Irradiance driven trophic plasticity in the coral Madracis pharensis from the Eastern Mediterranean.

The distribution of symbiotic scleractinian corals is driven, in part, by light availability, as host energy demands are partially met through translocation of photosynthate. Physiological plasticity in response to environmental conditions, such as light, enables the expansion of resilient phenotypes in the face of changing environmental conditions. Here we compared the physiology, morphology, and taxonomy of the host and endosymbionts of individual Madracis pharensis corals exposed to dramatically different light conditions based on colony orientation on the surface of a shipwreck at 30 m depth in the Bay of Haifa, Israel. We found significant differences in symbiont species consortia, photophysiology, and stable isotopes, suggesting that these corals can adjust multiple aspects of host and symbiont physiology in response to light availability. These results highlight the potential of corals to switch to a predominantly heterotrophic diet when light availability and/or symbiont densities are too low to sustain sufficient photosynthesis, which may provide resilience for corals in the face of climate change.

Heterotrophy in marine animal forests in an era of climate change.

Marine animal forests (MAFs) are benthic ecosystems characterised by biogenic three-dimensional structures formed by suspension feeders such as corals, gorgonians, sponges and bivalves. They comprise highly diversified communities among the most productive in the world's oceans. However, MAFs are in decline due to global and local stressors that threaten the survival and growth of their foundational species and associated biodiversity. Innovative and scalable interventions are needed to address the degradation of MAFs and increase their resilience under global change. Surprisingly, few studies have considered trophic interactions and heterotrophic feeding of MAF suspension feeders as an integral component of MAF conservation. Yet, trophic interactions are important for nutrient cycling, energy flow within the food web, biodiversity, carbon sequestration, and MAF stability. This comprehensive review describes trophic interactions at all levels of ecological organisation in tropical, temperate, and cold-water MAFs. It examines the strengths and weaknesses of available tools for estimating the heterotrophic capacities of the foundational species in MAFs. It then discusses the threats that climate change poses to heterotrophic processes. Finally, it presents strategies for improving trophic interactions and heterotrophy, which can help to maintain the health and resilience of MAFs.

Assessment of storm impact on coral reef structural complexity.

Extreme weather events are increasing in frequency and magnitude. Consequently, it is important to understand their effects and remediation. Resilience reflects the ability of an ecosystem to absorb change, which is important for understanding ecological dynamics and trajectories. To describe the impact of a powerful storm on coral reef structural complexity, we used novel computational tools and detailed 3D reconstructions captured at three time points over three years. Our data-set Reefs4D of 21 co-registered image-based models enabled us to calculate the differences at seven sites over time and is released with the paper. We employed six geometrical metrics, two of which are new algorithms for calculating fractal dimension of reefs in full 3D. We conducted a multivariate analysis to reveal which sites were affected the most and their relative recovery. We also explored the changes in fractal dimension per size category using our cube-counting algorithm. Three metrics showed a significant difference between time points, i.e., decline and subsequent recovery in structural complexity. The multivariate analysis and the results per size category showed a similar trend. Coral reef resilience has been the subject of seminal studies in ecology. We add important information to the discussion by focusing on 3D structure through image-based modeling. The full picture shows resilience in structural complexity, suggesting that the reef has not gone through a catastrophic phase shift. Our novel analysis framework is widely transferable and useful for research, monitoring, and management.

Sediment Microbiota as a Proxy of Environmental Health: Discovering Inter- and Intrakingdom Dynamics along the Eastern Mediterranean Continental Shelf.

Sedimentary marine habitats are the largest ecosystem on our planet in terms of area. Marine sediment microbiota govern most of the benthic biological processes and therefore are responsible for much of the global biogeochemical activity. Sediment microbiota respond, even rapidly, to natural change in environmental conditions as well as disturbances of anthropogenic sources. The latter greatly impact the continental shelf. Characterization and monitoring of the sediment microbiota may serve as an important tool for assessing environmental health and indicate changes in the marine ecosystem. This study examined the suitability of marine sediment microbiota as a bioindicator for environmental health in the eastern Mediterranean Sea. Integration of information from Bacteria, Archaea, and Eukaryota enabled robust assessment of environmental factors controlling sediment microbiota composition: seafloor-depth (here representing sediment grain size and total organic carbon), core depth, and season (11%, 4.2%, and 2.5% of the variance, respectively). Furthermore, inter- and intrakingdom cooccurrence patterns indicate that ecological filtration as well as stochastic processes may control sediment microbiota assembly. The results show that the sediment microbiota was robust over 3 years of sampling, in terms of both representation of region (outside the model sites) and robustness of microbial markers. Furthermore, anthropogenic disturbance was reflected by significant transformations in sediment microbiota. We therefore propose sediment microbiota analysis as a sensitive approach to detect disturbances, which is applicable for long-term monitoring of marine environmental health. IMPORTANCE Analysis of data, curated over 3 years of sediment sampling, improves our understanding of microbiota assembly in marine sediment. Furthermore, we demonstrate the importance of cross-kingdom integration of information in the study of microbial community ecology. Finally, the urgent need to propose an applicable approach for environmental health monitoring is addressed here by establishment of sediment microbiota as a robust and sensitive model.

