Mitigating the ecological collapse of coral reef ecosystems: Effective strategies to preserve coral reef ecosystems: Effective strategies to preserve coral reef ecosystems.

Global warming is decimating coral reefs. We need to implement mitigation and restoration strategies now to prevent coral reefs from disappearing altogether.

Nutrient depletion and heat stress impair the assimilation of nitrogen compounds in a scleractinian coral.

Concentrations of dissolved nitrogen in seawater can affect the resilience of the cnidarian-dinoflagellate symbiosis to climate change-induced bleaching. However, it is not yet known how the assimilation and translocation of the various nitrogen forms change during heat stress, nor how the symbiosis responds to nutrient depletion, which may occur due to increasing water stratification. Here, the tropical scleractinian coral Stylophora pistillata, in symbiosis with dinoflagellates of the genus Symbiodinium, was grown at different temperatures (26°C, 30°C and 34°C), before being placed in nutrient-replete or -depleted seawater for 24 h. The corals were then incubated with 13C-labelled sodium bicarbonate and different 15N-labelled nitrogen forms (ammonium, urea and dissolved free amino acids) to determine their assimilation rates. We found that nutrient depletion inhibited the assimilation of all nitrogen sources studied and that heat stress reduced the assimilation of ammonium and dissolved free amino acids. However, the host assimilated over 3-fold more urea at 30°C relative to 26°C. Overall, both moderate heat stress (30°C) and nutrient depletion individually decreased the total nitrogen assimilated by the symbiont by 66%, and combined, they decreased assimilation by 79%. This led to the symbiotic algae becoming nitrogen starved, with the C:N ratio increasing by over 3-fold at 34°C, potentially exacerbating the impacts of coral bleaching.

First report of black leaf streak disease in bananas caused by Pseudocercospora fijiensis on Mauritius island.

Pseudocercospora fijiensis, the causal agent of the black leaf streak disease of bananas (plants in the genus Musa) (BLSD), is considered to be the major economic threat to export-banana cultivation (de Bellaire, Fouré, Abadie, & Carlier, 2010). The disease has a worldwide distribution throughout the humid tropical regions and has been previously reported in the Southwestndian Ocean (SWIO) area: in 1993 in Mayotte and Comoros islands (DR Jones & Mourichon, 1993), in 2000 in Madagascar (Jones, 2003; Rivas, Zapater, Abadie, & Carlier, 2004) and in 2018 in Reunion Island (Rieux et al., 2019). In Mauritius, the presence of Pseudocercospora fijiensis was suspected in 1996 (Soomary & Benimadhu, 1998) but has never been confirmed, as symptoms could have been confounded with Pseudocercospora musae or Pseudocercospora eumusae, two causal agents of others leaf spot diseases of banana which were previously described in Mauritius in 1959 (Orieux & Felix, 1968) and 2000 (Carlier, Zapater, Lapeyre, Jones, & Mourichon, 2000), respectively. In March 2022, typical BLSD symptoms were observed at relatively low prevalence in a Cavendish crop located in the "Balance John" area (site S1 on Fig. S1-A) of Mauritius island. Typical early symptoms (stages 2) were 1- to 4-mm long brown streaks at the abaxial leaf surface, and typical older streaks (stages 3 and 4) were also observed (Fig. S1-B). These symptoms were mixed with symptoms of ELSD caused by P. eumusae. Since both species cannot be clearly distinguished only on the description of symptoms, conidial sporulation on stages 2 was checked in the laboratory (Ngando et al., 2015) since P. eumusae does not produce conidia on these young stages. In April 2022, banana leaves bearing symptoms of leaf spot diseases were collected in 7 different sites (Fig. S1-A). All leaf fragments were sent to the CIRAD laboratories where molecular diagnosis was performed following the protocol developed by Arzanlou et al. (2007). In brief, genomic DNA was extracted from ground leaf fragments displaying symptoms using the DNeasy® Plant Mini Kit (Qiagen®, Courtaboeuf, France). At each site, a total of 6 lesions cut from 6 different leaves were pooled. The DNA extracts were added as templates for real-time PCR assay designed to specifically detect the presence of P. fijiensis, P. musae and P. eumusae using MFbf/MFbrtaq/MFbp, MEbf/MEbrtaq/FMep and MMbf/Mmbrtaq/FMep primers and probes, respectively (Arzanlou et al., 2007). Both positive and negative controls were included in the assay and every sample reaction was duplicated. P. fijiensis was detected from 2 out of 7 sites (S2 and S7, see Fig.S2-B). P. eumusae was detected at all sites while P. musae was found in one site only (S6). Interestingly, our results also showed coinfection by P. fijiensis - P. eumusae & P. musae - P. eumusae on several sites. The presence of P. fijiensis was further confirmed by several investigations performed on conidia isolated from S2 samples including i) morphological observations of conidia displaying P. fijiensis type description (Pérez-Vicente, Carreel, Roussel, Carlier, & Abadie (2021), Fig. S2-A), ii) DNA sequencing of 16S ribosomal gene with ITS1 & ITS4 primers (GenBank accessions Nos. OR515818-OR515810) with BLAST results displaying percentages of identity > 99.70% with type strains and iii) Koch's postulates were fulfilled by artificial inoculation of detached leaf pieces as described in Pérez-Vicente, Carreel, Roussel, Carlier, & Abadie (2021) (Fig. S2-D). In brief, for the artificial inoculation, symptoms obtained after inoculation of both a strain isolated in Mauritius (S2-MAU) and a positive control (T+) were compared and shown to be typical of P. fijiensis species for the 3 replicates. To the best of our knowledge, this is the first official report of P. fijiensis and BLSD in Mauritius Island. This revelation holds significant importance for both the agricultural and scientific communities, shedding light on the potential spread and impact of this devastating pathogen in previously unaffected regions. From a global perspective, this discovery underscores the interconnectedness of agricultural ecosystems and the need for vigilance in monitoring and responding to emerging plant diseases in an increasingly interconnected world (Vega et al. 2022). Future investigations will be required to monitor the spread of BLSD on the island, describe the genetic structure of populations and identify routes of invasion at the SWOI scale.

