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Pigments homologous to the green fluorescent protein (GFP) have been proposed to fine-tune the internal light microclimate of corals, facilitating photoacclimation of photosynthetic coral symbionts (Symbiodiniaceae) to life in different reef habitats and environmental conditions. However, direct measurements of the in vivo light conditions inside the coral tissue supporting this conclusion are lacking. Here, we quantified the intra-tissue spectral light environment of corals expressing GFP-like proteins from widely different light regimes. We focus on: (1) photoconvertible red fluorescent proteins (pcRFPs), thought to enhance photosynthesis in mesophotic habitats via wavelength conversion, and (2) chromoproteins (CPs), which provide photoprotection to the symbionts in shallow water via light absorption. Optical microsensor measurements indicated that both pigment groups strongly alter the coral intra-tissue light environment. Estimates derived from light spectra measured in pcRFP-containing corals showed that fluorescence emission can contribute to >50% of orange-red light available to the photosynthetic symbionts at mesophotic depths. We further show that upregulation of pink CPs in shallow-water corals during bleaching leads to a reduction of orange light by 10–20% compared to low-CP tissue. Thus, screening by CPs has an important role in mitigating the light-enhancing effect of coral tissue scattering and skeletal reflection during bleaching. Our results provide the first experimental quantification of the importance of GFP-like proteins in fine-tuning the light microclimate of corals during photoacclimation.

Climate change-induced global warming threatens the survival of key ecosystems including shallow water coral reefs. Elevated temperatures can disrupt the normal physiological functioning of photosynthetic organisms by altering the fluidity and permeability of chloroplast membranes that is defined and regulated by their lipid composition. Since the habitat-forming reef corals rely on the obligatory symbiosis with dinoflagellates of the family Symbiodiniaceae, their heat stress response can be expected to be strongly influenced by the symbiont's lipid metabolism. However, in contrast to the steady increase in the knowledge of the functioning of coral symbionts at the genomic and transcriptomic level, the understanding of their membrane lipid composition and regulation in response to temperature stress is lagging behind. We have utilised mass spectrometry-based lipidomic analyses to identify the key polar lipids that form the biological membranes of reef coral symbionts, comparing the thermotolerant species Durusdinium trenchii with the thermosensitive taxon Cladocopium C3, both hosted by Acropora valida. Our results indicate that the superior thermotolerance D. trenchii inside the host corals could be achieved through (1) the amount and saturation of sulfoquinovosyldiacylglycerols, in particular through putative photosystem II interactions, (2) the increased digalactosyldiacylglycerol to monogalactosyldiacylglycerol ratio with the potential to stabilise thylakoid membranes and integrated proteins, and (3) the chaperone-like function of lyso-lipids. Thereby, our study provides novel insights into the heat tolerance of coral symbionts, contributing to the understanding of the potential of coral reef ecosystems to respond and adjust to heat stress events that are becoming more frequent due to climate change. Finally, our identification of multiple mechanisms of heat tolerance in Symbiodiniaceae furthers the knowledge of the general stress physiology of photosynthetic organisms.

Summary Coral bleaching, caused by the loss of brownish-colored dinoflagellate photosymbionts from the host tissue of reef-building corals, is a major threat to reef survival. Occasionally, bleached corals become exceptionally colorful rather than white. These colors derive from photoprotective green fluorescent protein (GFP)-like pigments produced by the coral host. There is currently no consensus regarding what causes colorful bleaching events and what the consequences for the corals are. Here, we document that colorful bleaching events are a recurring phenomenon in reef regions around the globe. Our analysis of temperature conditions associated with colorful bleaching events suggests that corals develop extreme coloration within 2 to 3 weeks after exposure to mild or temporary heat stress. We demonstrate that the increase of light fluxes in symbiont-depleted tissue promoted by reflection of the incident light from the coral skeleton induces strong expression of the photoprotective coral host pigments. We describe an optical feedback loop involving both partners of the association, discussing that the mitigation of light stress offered by host pigments could facilitate recolonization of bleached tissue by symbionts. Our data indicate that colorful bleaching has the potential to identify local environmental factors, such as nutrient stress, that can exacerbate the impact of elevated temperatures on corals, to indicate the severity of heat stress experienced by corals and to gauge their post-stress recovery potential. Video Abstract Download : Download video (160MB)

High levels of phytoplankton visible in satellite imagery are correlated with an increased uptake of carbon compounds by corals. This suggests that corals rely less on carbon production by photosynthetic symbionts when other resources are plentiful, and that the changes in the acquisition mode of carbon can be inferred by remote-sensing techniques.

