Explore the vast range of titles available.

As coral reefs struggle to survive under climate change, it is crucial to know whether they have the capacity to withstand changing conditions, particularly increasing seawater temperatures. Thermal tolerance requires the integrative response of the different components of the coral holobiont (coral host, algal photosymbiont, and associated microbiome). Here, using a controlled thermal stress experiment across three divergent Caribbean coral species, we attempt to dissect holobiont member metatranscriptome responses from coral taxa with different sensitivities to heat stress and use phylogenetic ANOVA to study the evolution of gene expression adaptation. We show that coral response to heat stress is a complex trait derived from multiple interactions among holobiont members. We identify host and photosymbiont genes that exhibit lineage-specific expression level adaptation and uncover potential roles for bacterial associates in supplementing the metabolic needs of the coral-photosymbiont duo during heat stress. Our results stress the importance of integrative and comparative approaches across a wide range of species to better understand coral survival under the predicted rise in sea surface temperatures. As corals struggle to survive under climate change, it is crucial to know whether they can withstand increasing seawater temperatures. Using a controlled thermal stress experiment across three divergent coral holobionts, this study examines metatranscriptomic responses to heat stress corresponding to the coral host, photosymbionts and associated microbiota.

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* Chl a ) 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  Ostreobium spp. Our study supports the key contribution of  Ostreobium spp .  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.

The success of symbiotic reef-building corals is largely determined by the efficiency with which they collect solar energy. Using thin coral laminae from the Caribbean scleractinian Porites branneri, we characterize the absorption spectra of intact coral surfaces. Comparisons of absorption spectra from corals with a broad range of photosynthetic pigment densities, collected during a natural bleaching event, indicate that they are capable of collecting more than 85% of solar radiation with one order of magnitude less pigment density than terrestrial leaves. Measurements of the light-absorption efficiency as a function of pigment density reveal that symbiotic algae in intact P. branneri absorb between two and five more light than freshly isolated symbionts. A theoretical model shows that multiple scattering by the skeleton can enhance the local light field, thus increasing absorption. As a result of this phenomenon, corals inhabiting high light environments can maximize their absorption capacity with low pigment investment while reducing self-shading in low-light environments. Local light field enhancements may have negative effects when corals are exposed to stressful conditions. During coral bleaching, increases in local irradiance associated with reductions in pigment density could exacerbate the negative effect of elevated temperatures. Symbiotic scleractinian corals are one of the most efficient solar energy collectors in nature, and the modulation of the internal light field by the coral skeleton may be an important driving force in the evolution of this group.

The potential effects of seasonal acclimatization on coral sensitivity to heat-stress, has received limited attention despite differing bleaching thresholds for summer and winter. In this study, we examined the response of two contrasting phenotypes, termed winter and summer, of four Caribbean reef corals to similar light and heat-stress levels. The four species investigated were categorized into two groups: species with the ability to harbour large number of symbionts, Orbicella annularis and O . faveolata , and species with reduced symbiont density ( Montastraea cavernosa and Pseudodiploria strigosa ). The first group showed higher capacity to enhance photosynthetic rates per area (P max ), while P max enhancement in the second group was more dependent on Symbiodinium performance (P sym ). In summer all four species presented higher productivity, but also higher sensitivity to lose coral photosynthesis under heat-stress. In contrast, corals in winter exhibit symbionts with higher capacity to photoacclimate to the increased levels of light-stress elicited by heat-stress. Overall, our study supports the importance of the acclimatory coral condition in addition to the previous thermal history, to determine the severity of the impact of heat-stress on coral physiology, but also the dependence of this response on the particular structural and functional traits of the species.

Multiple scattering of light on coral skeleton enhances light absorption efficiency of coral symbionts and plays a key role in the regulation of their internal diffuse light field. To understand the dependence of this enhancement on skeleton meso- and macrostructure, we analysed the scattering abilities of naked coral skeletons for 74 Indo-Pacific species. Sensitive morphotypes to thermal and light stress, flat-extraplanate and branching corals, showed the most efficient structures, while massive-robust species were less efficient. The lowest light-enhancing scattering abilities were found for the most primitive colonial growth form: phaceloid. Accordingly, the development of highly efficient light-collecting structures versus the selection of less efficient but more robust holobionts to cope with light stress may constitute a trade-off in the evolution of modern symbiotic scleractinian corals, characterizing two successful adaptive solutions. The coincidence of the most important structural modifications with epitheca decline supports the importance of the enhancement of light transmission across coral skeleton in modern scleractinian diversification, and the central role of these symbioses in the design and optimization of coral skeleton. Furthermore, the same ability that lies at the heart of the success of symbiotic corals as coral-reef-builders can also explain the ‘Achilles's heel’ of these symbioses in a warming ocean.