Species-Specific Response of Corals to Imbalanced Ratios of Inorganic Nutrients.

Dissolved inorganic phosphorus (DIP) is a limiting nutrient in the physiology of scleractinian corals. Anthropogenic addition of dissolved inorganic nitrogen (DIN) to coastal reefs increases the seawater DIN:DIP ratio and further increases P limitation, which is detrimental to coral health. The effects of imbalanced DIN:DIP ratios on coral physiology require further investigation in coral species other than the most studied branching corals. Here we investigated the nutrient uptake rates, elemental tissue composition and physiology of a foliose stony coral, Turbinaria reniformis, and a soft coral, Sarcophyton glaucum, exposed to four different DIN: DIP ratios (0.5:0.2, 0.5:1, 3:0.2, 3:1). The results show that T. reniformis had high uptake rates of DIN and DIP, proportional to the seawater nutrient concentrations. DIN enrichment alone led to an increase in tissue N content, shifting the tissue N:P ratio towards P limitation. However, S. glaucum had 5 times lower uptake rates and only took up DIN when the seawater was simultaneously enriched with DIP. This double uptake of N and P did not alter tissue stoichiometry. This study allows us to better understand the susceptibility of corals to changes in the DIN:DIP ratio and predict how coral species will respond under eutrophic conditions in the reef.

The Effect of Thermal Stress on the Physiology and Bacterial Communities of Two Key Mediterranean Gorgonians.

