; Bachelot, Benedicte ; Wright, Rachel M. ; Kenkel, Carly D. ; Bay, Line K. ; Correa, Adrienne M. S. ( February 2020 , Global Change Biology)

   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.

    

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