Bacterial symbionts of the precious coral Corallium rubrum are differentially distributed across colony-specific compartments and differ among colormorphs.

Corals engage in symbioses with micro-organisms that provide nutrients and protect the host. Where the prokaryotic microbes perform their symbiotic functions within a coral is, however, poorly understood. Here, we studied the tissue-specific microbiota of the coral Corallium rubrum by dissecting its tissues from the skeleton and separating the white polyps from the red-coloured coenenchyme, followed by 16S rRNA gene metabarcoding of the three fractions. Dissection was facilitated by incubating coral fragments in RNAlater, which caused tissues to detach from the skeleton. Our results show compartmentalisation of the microbiota. Specifically, Endozoicomonas, Parcubacteria and a Gammaproteobacteria were primarily located in polyps, whereas Nitrincolaceae and one Spirochaeta phylotype were found mainly in the coenenchyme. The skeleton-associated microbiota was distinct from the microbiota in the tissues. Given the difference in tissue colour and microbiota of the polyps and coenenchyme, we analysed the microbiota of three colormorphs of C. rubrum (red, pink, white), finding that the main difference was a very low abundance of Spirochaeta in white colormorphs. While the functions of C. rubrum's symbionts are unknown, their localisation within the colony suggests that microhabitats exist, and the presence of Spirochaeta appears to be linked to the colour of C. rubrum.

Unveiling microbiome changes in Mediterranean octocorals during the 2022 marine heatwaves: quantifying key bacterial symbionts and potential pathogens.

BACKGROUND: Climate change has accelerated the occurrence and severity of heatwaves in the Mediterranean Sea and poses a significant threat to the octocoral species that form the foundation of marine animal forests (MAFs). As coral health intricately relies on the symbiotic relationships established between corals and microbial communities, our goal was to gain a deeper understanding of the role of bacteria in the observed tissue loss of key octocoral species following the unprecedented heatwaves in 2022. RESULTS: Using amplicon sequencing and taxon-specific qPCR analyses, we unexpectedly found that the absolute abundance of the major bacterial symbionts, Spirochaetaceae (C. rubrum) and Endozoicomonas (P. clavata), remained, in most cases, unchanged between colonies with 0% and 90% tissue loss. These results suggest that the impairment of coral health was not due to the loss of the main bacterial symbionts. However, we observed a significant increase in the total abundance of bacterial opportunists, including putative pathogens such as Vibrio, which was not evident when only their relative abundance was considered. In addition, there was no clear relation between bacterial symbiont loss and the intensity of thermal stress, suggesting that factors other than temperature may have influenced the differential response of octocoral microbiomes at different sampling sites. CONCLUSIONS: Our results indicate that tissue loss in octocorals is not directly caused by the decline of the main bacterial symbionts but by the proliferation of opportunistic and pathogenic bacteria. Our findings thus underscore the significance of considering both relative and absolute quantification approaches when evaluating the impact of stressors on coral microbiome as the relative quantification does not accurately depict the actual changes in the microbiome. Consequently, this research enhances our comprehension of the intricate interplay between host organisms, their microbiomes, and environmental stressors, while offering valuable insights into the ecological implications of heatwaves on marine animal forests. Video Abstract.

Holobiont responses of mesophotic precious red coral Corallium rubrum to thermal anomalies.

Marine heat waves (MHWs) have increased in frequency and intensity worldwide, causing mass mortality of benthic organisms and loss of biodiversity in shallow waters. The Mediterranean Sea is no exception, with shallow populations of habitat-forming octocorals facing the threat of local extinction. The mesophotic zone, which is less affected by MHWs, may be of ecological importance in conservation strategies for these species. However, our understanding of the response of mesophotic octocoral holobionts to changes in seawater temperature remains limited. To address this knowledge gap, we conducted a study on an iconic Mediterranean octocoral, the red coral Corallium rubrum sampled at 60 m depth and 15 °C. We exposed the colonies to temperatures they occasionally experience (18 °C) and temperatures that could occur at the end of the century if global warming continues (21 °C). We also tested their response to extremely cold and warm temperatures (12 °C and 24 °C). Our results show a high tolerance of C. rubrum to a two-month long exposure to temperatures ranging from 12 to 21 °C as no colony showed signs of tissue loss, reduced feeding ability, stress-induced gene expression, or disruption of host-bacterial symbioses. At 24 °C, however, we measured a sharp decrease in the relative abundance of Spirochaetaceae, which are the predominant bacterial symbionts under healthy conditions, along with a relative increase in Vibrionaceae. Tissue loss and overexpression of the tumor necrosis factor receptor 1 gene were also observed after two weeks of exposure. In light of ongoing global warming, our study helps predict the consequences of MHWs on mesophotic coralligenous reefs and the biodiversity that depends on them.