Symbiodiniaceae Are the First Site of Heterotrophic Nitrogen Assimilation in Reef-Building Corals.

Coral reefs depend on the highly optimized mutualistic relationship between corals and Symbiodiniaceae dinoflagellates. Both partners exchange nutrients obtained through heterotrophy of the host and autotrophy of the symbionts. While heterotrophy helps corals withstand the harmful effects of seawater warming, the exchange of heterotrophic nutrients between the two partners is poorly understood. Here, we used compound-specific δ15N and δ13C of amino acids (δ15NAA and δ13CAA) and a 15N pulse-chase experiment with Artemia salina nauplii in two coral-dinoflagellate associations to trace the assimilation and allocation of heterotrophic nutrients within the partners. We observed that changes in the trophic position (TPGlx-Phe), δ15NAA, and δ13CAA with heterotrophy were holobiont-dependent. Furthermore, while TPGlx-Phe and δ15N of all AAs significantly increased with heterotrophy in the symbionts and host of Stylophora pistillata, only the δ15NAA of the symbionts changed in Turbinaria reniformis. Together with the pulse-chase experiment, the results suggested a direct transfer of heterotrophically acquired AAs to the symbionts of S. pistillata and a transfer of ammonium to the symbionts of T. reniformis. Overall, we demonstrated that heterotrophy underpinned the nutrition of Symbiodinaceae and possibly influenced their stress tolerance under changing environmental conditions. IMPORTANCE Coral reefs rely upon the highly optimized nutritional symbiosis between corals and Symbiodiniaceae dinoflagellates. Heterotrophic feeding on plankton is key to the resistance of corals to environmental stress. Yet, a detailed understanding of heterotrophic nutrient assimilation and utilization within the symbiosis is lacking. Here, we used the advanced tools of compound-specific isotope analysis of amino acids and 15N-labeling of plankton to show that heterotrophy underpinned the nutrition of Symbiodinaceae. Symbionts received either heterotrophically acquired amino acids or recycled ammonium due to their association with the coral host. This study brought new insight into the nutrient exchanges in coral-Symbiodiniaceae associations and allowed a better understanding of the mechanisms involved in coral resistance to environmental stress.

Selection of mesophotic habitats by Oculina patagonica in the Eastern Mediterranean Sea following global warming.

Globally, species are migrating in an attempt to track optimal isotherms as climate change increasingly warms existing habitats. Stony corals are severely threatened by anthropogenic warming, which has resulted in repeated mass bleaching and mortality events. Since corals are sessile as adults and with a relatively old age of sexual maturity, they are slow to latitudinally migrate, but corals may also migrate vertically to deeper, cooler reefs. Herein we describe vertical migration of the Mediterranean coral Oculina patagonica from less than 10 m depth to > 30 m. We suggest that this range shift is a response to rapidly warming sea surface temperatures on the Israeli Mediterranean coastline. In contrast to the vast latitudinal distance required to track temperature change, this species has migrated deeper where summer water temperatures are up to 2 °C cooler. Comparisons of physiology, morphology, trophic position, symbiont type, and photochemistry between deep and shallow conspecifics revealed only a few depth-specific differences. At this study site, shallow colonies typically inhabit low light environments (caves, crevices) and have a facultative relationship with photosymbionts. We suggest that this existing phenotype aided colonization of the mesophotic zone. This observation highlights the potential for other marine species to vertically migrate.

Tracing the Trophic Plasticity of the Coral-Dinoflagellate Symbiosis Using Amino Acid Compound-Specific Stable Isotope Analysis.

The association between corals and photosynthetic dinoflagellates is one of the most well-known nutritional symbioses, but nowadays it is threatened by global changes. Nutritional exchanges are critical to understanding the performance of this symbiosis under stress conditions. Here, compound-specific δ15N and δ13C values of amino acids (δ15NAA and δ13CAA) were assessed in autotrophic, mixotrophic and heterotrophic holobionts as diagnostic tools to follow nutritional interactions between the partners. Contrary to what was expected, heterotrophy was mainly traced through the δ15N of the symbiont's amino acids (AAs), suggesting that symbionts directly profit from host heterotrophy. The trophic index (TP) ranged from 1.1 to 2.3 from autotrophic to heterotrophic symbionts. In addition, changes in TP across conditions were more significant in the symbionts than in the host. The similar δ13C-AAs signatures of host and symbionts further suggests that symbiont-derived photosynthates are the main source of carbon for AAs synthesis. Symbionts, therefore, appear to be a key component in the AAs biosynthetic pathways, and might, via this obligatory function, play an essential role in the capacity of corals to withstand environmental stress. These novel findings highlight important aspects of the nutritional exchanges in the coral-dinoflagellates symbiosis. In addition, they feature δ15NAA as a useful tool for studies regarding the nutritional exchanges within the coral-symbiodiniaceae symbiosis.

Molecular and skeletal fingerprints of scleractinian coral biomineralization: From the sea surface to mesophotic depths.