Gorgonians are important habitat-providing species in the Mediterranean Sea, but their populations are declining due to microbial diseases and repeated mass mortality events caused by summer heat waves. Elevated seawater temperatures may impact the stress tolerance and disease resistance of gorgonians and lead to disturbances in their microbiota. However, our knowledge of the biological response of the gorgonian holobiont (i.e., the host and its microbiota) to thermal stress remains limited. Here, we investigated how the holobiont of two gorgonian species (Paramuricea clavata and Eunicella cavolini) are affected throughout a 7-week thermal stress event by following both the corals' physiology and the composition of their bacterial communities. We found that P. clavata was more sensitive to elevated seawater temperatures than E. cavolini, showing a greater loss in energy reserves, reduced feeding ability, and partial mortality. This lower thermotolerance may be linked to the ∼20× lower antioxidant defense capacity in P. clavata compared with E. cavolini. In the first 4 weeks of thermal stress, we also observed minor shifts in the microbiota of both species, suggesting that the microbiota likely plays a limited role in thermal acclimation of the holobiont. However, major stochastic changes occurred later on in some colonies, which were of a transient nature in E. cavolini, but were linked to partial colony mortality in P. clavata. Overall, our results show significant, but differential, effects of thermal stress on the holobionts of both E. cavolini and P. clavata and predict potentially severe impacts on gorgonian populations under future climate scenarios. IMPORTANCE In the Mediterranean Sea, the tree-shaped gorgonian corals form large forests that provide a place to live for many species. Because of this important ecological role, it is crucial to understand how common habitat-forming gorgonians, like Eunicella cavolini and Paramuricea clavata, are affected by high seawater temperatures that are expected in the future due to climate change. We found that both species lost biomass, but P. clavata was more affected, being also unable to feed and showing signs of mortality. The microbiota of both gorgonians also changed substantively under high temperatures. Although this could be linked to partial colony mortality in P. clavata, the changes were temporary in E. cavolini. The overall higher resistance of E. cavolini may be related to its much higher antioxidant defense levels than P. clavata. Climate change may thus have severe impacts on gorgonian populations and the habitats they provide.

Desert dust deposition supplies essential bioelements to Red Sea corals.

Climate change-related increase in seawater temperature has become a leading cause of coral bleaching and mortality. However, corals from the northern Red Sea show high thermal tolerance and no recorded massive bleaching event. This specific region is frequently subjected to intense dust storms, coming from the surrounding arid deserts, which are expected to increase in frequency and intensity in the future. The aerial dust deposition supplies essential bioelements to the water column. Here, we investigated the effect of dust deposition on the physiology of a Red Sea coral, Stylophora pistillata. We measured the modifications in coral and Symbiodiniaceae metallome (cellular metal content), as well as the changes in photosynthesis and oxidative stress status of colonies exposed during few weeks to dust deposition. Our results show that 1 mg L-1 of dust supplied nanomolar amounts of nitrate and other essential bioelements, such as iron, manganese, zinc and copper, rapidly assimilated by the symbionts. At 25°C, metal bioaccumulation enhanced the chlorophyll concentration and photosynthesis of dust-exposed corals compared to control corals. These results suggest that primary production was limited by metal availability in seawater. A 5°C increase in seawater temperature enhanced iron assimilation in both control and dust-enriched corals. Temperature rise increased the photosynthesis of control corals only, dust-exposed ones having already reached maximal photosynthesis rates at 25°C. Finally, we observed a combined effect of temperature and bioelement concentration on the assimilation of molybdenum, cadmium, manganese and copper, which were in higher concentrations in symbionts of dust-exposed corals maintained at 30°C. All together these observations highlight the importance of dust deposition in the supply of essential bioelements, such as iron, to corals and its role in sustaining coral productivity in Red Sea reefs.

CARMN-NOTCH2 fusion transcript drives high NOTCH2 expression in glomus tumors of the upper digestive tract.

Glomus tumors (GTs) are perivascular tumors mostly occurring in the distal extremities. Rare cases arise in the digestive tract and may be misdiagnosed with neuroendocrine or gastrointestinal stromal tumors. We aimed to specify the features of GT of the upper digestive tract. Clinical, histological, phenotypic, and molecular features of 16 digestive GTs were analyzed, of whom two underwent whole exome and RNA sequencing to search for gene alterations. RNA-sequencing disclosed a t(1:5)(p13;q32) translocation, which resulted in the fusion of CARMN and NOTCH2 in two GTs. The fusion gene encoded a protein sequence corresponding to the NOTCH2 intracellular domain that functions as transcription factor. These finding was supported by high expression of genes targeted by NOTCH. The CARMN-NOTCH2 translocation was detected in 14 out of 16 (88%) GTs of the upper digestive tract; but in only in two out of six cutaneous GTs (33%). Most digestive GT arose from the stomach (n = 13), and the others from duodenal (2) or oesophagous (1). Nuclear expression of NOTCH2 was detected in the 14 cases containing the fusion transcripts. The CARMN-NOTCH2 fusion transcript may contribute to activation of the NOTCH2 pathway in GT and drive tumor development. The high frequency of this translocation in GT of the upper digestive track suggest that detection of nuclear NOTCH2 expression may be useful diagnostic biomarker of these tumors.

