Phenotypic plasticity for improved light harvesting, in tandem with methylome repatterning in reef-building corals.

Acclimatization through phenotypic plasticity represents a more rapid response to environmental change than adaptation and is vital to optimize organisms' performance in different conditions. Generally, animals are less phenotypically plastic than plants, but reef-building corals exhibit plant-like properties. They are light dependent with a sessile and modular construction that facilitates rapid morphological changes within their lifetime. We induced phenotypic changes by altering light exposure in a reciprocal transplant experiment and found that coral plasticity is a colony trait emerging from comprehensive morphological and physiological changes within the colony. Plasticity in skeletal features optimized coral light harvesting and utilization and paralleled significant methylome and transcriptome modifications. Network-associated responses resulted in the identification of hub genes and clusters associated to the change in phenotype: inter-partner recognition and phagocytosis, soft tissue growth and biomineralization. Furthermore, we identified hub genes putatively involved in animal photoreception-phototransduction. These findings fundamentally advance our understanding of how reef-building corals repattern the methylome and adjust a phenotype, revealing an important role of light sensing by the coral animal to optimize photosynthetic performance of the symbionts.

Microbial invasion of the Caribbean by an Indo-Pacific coral zooxanthella.

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.

Key functional role of the optical properties of coral skeletons in coral ecology and evolution.

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.

Absorptance determinations on multicellular tissues.

The analysis of the variation of the capacity and efficiency of photosynthetic tissues to collect solar energy is fundamental to understand the differences among species in their ability to transform this energy into organic molecules. This analysis may also help to understand natural changes in species distribution and/or abundance, and differences in species ability to colonize contrasting light environments or respond to environmental changes. Unfortunately, the challenge that optical determinations on highly dispersive samples represent has strongly limited the progression of this analysis on multicellular tissues, limiting our knowledge of the role that optical properties of photosynthetic tissues may play in the optimization of photosynthesis and growth of benthonic primary producers. The aim of this study is to stimulate the use of optical tools in marine eco-physiology, offering a succinct description of the more convenient tools and also solutions to resolve the more common technical difficulties that arise while performing optical determinations on highly dispersive samples. Our study focuses on two-dimensional (2D-) parameters: absorptance, transmittance, and reflectance, and illustrates with correct and incorrect examples, specific problems and their respective solutions. We also offer a general view of the broad variation in light absorption shown by photosynthetic structures of marine primary producers, and its low association with pigment content. The ecological and evolutionary functional implications of this variability deserve to be investigated across different taxa, populations, and marine environments.

Global inequities between polluters and the polluted: climate change impacts on coral reefs.

For many ecosystem services, it remains uncertain whether the impacts of climate change will be mostly negative or positive and how these changes will be geographically distributed. These unknowns hamper the identification of regional winners and losers, which can influence debate over climate policy. Here, we use coral reefs to explore the spatial variability of climate stress by modelling the ecological impacts of rising sea temperatures and ocean acidification, two important coral stressors associated with increasing greenhouse gas (GHG) emissions. We then combine these results with national per capita emissions to quantify inequities arising from the distribution of cause (CO2 emissions) and effect (stress upon reefs) among coral reef countries. We find pollution and coral stress are spatially decoupled, creating substantial inequity of impacts as a function of emissions. We then consider the implications of such inequity for international climate policy. Targets for GHG reductions are likely to be tied to a country's emissions. Yet within a given level of GHG emissions, our analysis reveals that some countries experience relatively high levels of impact and will likely experience greater financial cost in terms of lost ecosystem productivity and more extensive adaptation measures. We suggest countries so disadvantaged be given access to international adaptation funds proportionate with impacts to their ecosystem. We raise the idea that funds could be more equitably allocated by formally including a metric of equity within a vulnerability framework.

Effects of surface geometry on light exposure, photoacclimation and photosynthetic energy acquisition in zooxanthellate corals.

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.