The adaptation of tropical coral communities to the world's hottest sea, the Persian/Arabian Gulf (PAG), has recently been associated with ecological selection acting on a group of coral-associated algal symbionts, the Symbiodinium thermophilum group. Previous studies have shown that considerable genetic diversity exists within the group and that group members found within the PAG are significantly differentiated from those found externally, in the Gulf of Oman and wider waters. However, little is known about this genetic diversity. As an initial step towards understanding whether this diversity could represent niche adapted, selectable populations within the S. thermophilum group that may act as natural sources of stress tolerant associations to Indo-Pacific reefs, we investigate whether the diversity is structured between populations and where the location of the internal-external genetic partition lies. We use regions of the nuclear ribosomal DNA (ITS1-5.8S-ITS2) and chloroplastic psbA gene (non-coding region) from > 100 S. thermophilum group-harbouring Porites spp. (P. lobata, P. lutea, and P. harrisoni) sampled across steep temperature and salinity gradients to conduct analyses of variance and create maximum parsimony networks to assess genetic structure and (dis)similarity within and between populations of S. thermophilum found within the PAG and externally in the Gulf of Oman. Our analyses resolve a sharp genetic boundary between Symbiodinium populations in the western Strait of Hormuz and identify significant genetic structure between populations with as little as 20 km between them demonstrating that differentiation between populations is likely due to factors other than limited connectivity. Further, we hypothesize that genotypes identified outside of the PAG in the Gulf of Oman existing in near-oceanic salinities, yet thermally challenging waters, putatively represent candidates for stress-tolerant symbionts that could act as natural seed populations of stress tolerant genotypes to the wider indo-Pacific.

The binary designation Symbiodinium thermophilum was invalid due to the absence of an illustration as required by Article 44.2 of the ICN. Herein, it is validated. This species is the most common symbiont in reef corals in the southern Persian/Arabian Gulf, the world's hottest body of water sustaining reef coral growth.

In response to high salinity, algal endosymbionts of corals produce floridoside, an osmolyte with antioxidant potential., The endosymbiosis between Symbiodinium dinoflagellates and stony corals provides the foundation of coral reef ecosystems. The survival of these ecosystems is under threat at a global scale, and better knowledge is needed to conceive strategies for mitigating future reef loss. Environmental disturbance imposing temperature, salinity, and nutrient stress can lead to the loss of the Symbiodinium partner, causing so-called coral bleaching. Some of the most thermotolerant coral-Symbiodinium associations occur in the Persian/Arabian Gulf and the Red Sea, which also represent the most saline coral habitats. We studied whether Symbiodinium alter their metabolite content in response to high-salinity environments. We found that Symbiodinium cells exposed to high salinity produced high levels of the osmolyte 2-O-glycerol-α-d-galactopyranoside (floridoside), both in vitro and in their coral host animals, thereby increasing their capacity and, putatively, the capacity of the holobiont to cope with the effects of osmotic stress in extreme environments. Given that floridoside has been previously shown to also act as an antioxidant, this osmolyte may serve a dual function: first, to serve as a compatible organic osmolyte accumulated by Symbiodinium in response to elevated salinities and, second, to counter reactive oxygen species produced as a consequence of potential salinity and heat stress.

Anthropogenic nutrient enrichment is often associated with coral reef decline. Consequently, there is a large consent that increased nutrient influxes in reef waters have negative longterm consequences for corals. However, the mechanisms by which dissolved inorganic nutrients can disturb corals and their symbiotic algae are subject to controversial debate. Herein, we discuss recent studies that demonstrate how nutrient enrichment affects the heat and light stress tolerance of corals and their bleaching susceptibility. We integrate direct and indirect effects of nutrient enrichment on corals in a model that explains why healthy coral reefs can exist over a rather broad range of natural nutrient environments at the lower end of the concentration scale and that anthropogenic nutrient enrichment can disturb the finely balanced processes via multiple pathways. We conceptualise that corals can suffer from secondary negative nutrient effects due to the alteration of their natural nutrient environment by increased phytoplankton loads. In this context, we suggest that phytoplankton represents a likely vector that can translate nutrients effects, induced for instance by coastal run-off, into nutrient stress on coral reefs in considerable distance to the site of primary nutrient enrichment. The presented synthesis of the literature suggests that the effects of nutrient enrichment and eutrophication beyond certain thresholds are negative for the physiological performance of the coral individual and for ecosystem functioning. Hence, the immediate implementation of knowledge-based nutrient management strategies is crucial for coral reef survival.