Differences in carbonate chemistry up-regulation of long-lived reef-building corals.

With climate projections questioning the future survival of stony corals and their dominance as tropical reef builders, it is critical to understand the adaptive capacity of corals to ongoing climate change. Biological mediation of the carbonate chemistry of the coral calcifying fluid is a fundamental component for assessing the response of corals to global threats. The Tara Pacific expedition (2016-2018) provided an opportunity to investigate calcification patterns in extant corals throughout the Pacific Ocean. Cores from colonies of the massive Porites and Diploastrea genera were collected from different environments to assess calcification parameters of long-lived reef-building corals. At the basin scale of the Pacific Ocean, we show that both genera systematically up-regulate their calcifying fluid pH and dissolved inorganic carbon to achieve efficient skeletal precipitation. However, while Porites corals increase the aragonite saturation state of the calcifying fluid (Ωcf) at higher temperatures to enhance their calcification capacity, Diploastrea show a steady homeostatic Ωcf across the Pacific temperature gradient. Thus, the extent to which Diploastrea responds to ocean warming and/or acidification is unclear, and it deserves further attention whether this is beneficial or detrimental to future survival of this coral genus.

Telomere DNA length regulation is influenced by seasonal temperature differences in short-lived but not in long-lived reef-building corals.

Telomeres are environment-sensitive regulators of health and aging. Here,we present telomere DNA length analysis of two reef-building coral genera revealing that the long- and short-term water thermal regime is a key driver of between-colony variation across the Pacific Ocean. Notably, there are differences between the two studied genera. The telomere DNA lengths of the short-lived, more stress-sensitive Pocillopora spp. colonies were largely determined by seasonal temperature variation, whereas those of the long-lived, more stress-resistant Porites spp. colonies were insensitive to seasonal patterns, but rather influenced by past thermal anomalies. These results reveal marked differences in telomere DNA length regulation between two evolutionary distant coral genera exhibiting specific life-history traits. We propose that environmentally regulated mechanisms of telomere maintenance are linked to organismal performances, a matter of paramount importance considering the effects of climate change on health.

Diversity of the Pacific Ocean coral reef microbiome.

Coral reefs are among the most diverse ecosystems on Earth. They support high biodiversity of multicellular organisms that strongly rely on associated microorganisms for health and nutrition. However, the extent of the coral reef microbiome diversity and its distribution at the oceanic basin-scale remains to be explored. Here, we systematically sampled 3 coral morphotypes, 2 fish species, and planktonic communities in 99 reefs from 32 islands across the Pacific Ocean, to assess reef microbiome composition and biogeography. We show a very large richness of reef microorganisms compared to other environments, which extrapolated to all fishes and corals of the Pacific, approximates the current estimated total prokaryotic diversity for the entire Earth. Microbial communities vary among and within the 3 animal biomes (coral, fish, plankton), and geographically. For corals, the cross-ocean patterns of diversity are different from those known for other multicellular organisms. Within each coral morphotype, community composition is always determined by geographic distance first, both at the island and across ocean scale, and then by environment. Our unprecedented sampling effort of coral reef microbiomes, as part of the Tara Pacific expedition, provides new insight into the global microbial diversity, the factors driving their distribution, and the biocomplexity of reef ecosystems.

Ecology of Endozoicomonadaceae in three coral genera across the Pacific Ocean.

Health and resilience of the coral holobiont depend on diverse bacterial communities often dominated by key marine symbionts of the Endozoicomonadaceae family. The factors controlling their distribution and their functional diversity remain, however, poorly known. Here, we study the ecology of Endozoicomonadaceae at an ocean basin-scale by sampling specimens from three coral genera (Pocillopora, Porites, Millepora) on 99 reefs from 32 islands across the Pacific Ocean. The analysis of 2447 metabarcoding and 270 metagenomic samples reveals that each coral genus harbored a distinct new species of Endozoicomonadaceae. These species are composed of nine lineages that have distinct biogeographic patterns. The most common one, found in Pocillopora, appears to be a globally distributed symbiont with distinct metabolic capabilities, including the synthesis of amino acids and vitamins not produced by the host. The other lineages are structured partly by the host genetic lineage in Pocillopora and mainly by the geographic location in Porites. Millepora is more rarely associated to Endozoicomonadaceae. Our results show that different coral genera exhibit distinct strategies of host-Endozoicomonadaceae associations that are defined at the bacteria lineage level.