The PsbO homolog from Symbiodinium kawagutii (Dinophyceae) characterized using biochemical and molecular methods.

A photosystem II component, the PsbO protein is essential for maximum rates of oxygen production during photosynthesis, and has been extensively characterized in plants and cyanobacteria but not in symbiotic dinoflagellates. Its close interaction with D1 protein has important environmental implications since D1 has been identified as the primary site of damage in endosymbiotic dinoflagellates after thermal stress. We identified and biochemically characterized the PsbO homolog from Symbiodinium kawagutii as a 28-kDa protein, and immunolocalized it to chloroplast membranes. Chloroplast association was further confirmed by western blot on photosynthetic membrane preparations. TX-114 phase partitioning, chromatography, and SDS-PAGE for single band separation and partial peptide sequencing yielded peptides identical or with high identity to PsbO from dinoflagellates. Analysis of a cDNA library revealed three genes differing by only one aminoacid residue in the in silico-translated ORFs despite greater differences at nucleotide level in the untranslated, putative regulatory sequences. The consensus full amino acid sequence displayed all the characteristic domains and features of PsbO from other sources, but changes in functionally critical, highly conserved motifs were detected. Our biochemical, molecular, and immunolocalization data led to the conclusion that the 28-kDa protein from S. kawagutii is the PsbO homolog, thereby named SkPsbO. We discuss the implications of critical amino acid substitutions for a putative regulatory role of this protein.

The δ15N in Orbicella faveolata organic matter reveals anthropogenic impact by sewage inputs in a Mexican Caribbean coral reef lagoon.

Coral-reef ecosystems provide essentials services to human societies, representing the most important source of income (e.g., tourism and artisanal fishing) for many coastal developing countries. In the Caribbean region, most touristic and coastal developments are in the vicinity of coral reefs where they may contribute to reef degradation. Here we evaluated the influence of sewage inputs in the coral reef lagoon of Puerto Morelos during a period of 40 years (1970-2012). Annual δ15N values were determined in the organic matter (OM) extracted from coral skeletons of Orbicella faveolata. Average protein content in the OM was 0.33 mg of protein g-1 CaCO3 (±0.10 SD) and a 0.03% of OM relative to the sample weight (n =100). The average of N g-1 CaCO3 was 0.002% (± 0.001 SD). The results showed an increase (p < 0.001) in δ15N over the time, positively correlated with population growth derived from touristic development. These findings emphasize the need to generate urban-planning remediation strategies that consider the impact on natural environments, reduce sewage pollution, and mitigate local stressors that threaten the status of coral-reef communities in the Caribbean region.

Evaluation of the current understanding of the impact of climate change on coral physiology after three decades of experimental research.

After three decades of coral research on the impacts of climate change, there is a wide consensus on the adverse effects of heat-stress, but the impacts of ocean acidification (OA) are not well established. Using a review of published studies and an experimental analysis, we confirm the large species-specific component of the OA response, which predicts moderate impacts on coral physiology and pigmentation by 2100 (scenario-B1 or SSP2-4.5), in contrast with the severe disturbances induced by only +2 °C of thermal anomaly. Accordingly, global warming represents a greater threat for coral calcification than OA. The incomplete understanding of the moderate OA response relies on insufficient attention to key regulatory processes of these symbioses, particularly the metabolic dependence of coral calcification on algal photosynthesis and host respiration. Our capacity to predict the future of coral reefs depends on a correct identification of the main targets and/or processes impacted by climate change stressors.

Photosynthetic usable energy explains vertical patterns of biodiversity in zooxanthellate corals.

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.

Validation of parameters and protocols derived from chlorophyll a fluorescence commonly utilised in marine ecophysiological studies.