Reef-building corals, the major producers of biogenic calcium carbonate, form skeletons in a plethora of morphological forms. Here we studied skeletal modifications of Stylophora pistillata (clade 4) colonies that adapt to increasing depths with decreasing ambient light. The coral show characteristic transitions from spherical morphologies (shallow depths, 5 m deep) to flat and branching geometries (mesophotic depths, 60 m deep). Such changes are typically ascribed to the algal photosymbiont physiological feedback with the coral that host them. We find specific fine-scale skeletal variability in accretion of structure at shallow- and mesophotic depth morphotypes that suggest underlying genomic regulation of biomineralization pathways of the coral host. To explain this, we conducted comparative morphology-based analyses, including optical and electron microscopy, tomography and X-ray diffraction analysis coupled with a comprehensive transcriptomic analysis of S. pistillata. The samples originated from Gulf of Eilat in the Red Sea collected along a depth gradient from shallow to mesophotic depths (5 to 60 m). Additional samples were experimentally transplanted from 5 m to 60 m and from 60 m to 5 m. Interestingly, both morphologically and functionally, transplanted corals partly adapt by exhibiting typical depth-specific properties. In mesophotic depths, we find that the organic matrix fraction is enriched in the coralla, well matching the overrepresentation of transcripts encoding biomineralization "tool-kit" structural extracellularproteins that was observed. These results provide insights into the molecular mechanisms of calcification and skeletal adaptation that repeatedly allowed this coral group to adapt to a range of environments presumably with a rich geological past. STATEMENT OF SIGNIFICANCE: Understanding the reef coral physiological plasticity under a rapidly changing climate is of crucial importance for the protection of coral reef ecosystems. Most of the reef corals operate near their upper limit of heat tolerance. A possible rescue for some coral species is migration to deeper, cooler mesophotic depths. However, gradually changing environmental parameters (especially light) along the depth gradient pose new adaptative stress on corals with largely unknown influences on the various biological molecular pathways. This work provides a first comprehensive analysis of changes in gene expression, including biomineralization "tool kit" genes, and reports the fine-scale microstructural and crystallographic skeletal details in S. pistillata collected in the Red Sea along a depth gradient spannign 5 to 60 m.

Energy Sources of the Depth-Generalist Mixotrophic Coral Stylophora pistillata.

Energy sources of corals, ultimately sunlight and plankton availability, change dramatically from shallow to mesophotic (30-150 m) reefs. Depth-generalist corals, those that occupy both of these two distinct ecosystems, are adapted to cope with such extremely diverse conditions. In this study, we investigated the trophic strategy of the depth-generalist hermatypic coral Stylophora pistillata and the ability of mesophotic colonies to adapt to shallow reefs. We compared symbiont genera composition, photosynthetic traits and the holobiont trophic position and carbon sources, calculated from amino acids compound-specific stable isotope analysis (AA-CSIA), of shallow, mesophotic and translocated corals. This species harbors different Symbiodiniaceae genera at the two depths: Cladocopium goreaui (dominant in mesophotic colonies) and Symbiodinium microadriaticum (dominant in shallow colonies) with a limited change after transplantation. This allowed us to determine which traits stem from hosting different symbiont species compositions across the depth gradient. Calculation of holobiont trophic position based on amino acid δ15N revealed that heterotrophy represents the same portion of the total energy budget in both depths, in contrast to the dogma that predation is higher in corals growing in low light conditions. Photosynthesis is the major carbon source to corals growing at both depths, but the photosynthetic rate is higher in the shallow reef corals, implicating both higher energy consumption and higher predation rate in the shallow habitat. In the corals transplanted from deep to shallow reef, we observed extensive photo-acclimation by the Symbiodiniaceae cells, including substantial cellular morphological modifications, increased cellular chlorophyll a, lower antennae to photosystems ratios and carbon signature similar to the local shallow colonies. In contrast, non-photochemical quenching remains low and does not increase to cope with the high light regime of the shallow reef. Furthermore, host acclimation is much slower in these deep-to-shallow transplanted corals as evident from the lower trophic position and tissue density compared to the shallow-water corals, even after long-term transplantation (18 months). Our results suggest that while mesophotic reefs could serve as a potential refuge for shallow corals, the transition is complex, as even after a year and a half the acclimation is only partial.

Conditioning film and initial biofilm formation on electrochemical CaCO3 deposition on a metallic net in the marine environment.

Electrochemical deposition of minerals is a unique technology for artificial reef constructions, relying on calcium carbonate (CaCO3) build-up over metallic structures through electrolysis of seawater. The present study traces the first 72 h following electric current termination on bacterial biofilm build-up on a metallic net covered with CaCO3. 16S rRNA clone libraries indicated a dynamic succession. Proteobacteria and Bacteroidetes were evident at all sampling times while Cyanobacteria appeared only within the first 8 h. A significant increase in total organic carbon (TOC) and total protein was observed after 48 h with a significant correlation (R(2) = 0.74), indicating TOC is a good tool for characterizing initial biofilm formation. 18S rRNA gene sequences obtained 72 h following current termination indicated a significant presence of Cnidarians (51%). Understanding the dynamics among primary bacterial settlers is important because they play a crucial role in driving the colonization of sessile invertebrate communities on artificial, as well as natural surfaces.