Symbiont regulation in Stylophora pistillata during cold stress: an acclimation mechanism against oxidative stress and severe bleaching.

Widespread coral bleaching and mortality, leading to coral reef decline, have been mainly associated with climate-change-driven increases in sea surface temperature. However, bleaching and mortality events have also been related to decreases in sea surface temperature, with cold stress events (e.g. La Niña events) being expected to increase in frequency or intensity as a result of a changing climate. Cold stress creates physiological symptoms in symbiotic reef-building corals similar to those observed when they are heat stressed, and the biochemical mechanisms underpinning cold stress in corals have been suggested to be related to an oxidative stress condition. However, up to now, this hypothesis had not been tested. This study assessed how short and long cold excursions in seawater temperature affect the physiology and biochemical processes related to oxidative stress in the reef-building coral Stylophora pistillata We provide, for the first time, direct evidence that the mechanisms underpinning cold stress and bleaching are related to the production of reactive oxygen species, and that rapid expulsion of a significant proportion of the symbiont population by the host during cooling conditions is an acclimation mechanism to avoid oxidative stress and, ultimately, severe bleaching. Furthermore, this study is one of the first to show that upwelling conditions (short-term cold stress+nutrient enrichment) can provoke a more severe oxidative stress condition in corals than cold stress alone.

Diazotrophic community and associated dinitrogen fixation within the temperate coral Oculina patagonica.

Dinitrogen (N2 ) fixing bacteria (diazotrophs) are an important source of new nitrogen in oligotrophic environments and represent stable members of the microbiome in tropical corals, while information on corals from temperate oligotrophic regions is lacking. Therefore, this study provides new insights into the diversity and activity of diazotrophs associated with the temperate coral Oculina patagonica from the Mediterranean Sea by combining metabarcoding sequencing of amplicons of both the 16S rRNA and nifH genes and 15 N2 stable isotope tracer analysis to assess diazotroph-derived nitrogen (DDN) assimilation by the coral. Results show that the diazotrophic community of O. patagonica is dominated by autotrophic bacteria (i.e. Cyanobacteria and Chlorobia). The majority of DDN was assimilated into the tissue and skeletal matrix, and DDN assimilation significantly increased in bleached corals. Thus, diazotrophs may constitute an additional nitrogen source for the coral host, when nutrient exchange with Symbiodinium is disrupted (e.g. bleaching) and external food supply is limited (e.g. oligotrophic summer season). Furthermore, we hypothesize that DDN can facilitate the fast proliferation of endolithic algae, which provide an alternative carbon source for bleached O. patagonica. Overall, O. patagonica could serve as a good model for investigating the importance of diazotrophs in coral recovery from bleaching.

Coral bleaching is linked to the capacity of the animal host to supply essential metals to the symbionts.

Massive coral bleaching events result in extensive coral loss throughout the world. These events are mainly caused by seawater warming, but are exacerbated by the subsequent decrease in nutrient availability in surface waters. It has therefore been shown that nitrogen, phosphorus or iron limitation contribute to the underlying conditions by which thermal stress induces coral bleaching. Generally, information on the trophic ecology of trace elements (micronutrients) in corals, and on how they modulate the coral response to thermal stress is lacking. Here, we demonstrate for the first time that heterotrophic feeding (i.e. the capture of zooplankton prey by the coral host) and thermal stress induce significant changes in micro element concentrations and isotopic signatures of the scleractinian coral Stylophora pistillata. The results obtained first reveal that coral symbionts are the major sink for the heterotrophically acquired micronutrients and accumulate manganese, magnesium and iron from the food. These metals are involved in photosynthesis and antioxidant protection. In addition, we show that fed corals can maintain high micronutrient concentrations in the host tissue during thermal stress and do not bleach, whereas unfed corals experience a significant decrease in copper, zinc, boron, calcium and magnesium in the host tissue and bleach. In addition, the significant increase in δ65 Cu and δ66 Zn signature of symbionts and host tissue at high temperature suggests that these isotopic compositions are good proxy for stress in corals. Overall, present findings highlight a new way in which coral heterotrophy and micronutrient availability contribute to coral resistance to global warming and bleaching.

Seasonal Stability in the Microbiomes of Temperate Gorgonians and the Red Coral Corallium rubrum Across the Mediterranean Sea.