This study documents the first validation of the suitability of the most common parameters and protocols used in marine ecophysiology to characterise photosynthesis by means of chlorophyll a fluorescence tools. We demonstrate that the effective yield of PSII (ΔF /F m ') is significantly underestimated when using short inductions times (≤1 min) following the rapid light curve protocol (RLC). The consequent electron transport rates (ETR) underestimations are species-specific and highly variable with irradiance and the photoacclimatory condition of the sample. Our analysis also questions the use of relative descriptors (relETR), as they not only overestimate photosynthesis, but overlook one of the fundamental components of the photosynthetic response: light absorption regulation. Absorptance determinations were fundamental to characterise the ETR response of low-pigmented seagrass leaves, and also uncovered relevant differences between two coral species and the accclimatory response of a cultured dinoflagellate to temperature. ETR and oxygen evolution determinations showed close correlations for all organisms tested with the expected slope of 4 e- per O2 molecule evolved, when correct photosynthesis inductions and light absorption determinations were applied. However, ETR curves cannot be equated to conventional photosynthetic response to irradiance (P vs E ) curves, and caution is needed when using ETR to characterise photosynthesis rates above photosynthesis saturation (E k ). This validation strongly supports the utility of fluorescence tools, underlining the need to correct two decades of propagation of erroneous concepts, protocols and parameters in marine eco-physiology. We aim also to emphasise the importance of optical descriptions for understanding photosynthesis, and for interpreting fluorescence measurements. In combination with conventional gross photosynthesis (GPS) approaches, optical characterisations open an extraordinary opportunity to determine two central parameters of photosynthesis performance: the quantum yield (φmax ) of the process and its minimum quantum requirements (1/φmax ). The combination of both approaches potentiates the possibilities of chlorophyll a fluorescence tools to characterise marine photosynthesis biodiversity.

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

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 (De675) 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 Qm and increases in De675 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.

Linking photoacclimation responses and microbiome shifts between depth-segregated sibling species of reef corals.

Metazoans host complex communities of microorganisms that include dinoflagellates, fungi, bacteria, archaea and viruses. Interactions among members of these complex assemblages allow hosts to adjust their physiology and metabolism to cope with environmental variation and occupy different habitats. Here, using reciprocal transplantation across depths, we studied adaptive divergence in the corals Orbicella annularis and O. franksi, two young species with contrasting vertical distribution in the Caribbean. When transplanted from deep to shallow, O. franksi experienced fast photoacclimation and low mortality, and maintained a consistent bacterial community. By contrast, O. annularis experienced high mortality and limited photoacclimation when transplanted from shallow to deep. The photophysiological collapse of O. annularis in the deep environment was associated with an increased microbiome variability and reduction of some bacterial taxa. Differences in the symbiotic algal community were more pronounced between coral species than between depths. Our study suggests that these sibling species are adapted to distinctive light environments partially driven by the algae photoacclimation capacity and the microbiome robustness, highlighting the importance of niche specialization in symbiotic corals for the maintenance of species diversity. Our findings have implications for the management of these threatened Caribbean corals and the effectiveness of coral reef restoration efforts.

Reserve design for uncertain responses of coral reefs to climate change.

Rising sea temperatures cause mass coral bleaching and threaten reefs worldwide. We show how maps of variations in thermal stress can be used to help manage reefs for climate change. We map proxies of chronic and acute thermal stress and develop evidence-based hypotheses for the future response of corals to each stress regime. We then incorporate spatially realistic predictions of larval connectivity among reefs of the Bahamas and apply novel reserve design algorithms to create reserve networks for a changing climate. We show that scales of larval dispersal are large enough to connect reefs from desirable thermal stress regimes into a reserve network. Critically, we find that reserve designs differ according to the anticipated scope for phenotypic and genetic adaptation in corals, which remains uncertain. Attempts to provide a complete reserve design that hedged against different evolutionary outcomes achieved limited success, which emphasises the importance of considering the scope for adaptation explicitly. Nonetheless, 15% of reserve locations were selected under all evolutionary scenarios, making them a high priority for early designation. Our approach allows new insights into coral holobiont adaptation to be integrated directly into an adaptive approach to management.