Fatal infestations of land-based Acropora cultures with so-called Acropora-eating flatworms (AEFWs) are a global phenomenon. We evaluate the hypothesis that AEFWs represent a risk to coral reefs by studying the biology and the invasive potential of an AEFW strain from the UK. Molecular analyses identified this strain as Amakusaplana acroporae, a new species described from two US aquaria and one natural location in Australia. Our molecular data together with life history strategies described here suggest that this species accounts for most reported cases of AEFW infestations. We show that local parasitic activity impairs the light-acclimation capacity of the whole host colony. A. acroporae acquires excellent camouflage by harbouring photosynthetically competent, host-derived zooxanthellae and pigments of the green-fluorescent protein family. It shows a preference for Acropora valida but accepts a broad host range. Parasite survival in isolation (5–7 d) potentially allows for an invasion when introduced as non-native species in coral reefs.

International audience; Phosphorus (P), an essential structural and functional component of all living organisms, is considered to be the ultimate limiting nutrient in marine ecosystems. To optimize its acquisition, marine species such as protozoa, sponges, foraminifera, clams, and reef corals, among others, have entered symbiotic relationships with algae, which recycle waste products of the animal host and transform dissolved inorganic nutrients into organic molecules, making them bioavailable to their host. Such associations provide a competitive edge in an environment where ambient nutrient availability is low. The aim of this review is to summarize the current knowledge on the P sources available to reef organisms with algal symbionts, to discuss the means by which P is taken up and stored within the symbiosis, and to assess the effects of eutrophication-induced phosphate enrichment on the algal and host physiology. Finally, we give an overview of knowledge gaps and open questions that should be addressed to better understand the role of phosphorus in reef symbioses functioning. © 2016 by the Ecological Society of America.

Mass coral bleaching, resulting from the breakdown of coral-algal symbiosis has been identified as the most severe threat to coral reef survival on a global scale. Regionally, nutrient enrichment of reef waters is often associated with a significant loss of coral cover and diversity. Recently, increased dissolved inorganic nitrogen concentrations have been linked to a reduction of the temperature threshold of coral bleaching, a phenomenon for which no mechanistic explanation is available. Here we show that increased levels of dissolved inorganic nitrogen in combination with limited phosphate concentrations result in an increased susceptibility of corals to temperature-and light-induced bleaching. Mass spectrometric analyses of the algal lipidome revealed a marked accumulation of sulpholipids under these conditions. Together with increased phosphatase activities, this change indicates that the imbalanced supply of dissolved inorganic nitrogen results in phosphate starvation of the symbiotic algae. Based on these findings we introduce a conceptual model that links unfavourable ratios of dissolved inorganic nutrients in the water column with established mechanisms of coral bleaching. Notably, this model improves the understanding of the detrimental effects of coastal nutrient enrichment on coral reefs, which is urgently required to support knowledge-based management strategies to mitigate the effects of climate change. © 2013 Macmillan Publishers Limited. All rights reserved.

Aquarium systems allow technically sophisticated experiments that promise new opportunities to answer urgent questions about reef coral biology, for instance assessing the responses to decreasing environmental pH and/or increased temperatures. Over recent years, long-term culture and (predominantly asexual) propagation of corals has become possible in such systems. At present however, only limited data are available that clarify whether or not responses of the coral holobiont are dominated by the acclimatization to life in captivity or continue to reflect, for example, taxonomic differences seen in nature. We studied the diversity of the symbiotic algae in corals and sea anemones after long-term aquaculture by analysis of their small subunit (SSU) ribosomal DNA gene. A field sample ofAcropora clathratafrom the Arabian Gulf which was used as a control contained clade C zooxanthellae. The aquarium corals also harboured clade C symbionts, but sequencing of the SSU DNA suggested that the analysed animals host different subclades. A prevalence of clade C is also found among corals from the Indo-Pacific region, the origin of most of the aquarium samples. An individual of the temperate sea anemoneAnemonia sulcata (viridis)contained clade A symbionts, similar to those found in nature, even after nearly 10 years of co-culture with sea anemones(Entacmaea quadricolor)and corals hosting clade C symbionts. The results indicate that the specific host–symbiont association occurring in nature appears to persist over >2 years timescales in captivity, with no mixing of symbionts between hosts maintained in the same aquarium or apparent selection of stress-tolerant symbiont strains such as clade D.