Populations of key benthic habitat-forming octocoral species have declined significantly in the Mediterranean Sea due to mass mortality events caused by microbial disease outbreaks linked to high summer seawater temperatures. Recently, we showed that the microbial communities of these octocorals are relatively structured; however, our knowledge on the seasonal dynamics of these microbiomes is still limited. To investigate their seasonal stability, we collected four soft gorgonian species (Eunicella singularis, Eunicella cavolini, Eunicella verrucosa and Leptogorgia sarmentosa) and the precious red coral (Corallium rubrum) from two coastal locations with different terrestrial impact levels in the Mediterranean Sea, and used next-generation amplicon sequencing of the 16S rRNA gene. The microbiomes of all soft gorgonian species were dominated by the same 'core microbiome' bacteria belonging to the Endozoicomonas and the Cellvibrionales clade BD1-7, whereas the red coral microbiome was primarily composed of 'core' Spirochaetes, Oceanospirillales ME2 and Parcubacteria. The associations with these bacterial taxa were relatively consistent over time at each location for each octocoral species. However, differences in microbiome composition and seasonal dynamics were observed between locations and could primarily be attributed to locally variant bacteria. Overall, our data provide further evidence of the intricate symbiotic relationships that exist between Mediterranean octocorals and their associated microbes, which are ancient and highly conserved over both space and time, and suggest regulation of the microbiome composition by the host, depending on local conditions.

Computing the carbonate chemistry of the coral calcifying medium and its response to ocean acidification.

Critical to determining vulnerability or resilience of reef corals to Ocean Acidification (OA) is a clearer understanding of the extent to which corals can control carbonate chemistry in their Extracellular Calcifying Medium (ECM) where the CaCO3 skeleton is produced. Here, we employ a mathematical framework to calculate ECM aragonite saturation state (Ωarag.(ECM)) and carbonate system ion concentration using measurements of calcification rate, seawater characteristics (temperature, salinity and pH) and ECM pH (pH(ECM)). Our calculations of ECM carbonate chemistry at current-day seawater pH, indicate that Ωarag.(ECM) ranges from ∼10 to 38 (mean 20.41), i.e. about 5 to 6-fold higher than seawater. Accordingly, Dissolved Inorganic Carbon (DIC) and Total Alkalinity (TA) were calculated to be around 3 times higher in the ECM than in seawater. We also assessed the effects of acidification on ECM chemical properties of the coral Stylophora pistillata. At reduced seawater pH our calculations indicate that Ωarag.(ECM) remains almost constant. DIC(ECM) and TA(ECM) gradually increase as seawater pH declines, reaching values about 5 to 6-fold higher than in seawater, respectively for DIC and TA. We propose that these ECM characteristics buffer the effect of acidification and explain why certain corals continue to produce CaCO3 even when seawater chemistry is less favourable.

Comparative Assessment of Mediterranean Gorgonian-Associated Microbial Communities Reveals Conserved Core and Locally Variant Bacteria.

Gorgonians are key habitat-forming species of Mediterranean benthic communities, but their populations have suffered from mass mortality events linked to high summer seawater temperatures and microbial disease. However, our knowledge on the diversity, dynamics and function of gorgonian-associated microbial communities is limited. Here, we analysed the spatial variability of the microbiomes of five sympatric gorgonian species (Eunicella singularis, Eunicella cavolini, Eunicella verrucosa, Leptogorgia sarmentosa and Paramuricea clavata), collected from the Mediterranean Sea over a scale of ∼1100 km, using next-generation amplicon sequencing of the 16S rRNA gene. The microbiomes of all gorgonian species were generally dominated by members of the genus Endozoicomonas, which were at very low abundance in the surrounding seawater. Although the composition of the core microbiome (operational taxonomic units consistently present in a species) was found to be unique for each host species, significant overlap was observed. These spatially consistent associations between gorgonians and their core bacteria suggest intricate symbiotic relationships and regulation of the microbiome composition by the host. At the same time, local variations in microbiome composition were observed. Functional predictive profiling indicated that these differences could be attributed to seawater pollution. Taken together, our data indicate that gorgonian-associated microbiomes are composed of spatially conserved bacteria (core microbiome members) and locally variant members, and that local pollution may influence these local associations, potentially impacting gorgonian health.

[Focus on the Immunoscore and its potential clinical implications]. / Mise au point sur l'Immunoscore et ses potentielles implications cliniques.