Host transcriptomic plasticity and photosymbiotic fidelity underpin Pocillopora acclimatization across thermal regimes in the Pacific Ocean.

Heat waves are causing declines in coral reefs globally. Coral thermal responses depend on multiple, interacting drivers, such as past thermal exposure, endosymbiont community composition, and host genotype. This makes the understanding of their relative roles in adaptive and/or plastic responses crucial for anticipating impacts of future warming. Here, we extracted DNA and RNA from 102 Pocillopora colonies collected from 32 sites on 11 islands across the Pacific Ocean to characterize host-photosymbiont fidelity and to investigate patterns of gene expression across a historical thermal gradient. We report high host-photosymbiont fidelity and show that coral and microalgal gene expression respond to different drivers. Differences in photosymbiotic association had only weak impacts on host gene expression, which was more strongly correlated with the historical thermal environment, whereas, photosymbiont gene expression was largely determined by microalgal lineage. Overall, our results reveal a three-tiered strategy of thermal acclimatization in Pocillopora underpinned by host-photosymbiont specificity, host transcriptomic plasticity, and differential photosymbiotic association under extreme warming.

Integrative omics framework for characterization of coral reef ecosystems from the Tara Pacific expedition.

Coral reef science is a fast-growing field propelled by the need to better understand coral health and resilience to devise strategies to slow reef loss resulting from environmental stresses. Key to coral resilience are the symbiotic interactions established within a complex holobiont, i.e. the multipartite assemblages comprising the coral host organism, endosymbiotic dinoflagellates, bacteria, archaea, fungi, and viruses. Tara Pacific is an ambitious project built upon the experience of previous Tara Oceans expeditions, and leveraging state-of-the-art sequencing technologies and analyses to dissect the biodiversity and biocomplexity of the coral holobiont screened across most archipelagos spread throughout the entire Pacific Ocean. Here we detail the Tara Pacific workflow for multi-omics data generation, from sample handling to nucleotide sequence data generation and deposition. This unique multidimensional framework also includes a large amount of concomitant metadata collected side-by-side that provide new assessments of coral reef biodiversity including micro-biodiversity and shape future investigations of coral reef dynamics and their fate in the Anthropocene.

Endogenous viral elements reveal associations between a non-retroviral RNA virus and symbiotic dinoflagellate genomes.

Endogenous viral elements (EVEs) offer insight into the evolutionary histories and hosts of contemporary viruses. This study leveraged DNA metagenomics and genomics to detect and infer the host of a non-retroviral dinoflagellate-infecting +ssRNA virus (dinoRNAV) common in coral reefs. As part of the Tara Pacific Expedition, this study surveyed 269 newly sequenced cnidarians and their resident symbiotic dinoflagellates (Symbiodiniaceae), associated metabarcodes, and publicly available metagenomes, revealing 178 dinoRNAV EVEs, predominantly among hydrocoral-dinoflagellate metagenomes. Putative associations between Symbiodiniaceae and dinoRNAV EVEs were corroborated by the characterization of dinoRNAV-like sequences in 17 of 18 scaffold-scale and one chromosome-scale dinoflagellate genome assembly, flanked by characteristically cellular sequences and in proximity to retroelements, suggesting potential mechanisms of integration. EVEs were not detected in dinoflagellate-free (aposymbiotic) cnidarian genome assemblies, including stony corals, hydrocorals, jellyfish, or seawater. The pervasive nature of dinoRNAV EVEs within dinoflagellate genomes (especially Symbiodinium), as well as their inconsistent within-genome distribution and fragmented nature, suggest ancestral or recurrent integration of this virus with variable conservation. Broadly, these findings illustrate how +ssRNA viruses may obscure their genomes as members of nested symbioses, with implications for host evolution, exaptation, and immunity in the context of reef health and disease.

Pervasive tandem duplications and convergent evolution shape coral genomes.