Coral reefs are in rapid decline on a global scale due to human activities and a changing climate. Shallow water reefs depend on the obligatory symbiosis between the habitat forming coral host and its algal symbiont from the genus Symbiodinium (zooxanthellae). This association is highly sensitive to thermal perturbations and temperatures as little as 1°C above the average summer maxima can cause the breakdown of this symbiosis, termed coral bleaching. Predicting the capacity of corals to survive the expected increase in seawater temperatures depends strongly on our understanding of the thermal tolerance of the symbiotic algae. Here we use molecular phylogenetic analysis of four genetic markers to describe Symbiodinium thermophilum, sp. nov. from the Persian/Arabian Gulf, a thermally tolerant coral symbiont. Phylogenetic inference using the non-coding region of the chloroplast psbA gene resolves S. thermophilum as a monophyletic lineage with large genetic distances from any other ITS2 C3 type found outside the Gulf. Through the characterisation of Symbiodinium associations of 6 species (5 genera) of Gulf corals, we demonstrate that S. thermophilum is the prevalent symbiont all year round in the world's hottest sea, the southern Persian/Arabian Gulf.

Predicted increases in seawater temperatures accelerate coral reef decline due to mortality by heat-driven coral bleaching. Alteration of the natural nutrient environment of reef corals reduces tolerance of corals to heat and light stress and thus will exacerbate impacts of global warming on reefs. Still, many reefs demonstrate remarkable regeneration from past stress events. This paper investigates the effects of sea surface temperature (SST) and water column productivity on recovery of coral reefs. In 71 Indo-Pacific sites, coral cover changes over the past 1-3 decades correlated negative-exponentially with mean SST, chlorophyll a, and SST rise. At six monitoring sites (Persian/Arabian Gulf, Red Sea, northern and southern Galápagos, Easter Island, Panama), over half of all corals were

The genomic framework that enables corals to adjust to unfavourable conditions is crucial for coral reef survival in a rapidly changing climate. We have explored the striking intraspecific variability in the expression of coral pigments from the green fluorescent protein (GFP) family to elucidate the genomic basis for the plasticity of stress responses among reef corals. We show that multicopy genes can greatly increase the dynamic range over which corals can modulate transcript levels in response to the light environment. Using the red fluorescent protein amilFP597 in the coral Acropora millepora as a model, we demonstrate that its expression increases with light intensity, but both the minimal and maximal gene transcript levels vary markedly among colour morphs. The pigment concentration in the tissue of different morphs is strongly correlated with the number of gene copies with a particular promoter type. These findings indicate that colour polymorphism in reef corals can be caused by the environmentally regulated expression of multicopy genes. High‐level expression of amilFP597 is correlated with reduced photodamage of zooxanthellae under acute light stress, supporting a photoprotective function of this pigment. The cluster of light‐regulated pigment genes can enable corals to invest either in expensive high‐level pigmentation, offering benefits under light stress, or to rely on low tissue pigment concentrations and use the conserved resources for other purposes, which is preferable in less light‐exposed environments. The genomic framework described here allows corals to pursue different strategies to succeed in habitats with highly variable light stress levels. In summary, our results suggest that the intraspecific plasticity of reef corals’ stress responses is larger than previously thought.