The role of the immune response at the tumor site is now recognized as crucial in the clinical course of patients with cancer. The importance of the immune cell type, their functional orientation, their density and location within the tumor's regions (tumor/invasion margin) has recently been shown and were grouped together under the term "immune contexture". A strong infiltration by cytotoxic and memory T cells in a Th1-polarized tumor microenvironment appears to have a major prognosis impact. A test called Immunoscore taking into account these various parameters has been suggested to measure in a simple, reproducible and robust manner the intra- and peritumoral immune response. The prognostic value of Immunoscore has recently been validated in colon cancers by a large international retrospective study under the aegis of the Society for Immunotherapy of Cancer (SITC). The Immunoscore could have several potential clinical applications such as prognostic as well as theranostic.

[Immune response and digestive cancers: Prognostic and therapeutic implications]. / Réponse immune et cancers digestifs : implications pronostiques et thérapeutiques.

The aim of this article is to emphasize the impact of the immune response in digestive cancers, especially from colorectal (CRC) origin. In this setting, an adaptive lymphocytic infiltrate underlines the prognostic impact of the immune response, because it is associated to a favorable outcome. The next challenge will be to validate, in a prospective therapeutic trial, the integration of the immune response as decisional parameter for adjuvant therapy. The immune response is also a predictive parameter in microsatellite instable metastatic CRC, characterized by an adaptive lymphocytic infiltrate, leading to a very high response rate to immune therapies. However, prognostic and predictive biomarkers still need to be optimized in order to better select patients. These data are also valuable for digestive non-colorectal cancers, which are briefly analyzed. The methodology for the assessment of these prognostic and predictive biomarkers, which represents an important issue in precision medicine, is also discussed.

Molecular assessment of the effect of light and heterotrophy in the scleractinian coral Stylophora pistillata.

Corals acquire nutrients via the transfer of photosynthates by their endosymbionts (autotrophy), or via zooplankton predation by the animal (heterotrophy). During stress events, corals lose their endosymbionts, and undergo starvation, unless they increase their heterotrophic capacities. Molecular mechanisms by which heterotrophy sustains metabolism in stressed corals remain elusive. Here for the first time, to the best of our knowledge, we identified specific genes expressed in heterotrophically fed and unfed colonies of the scleractinian coral Stylophora pistillata, maintained under normal and light-stress conditions. Physiological parameters and gene expression profiling demonstrated that fed corals better resisted stress than unfed ones by exhibiting less oxidative damage and protein degradation. Processes affected in light-stressed unfed corals (HLU), were related to energy and metabolite supply, carbohydrate biosynthesis, ion and nutrient transport, oxidative stress, Ca(2+) homeostasis, metabolism and calcification (carbonic anhydrases, calcium-transporting ATPase, bone morphogenetic proteins). Two genes (cp2u1 and cp1a2), which belong to the cytochrome P450 superfamily, were also upregulated 249 and 10 times, respectively, in HLU corals. In contrast, few of these processes were affected in light-stressed fed corals (HLF) because feeding supplied antioxidants and energetic molecules, which help repair oxidative damage. Altogether, these results show that heterotrophy helps prevent the cascade of metabolic problems downstream of oxidative stress.

Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas.

Endozoicomonas bacteria are emerging as extremely diverse and flexible symbionts of numerous marine hosts inhabiting oceans worldwide. Their hosts range from simple invertebrate species, such as sponges and corals, to complex vertebrates, such as fish. Although widely distributed, the functional role of Endozoicomonas within their host microenvironment is not well understood. In this review, we provide a summary of the currently recognized hosts of Endozoicomonas and their global distribution. Next, the potential functional roles of Endozoicomonas, particularly in light of recent microscopic, genomic, and genetic analyses, are discussed. These analyses suggest that Endozoicomonas typically reside in aggregates within host tissues, have a free-living stage due to their large genome sizes, show signs of host and local adaptation, participate in host-associated protein and carbohydrate transport and cycling, and harbour a high degree of genomic plasticity due to the large proportion of transposable elements residing in their genomes. This review will finish with a discussion on the methodological tools currently employed to study Endozoicomonas and host interactions and review future avenues for studying complex host-microbial symbioses.

New insights into carbon acquisition and exchanges within the coral-dinoflagellate symbiosis under NH4+ and NO3- supply.