Human-induced environmental changes have ushered in the rapid decline of coral reef ecosystems, particularly by disrupting the symbioses between reef-building corals and their photosymbionts. However, escalating stressful conditions enable some symbionts to thrive as opportunists. We present evidence that a stress-tolerant “zooxanthella” from the Indo-Pacific Ocean, Symbiodinium trenchii , has rapidly spread to coral communities across the Greater Caribbean. In marked contrast to populations from the Indo-Pacific, Atlantic populations of S. trenchii contained exceptionally low genetic diversity, including several widespread and genetically similar clones. Colonies with this symbiont tolerate temperatures 1–2 °C higher than other host–symbiont combinations; however, calcification by hosts harboring S. trenchii is reduced by nearly half, compared with those harboring natives, and suggests that these new symbioses are maladapted. Unforeseen opportunism and geographical expansion by invasive mutualistic microbes could profoundly influence the response of reef coral symbioses to major environmental perturbations but may ultimately compromise ecosystem stability and function. Significance This research documents the spread of an opportunistic coral endosymbiont, Symbiodinium trenchii , from the Indo-Pacific into the Greater Caribbean, a region afflicted by human-related impacts including climate warming and environmental degradation. As a symbiont, it increases the resilience of photosynthetic corals to environmental perturbation but may diminish the animal’s capacity to calcify and build reefs. This work exposes a critical need to better understand the consequences of microbial introductions (even mutualistic species) on ecosystem stability and function and raises questions about the long-term impact of new, but maladapted, symbioses on the productivity of reef coral communities in the Atlantic Ocean.

Symbiotic corals display a great array of morphologies, each of which has unique effects on light interception and the photosynthetic performance of in hospite zooxanthellae. Changes in light availability elicit photoacclimation responses to optimize the energy balances in primary producers, extensively documented for corals exposed to contrasting light regimes along depth gradients. Yet, response variation driven by coral colony geometry and its energetic implications on colonies with contrasting morphologies remain largely unknown. In this study, we assessed the effect of the inclination angle of coral surface on light availability, short- and long-term photoacclimation responses, and potential photosynthetic usable energy. Increasing surface inclination angle resulted in an order of magnitude reduction of light availability, following a linear relationship explained by the cosine law and relative changes in the direct and diffuse components of irradiance. The light gradient induced by surface geometry triggered photoacclimation responses comparable to those observed along depth gradients: changes in the quantum yield of photosystem II, photosynthetic parameters, and optical properties and pigmentation of the coral tissue. Differences in light availability and photoacclimation driven by surface inclination led to contrasting energetic performance. Horizontally and vertically oriented coral surfaces experienced the largest reductions in photosynthetic usable energy as a result of excessive irradiance and light-limiting conditions, respectively. This pattern is predicted to change with depth or local water optical properties. Our study concludes that colony geometry plays an essential role in shaping the energy balance and determining the light niche of zooxanthellate corals.