Elucidating gene expression adaptation of phylogenetically divergent coral holobionts under heat stress.

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.

Multiple light scattering and absorption in reef-building corals.

We present an experimental and numerical study of the effects of multiple scattering on the optical properties of reef-building corals. For this, we propose a simplified optical model of the coral and describe in some detail methods for characterizing the coral skeleton and the layer containing the symbiotic algae. The model is used to study the absorption of light by the layer of tissue containing the microalgae by means of Monte Carlo simulations. The results show that, through scattering, the skeleton homogenizes and enhances the light environment in which the symbionts live. We also present results that illustrate the modification of the internal light environment when the corals loose symbionts or pigmentation.

Host pigments: potential facilitators of photosynthesis in coral symbioses.

Reef-building corals occur as a range of colour morphs because of varying types and concentrations of pigments within the host tissues, but little is known about their physiological or ecological significance. Here, we examined whether specific host pigments act as an alternative mechanism for photoacclimation in the coral holobiont. We used the coral Montipora monasteriata (Forskål 1775) as a case study because it occurs in multiple colour morphs (tan, blue, brown, green and red) within varying light-habitat distributions. We demonstrated that two of the non-fluorescent host pigments are responsive to changes in external irradiance, with some host pigments up-regulating in response to elevated irradiance. This appeared to facilitate the retention of antennal chlorophyll by endosymbionts and hence, photosynthetic capacity. Specifically, net P(max) Chl a(-1) correlated strongly with the concentration of an orange-absorbing non-fluorescent pigment (CP-580). This had major implications for the energetics of bleached blue-pigmented (CP-580) colonies that maintained net P(max) cm(-2) by increasing P(max) Chl a(-1). The data suggested that blue morphs can bleach, decreasing their symbiont populations by an order of magnitude without compromising symbiont or coral health.

Seasonal variation modulates coral sensibility to heat-stress and explains annual changes in coral productivity.

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 (Pmax), while Pmax enhancement in the second group was more dependent on Symbiodinium performance (Psym). 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.

The effects of elevated seawater temperatures on Caribbean gorgonian corals and their algal symbionts, Symbiodinium spp.

Global climate change not only leads to elevated seawater temperatures but also to episodic anomalously high or low temperatures lasting for several hours to days. Scleractinian corals are detrimentally affected by thermal fluctuations, which often lead to an uncoupling of their mutualism with Symbiodinium spp. (coral bleaching) and potentially coral death. Consequently, on many Caribbean reefs scleractinian coral cover has plummeted. Conversely, gorgonian corals persist, with their abundance even increasing. How gorgonians react to thermal anomalies has been investigated utilizing limited parameters of either the gorgonian, Symbiodinium or the combined symbiosis (holobiont). We employed a holistic approach to examine the effect of an experimental five-day elevated temperature episode on parameters of the host, symbiont, and the holobiont in Eunicea tourneforti, E. flexuosa and Pseudoplexaura porosa. These gorgonian corals reacted and coped with 32°C seawater temperatures. Neither Symbiodinium genotypes nor densities differed between the ambient 29.5°C and 32°C. Chlorophyll a and c2 per Symbiodinium cell, however, were lower at 32°C leading to a reduction in chlorophyll content in the branches and an associated reduction in estimated absorbance and increase in the chlorophyll a specific absorption coefficient. The adjustments in the photochemical parameters led to changes in photochemical efficiencies, although these too showed that the gorgonians were coping. For example, the maximum excitation pressure, Qm, was significantly lower at 32°C than at 29.5°C. In addition, although per dry weight the amount of protein and lipids were lower at 32°C, the overall energy content in the tissues did not differ between the temperatures. Antioxidant activity either remained the same or increased following exposure to 32°C further reiterating a response that dealt with the stressor. Taken together, the capability of Caribbean gorgonian corals to modify symbiont, host and consequently holobiont parameters may partially explain their persistence on reefs faced with climate change.