Anthropogenic nutrient enrichment affects the biogeochemical cycles and nutrient stoichiometry of coastal ecosystems and is often associated with coral reef decline. However, the mechanisms by which dissolved inorganic nutrients, and especially nitrogen forms (ammonium versus nitrate) can disturb the association between corals and their symbiotic algae are subject to controversial debate. Here, we investigated the coral response to varying N : P ratios, with nitrate or ammonium as a nitrogen source. We showed significant differences in the carbon acquisition by the symbionts and its allocation within the symbiosis according to nutrient abundance, type and stoichiometry. In particular, under low phosphate concentration (0.05 µM), a 3 µM nitrate enrichment induced a significant decrease in carbon fixation rate and low values of carbon translocation, compared with control conditions (N : P = 0.5 : 0.05), while these processes were significantly enhanced when nitrate was replaced by ammonium. A combined enrichment in ammonium and phosphorus (N : P = 3 : 1) induced a shift in nutrient allocation to the symbionts, at the detriment of the host. Altogether, these results shed light into the effect of nutrient enrichment on reef corals. More broadly, they improve our understanding of the consequences of nutrient loading on reef ecosystems, which is urgently required to refine risk management strategies.

Among-species variation in the energy budgets of reef-building corals: scaling from coral polyps to communities.

The symbiosis between corals and dinoflagellates promotes the rapid growth of corals in shallow tropical oceans, and the high overall productivity of coral reefs. The aim of this study was to quantify and understand variation in carbon acquisition and allocation among coral species. We measured multiple physiological traits (including symbiont density, calcification, photosynthesis and tissue composition) for the same coral fragments to facilitate direct comparisons between species (Stylophora pistillata, Pocillopora damicornis, Galaxea fascicularis, Turbinaria reniformis and Acropora sp.). Tissue protein content was highly sensitive to the availability of particulate food, increasing in fed colonies of all species. Despite among-species variation in physiology, and consistent effects of feeding on some traits, overall energy allocation to tissue compared with skeleton growth did not depend on food availability. Extrapolating from our results, estimated whole-assemblage carbon uptake varied >20-fold across different coral assemblages, but this variation was largely driven by differences in the tissue surface area of different colony morphologies, rather than by differences in surface-area-specific physiological rates. Our results caution against drawing conclusions about reef productivity based solely on physiological rates measured per unit tissue surface area. Understanding the causes and consequences of among-species variation in physiological energetics provides insight into the mechanisms that underlie the fluxes of organic matter within reefs, and between reefs and the open ocean.

Trophic dynamics of scleractinian corals: stable isotope evidence.

Reef-building corals form symbioses with dinoflagellates from the diverse genus Symbiodinium. This symbiotic association has developed adaptations to acquire and share nutrients, which are essential for its survival and growth in nutrient-poor tropical waters. The host is thus able to prey on a wide range of organic food sources (heterotrophic nutrition) whereas the symbionts acquire most of the inorganic nutrients (autotrophic nutrition). However, nutrient fluxes between the two partners remain unclear, especially concerning heterotrophically acquired carbon and nitrogen. We combined physiological measurements and pulse-chase isotopic labeling of heterotrophic carbon and nitrogen, as well as autotrophic carbon to track nutrient fluxes in two coral species, Stylophora pistillata and Turbinaria reniformis, in symbiosis with Symbiodinium clades A, and C,D respectively. We showed a rapid acquisition, exchange and a long-term retention of heterotrophic nutrients within the symbiosis, whereas autotrophic nutrients were rapidly used to meet immediate metabolic needs. In addition, there was a higher retention of heterotrophic nitrogen compared with carbon, in agreement with the idea that tropical corals are nitrogen-limited. Finally, a coupling between auto- and heterotrophy was observed in the species S. pistillata, with a higher acquisition and retention of heterotrophic nutrients under low irradiance to compensate for a 50% reduction in autotrophic nutrient acquisition and translocation. Conversely, T. reniformis conserved an equivalent heterotrophic nutrient acquisition at both light levels because this coral species did not significantly reduce its rates of gross photosynthesis and autotrophic carbon acquisition between the two irradiances. These experiments advance the current understanding of the nutrient exchanges between the two partners of a symbiotic association, providing evidence of the complexity of the host-symbiont relationship.