BACKGROUND: Over the last decade, several coral genomes have been sequenced allowing a better understanding of these symbiotic organisms threatened by climate change. Scleractinian corals are reef builders and are central to coral reef ecosystems, providing habitat to a great diversity of species. RESULTS: In the frame of the Tara Pacific expedition, we assemble two coral genomes, Porites lobata and Pocillopora cf. effusa, with vastly improved contiguity that allows us to study the functional organization of these genomes. We annotate their gene catalog and report a relatively higher gene number than that found in other public coral genome sequences, 43,000 and 32,000 genes, respectively. This finding is explained by a high number of tandemly duplicated genes, accounting for almost a third of the predicted genes. We show that these duplicated genes originate from multiple and distinct duplication events throughout the coral lineage. They contribute to the amplification of gene families, mostly related to the immune system and disease resistance, which we suggest to be functionally linked to coral host resilience. CONCLUSIONS: At large, we show the importance of duplicated genes to inform the biology of reef-building corals and provide novel avenues to understand and screen for differences in stress resilience.

Redistribution of fisheries catch potential in Mediterranean and North European waters under climate change scenarios.

The Mediterranean Sea is a hotspot of global warming where key commercial species, such as demersal and pelagic fishes, and cephalopods, could experience abrupt distribution shifts in the near future. However, the extent to which these range shifts may impact fisheries catch potential remains poorly understood at the scale of Exclusive Economic Zones (EEZs). Here, we evaluated the projected changes in Mediterranean fisheries catches potential, by target fishing gears, under different climate scenarios throughout the 21st century. We show that the future Mediterranean maximum catch potential may decrease considerably by the end of the century under high emission scenarios in South Eastern Mediterranean countries. These projected decreases range between -20 to -75 % for catch by pelagic trawl and seine, -50 to -75 % for fixed nets and traps and exceed -75 % for benthic trawl. In contrast, fixed nets and traps, and benthic trawl fisheries may experience an increase in their catch potential in the North and Celtic seas, while future catches by pelagic trawl and seine may decrease in the same areas. We show that a high emission scenario may considerably amplify the future redistribution of fisheries catch potential across European Seas, thus highlighting the need to limit global warming. Our projections at the manageable scale of EEZ and the quantification of climate-induced impacts on a large part of the Mediterranean and European fisheries is therefore a first, and considerable step toward the development of climate mitigation and adaptations strategies for the fisheries sector.

Testing hypotheses on the calcification in scleractinian corals using a spatio-temporal model that shows a high degree of robustness.

Calcification in photosynthetic scleractinian corals is a complicated process that involves many different biological, chemical, and physical sub-processes that happen within and around the coral tissue. Identifying and quantifying the role of separate processes in vivo or in vitro is difficult or not possible. A computational model can facilitate this research by simulating the sub-processes independently. This study presents a spatio-temporal model of the calcification physiology, which is based on processes that are considered essential for calcification: respiration, photosynthesis, Ca2＋-ATPase, carbonic anhydrase. The model is used to test different hypotheses considering ion transport across the calicoblastic cells and Light Enhanced Calcification (LEC). It is also used to quantify the effect of ocean acidification (OA) on the Extracellular Calcifying Medium (ECM) and ATP-consumption of Ca2＋-ATPase. It was able to reproduce the experimental data of three separate studies and finds that paracellular transport plays a minor role compared to transcellular transport. In the model, LEC results from increased Ca2＋-ATPase activity in combination with increased metabolism. Implementing OA increases the concentration of CO2 throughout the entire tissue, thereby increasing the availability of CO3- in the ECM. As a result, the model finds that calcification becomes more energy-demanding and the calcification rate increases.

An alternative and effective method for extracting skeletal organic matrix adapted to the red coral Corallium rubrum.

Skeleton formation in corals is a biologically controlled process in which an extracellular organic matrix (OM) is entrapped inside the calcified structure. The analysis of OM requires a time-consuming and tedious extraction that includes grinding, demineralization, multiple rinsing and concentration steps. Here we present an alternative and straightforward method for the red coral Corallium rubrum that requires little equipment and saves steps. The entire skeleton is directly demineralized to produce a tractable material called ghost, which is further rinsed and melted at 80°C in water. The comparative analysis of the standard and alternative methods by electrophoresis, western blot, and FTIR of C. rubrum OM, shows that the 'alternative OM' is of higher quality. Advantages and limitations of both methods are discussed.