Community dynamics and physiology of Symbiodinium associated with Orbicella (= Montastraea) faveolata were examined before, during, and after a thermally induced coral bleaching event in Puerto Morelos, Mexico. We combined microsampling molecular genotyping with in situ pulse-amplitude modulated fluorometry to correlate colony variability of Symbiodinium population identities and the phenomena of partial coral bleaching. Pigmented nonbleached portions of O. (=M.) faveolata were compared with bleached portions of the same colony. During bleaching, maximum quantum yield of photosystem II (PSII; Fv : Fm) was significantly lower and highly variable (range 0.110 to 0.680) compared with previous summers in which coral bleaching was absent (range 0.516 to 0.661) and recovery (range 0.480 to 0.716). Differential susceptibility to environmental perturbation of Fv : Fm corresponded to distinct genetic identities of Symbiodinium. Analysis of ribosomal deoxyribonucleic acid (rDNA) internal transcribed spacer 2 (ITS2) revealed regions of the coral colonies that had phylotype A3 prior to bleaching were more resistant to the bleaching perturbation than adjacent bleaching-prone patches that harbored phylotypes B17 and C7. During environmental perturbation, regions of the colonies containing predominantly Symbiodinium phylotypes A3 or D1a retained significantly higher Fv : Fm values than adjacent regions with phylotypes B17 and C7. Following bleaching, rapid recovery of symbiotic algal densities greatly exceeded normal seasonal oscillations. During recovery we document shifts in Symbiodinium populations and increase prevalence of Symbiodinium types A3 and D1a, phylotypes known to have enhanced thermal tolerances. Thermal tolerance of Symbiodinium spp. influences the changes of coral–Symbiodinium communities during disturbance events and the dynamics of coral–Symbiodinium repopulation.

In order to understand the contribution of pigmented coral tissues to the extraordinary optical properties of the coral-symbiont-skeleton unit, we analyzed the associations between structural and optical traits for four coral species, which broadly differ in skeleton morphology, tissue thickness and in the variation of coral pigmentation, symbiont content, Symbiodinium dominant type and Symbiodinium cell pigmentation (Ci). Significant differences among species were found for the maximum capacity of light absorption (Amax) and for the minimum pigmentation required to reach that maximum. The meandroid morphotype represented by Pseudodiploria strigosa showed a slightly lower Amax than the other three chalice-type species, while the thickest species, Montastraea cavernosa, required 2 to 3.5 times higher pigmentation to reach Amax. In contrast, Orbicella faveolata and O. annularis, which were able to harbour high number of symbionts and achieve the highest photosynthetic rates per area, showed the largest abilities for light collection at decreasing symbiont densities, leading to a more fragile photophysiological condition under light and heat-stress. Holobiont photosynthesis was more dependent on Symbiodinium performance in the less populated organisms. At reduced pigmentation, we observed a similar non-linear increase in holobiont light absorption efficiency (a*Chla), which was differentially modulated by reductions in the number of symbionts and Symbiodinium Ci. For similar pigmentation, larger symbiont losses relative to Ci declines resulted in smaller increases in a*Chla. Two additional optical traits were used to characterize light absorption efficiency of Symbiodinium (a*sym) and coral host (a*M). Optimization of a*sym was well represented by P. strigosa, whereas a*M was better optimized by O. annularis. The species with the largest symbiont content, O. faveolata, and with the thickest tissues, M. cavernosa, represented, respectively, less efficient solutions for both coral traits. Our comparison demonstrates the utility of optical traits to characterize inter-specific differences in coral acclimatization and performance. Furthermore, holobiont light absorption efficiency (a*Chla) appeared as a better proxy for the “bleached phenotype” than simple reductions in coral color. The analysis of a putative coordinated variation in the number of symbionts and in Symbiodinium cell pigmentation deserves special attention to understand holobiont optimization of energy collection (a*Chla) and photosynthetic performance.

The biodiversity in coral reef ecosystems is distributed heterogeneously across spatial and temporal scales, being commonly influenced by biogeographic factors, habitat area and disturbance frequency. A potential association between gradients of usable energy and biodiversity patterns has received little empirical support in these ecosystems. Here, we analyzed the productivity and biodiversity variation over depth gradients in symbiotic coral communities, whose members rely on the energy translocated by photosynthetic algal symbionts (zooxanthellae). Using a mechanistic model we explored the association between the depth-dependent variation in photosynthetic usable energy to corals and gradients of species diversity, comparing reefs with contrasting water clarity and biodiversity patterns across global hotspots of marine biodiversity. The productivity-biodiversity model explained between 64 and 95% of the depth-related variation in coral species richness, indicating that much of the variation in species richness with depth is driven by changes in the fractional contribution of photosynthetically fixed energy by the zooxanthellae. These results suggest a fundamental role of solar energy availability and photosynthetic production in explaining global-scale patterns of coral biodiversity and community structure along depth gradients. Accordingly, the maintenance of water optical quality in coral reefs is fundamental to protect coral biodiversity and prevent reef degradation.