The symbiotic association of corals and unicellular algae of the genus Symbiodinium in the southern Persian/Arabian Gulf (PAG) display an exceptional heat tolerance, enduring summer peak temperatures of up to 36?°C. As yet, it is not clear whether this resilience is related to the presence of specific symbiont types that are exclusively found in this region. Therefore, we used molecular markers to identify the symbiotic algae of three Porites species along >1000?km of coastline in the PAG and the Gulf of Oman and found that a recently described species, Symbiodinium thermophilum, is integral to coral survival in the southern PAG, the world’s hottest sea. Despite the geographic isolation of the PAG, we discovered that representatives of the S. thermophilum group can also be found in the adjacent Gulf of Oman providing a potential source of thermotolerant symbionts that might facilitate the adaptation of Indian Ocean populations to the higher water temperatures expected for the future. However, corals from the PAG associated with S. thermophilum show strong local adaptation not only to high temperatures but also to the exceptionally high salinity of their habitat. We show that their superior heat tolerance can be lost when these corals are exposed to reduced salinity levels common for oceanic environments elsewhere. Consequently, the salinity prevailing in most reefs outside the PAG might represent a distribution barrier for extreme temperature-tolerant coral/Symbiodinium associations from the PAG.

Corals in the Arabian/Persian Gulf endure summer temperatures of up to 36 °C, making them ideal subjects to study the mechanisms underlying thermal tolerance. Unexpectedly, we found the “generalist” Symbiodinium clade C3 to be the prevalent symbiont among seven coral species from Abu Dhabi (UAE) waters. Moreover, C3 represented the only dominant symbiont type in Porites spp. from this region. The “thermotolerant” symbionts D1a and C15 were not encountered, indicating that the association with these symbionts cannot be the sole reason for the heat tolerance of Gulf corals. The association of Porites lobata with specific symbiont types (C3 vs. C15) in samples from habitats with very different temperature regimes (Abu Dhabi vs. Fiji) remained unaffected by laboratory culture. During temperature stress experiments specimens from both locations strongly downregulated green fluorescent protein (GFP)-like pigments. However, the Abu Dhabi samples were less prone to bleaching and showed lower mortality.

The phenomenon of coral fluorescence in mesophotic reefs, although well described for shallow waters, remains largely unstudied. We found that representatives of many scleractinian species are brightly fluorescent at depths of 50–60 m at the Interuniversity Institute for Marine Sciences (IUI) reef in Eilat, Israel. Some of these fluorescent species have distribution maxima at mesophotic depths (40–100 m). Several individuals from these depths displayed yellow or orange-red fluorescence, the latter being essentially absent in corals from the shallowest parts of this reef. We demonstrate experimentally that in some cases the production of fluorescent pigments is independent of the exposure to light; while in others, the fluorescence signature is altered or lost when the animals are kept in darkness. Furthermore, we show that green-to-red photoconversion of fluorescent pigments mediated by short-wavelength light can occur also at depths where ultraviolet wavelengths are absent from the underwater light field. Intraspecific colour polymorphisms regarding the colour of the tissue fluorescence, common among shallow water corals, were also observed for mesophotic species. Our results suggest that fluorescent pigments in mesophotic reefs fulfil a distinct biological function and offer promising application potential for coral-reef monitoring and biomedical imaging., 論文

The competition for space among fluorescent and nonfluorescent Anemonia species was monitored in the Mediterranean Sea in order to see whether the fluorescent species A. sulcata var. smaragdina was a better competitor in shallow water habitats. Over a period of 11 years, A. sulcata var. smaragdina convincingly out competed the nonfluorescent A. rustica. We thereby found support for the notion that the GFP-like pigments may increase competitive ability in anthozoans.

Homologs of the green fluorescent protein (GFP) are a prevalent group of host pigments responsible for the green, red and purple-blue colours of many reef-building corals. They have been suggested to contribute to the striking coloration changes of different corals species in response to wounding and infestation with epibionts/parasites. In order to elucidate the physiological processes underlying the potentially disease-related colour changes, we have analysed spatial and temporal expression patterns of GFP-like proteins and other biomarkers in corals from the Red Sea, the Arabian/Persian Gulf and Fiji both in their natural habitat and under specific laboratory conditions. The expression of distinct GFP-like proteins and the growth marker proliferating cell nuclear antigen was upregulated in growing branch tips and margins of healthy coral colonies as well as in disturbed colony parts. Furthermore, phenoloxidase activity increased in these proliferating tissues. It is thus demonstrated that locally accelerated growth is part of the innate immune response and repair mechanisms in reef-building corals and, moreover, these processes can be detected utilizing the excellent biomarker properties of GFP-like proteins. Finally, the results of this work suggest an additional vulnerability of corals in predicted future scenarios of increased ocean acidification, warming and eutrophication that are anticipated to reduce coral growth capacity.