Expected contraction in the distribution ranges of demersal fish of high economic value in the Mediterranean and European Seas.

Fisheries and aquaculture are facing many challenges worldwide, especially adaptation to climate change. Investigating future distributional changes of largely harvested species has become an extensive research topic, aiming at providing realistic ecological scenarios on which to build management measures, to help fisheries and aquaculture adapt to future climate-driven changes. Here, we use an ensemble modelling approach to estimate the contemporary and future distributional range of eight demersal fish species of high economic value in the Mediterranean Sea. We identify a cardinal influence of (i) temperature on fish species distributions, all being shaped by yearly mean and seasonality in sea bottom temperature, and (ii) the primary production. By assessing the effects of changes in future climate conditions under three Representative Concentration Pathway (RCP2.6, RCP4.5 and RCP8.5) scenarios over three periods of the twenty-first century, we project a contraction of the distributional range of the eight species in the Mediterranean Sea, with a general biogeographical displacement towards the North European coasts. This will help anticipating changes in future catch potential in a warmer world, which is expected to have substantial economic consequences for Mediterranean fisheries.

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.

Coral holobionts and biotechnology: from Blue Economy to coral reef conservation.

Corals are of ecological and economic importance, providing habitat for species and contributing to coastal protection, fisheries, and tourism. Their biotechnological potential is also increasingly recognized. Particularly, the production of pharmaceutically interesting compounds by corals and their microbial associates stimulated natural product-based drug discovery. The efficient light distribution by coral skeletons for optimal photosynthesis by algal symbionts has led to 3D-printed bionic corals that may be used to upscale micro-algal cultivation for bioenergy generation. However, corals are under threat from climate change and pollution, and biotechnological approaches to increase their resilience, like 'probiotics' and 'assisted evolution', are being evaluated. In this review, we summarize the recent biotechnological developments related to corals with an emphasis on coral conservation, drug discovery and bioenergy.

Effects of Ocean Acidification on Resident and Active Microbial Communities of Stylophora pistillata.

Ocean warming and ocean acidification (OA) are direct consequences of climate change and affect coral reefs worldwide. While the effect of ocean warming manifests itself in increased frequency and severity of coral bleaching, the effects of ocean acidification on corals are less clear. In particular, long-term effects of OA on the bacterial communities associated with corals are largely unknown. In this study, we investigated the effects of ocean acidification on the resident and active microbiome of long-term aquaria-maintained Stylophora pistillata colonies by assessing 16S rRNA gene diversity on the DNA (resident community) and RNA level (active community). Coral colony fragments of S. pistillata were kept in aquaria for 2 years at four different pCO2 levels ranging from current pH conditions to increased acidification scenarios (i.e., pH 7.2, 7.4, 7.8, and 8). We identified 154 bacterial families encompassing 2,047 taxa (OTUs) in the resident and 89 bacterial families including 1,659 OTUs in the active communities. Resident communities were dominated by members of Alteromonadaceae, Flavobacteriaceae, and Colwelliaceae, while active communities were dominated by families Cyclobacteriacea and Amoebophilaceae. Besides the overall differences between resident and active community composition, significant differences were seen between the control (pH 8) and the two lower pH treatments (7.2 and 7.4) in the active community, but only between pH 8 and 7.2 in the resident community. Our analyses revealed profound differences between the resident and active microbial communities, and we found that OA exerted stronger effects on the active community. Further, our results suggest that rDNA- and rRNA-based sequencing should be considered complementary tools to investigate the effects of environmental change on microbial assemblage structure and activity.

The Evolution of Calcification in Reef-Building Corals.

Corals build the structural foundation of coral reefs, one of the most diverse and productive ecosystems on our planet. Although the process of coral calcification that allows corals to build these immense structures has been extensively investigated, we still know little about the evolutionary processes that allowed the soft-bodied ancestor of corals to become the ecosystem builders they are today. Using a combination of phylogenomics, proteomics, and immunohistochemistry, we show that scleractinian corals likely acquired the ability to calcify sometime between ∼308 and ∼265 Ma through a combination of lineage-specific gene duplications and the co-option of existing genes to the calcification process. Our results suggest that coral calcification did not require extensive evolutionary changes, but rather few coral-specific gene duplications and a series of small, gradual optimizations of ancestral proteins and their co-option to the calcification process.