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ABSTRACT Coral bleaching has been rapidly increasing in recent years due to abnormally elevated temperature, leading to massive damage to coral reefs worldwide. Understanding the processes and micro-ecological mechanisms of coral symbionts in response to bleaching is crucial as evidence accumulates that micro-organisms (particularly the bacteria) contribute to the health and recovery of coral, especially during heat stress. However, the exact functional mechanism of bacteria has not yet been fully elucidated. In this study, we performed metagenomic and metaproteomic analyses of healthy and bleached Acropora muricata corals to identify taxonomic and functional shifts in coral symbionts during a natural thermal bleaching event on Hainan Island. The results showed that symbiont species tended to be more abundant in bleached corals than healthy corals, and the bacterial community appeared to be crucial to coral bleaching. The relative abundance of opportunistic pathogens dramatically increased in bleached corals, accompanied by the reduction of beneficial bacteria. In addition, a direct comparison of metagenomic data sets indicated major changes in functional genes, with bleached corals exhibiting significant metabolic enrichment, while healthy corals maintained lower metabolism and energy consumption. Carbohydrate-active enzyme genes were remarkably activated, and virulence factors were highly represented in bleached corals, which was directly related to the increased abundance of pathogenic bacteria. Metaproteomic analysis also demonstrated that bleaching greatly affected photosynthesis and energy metabolism of coral symbionts. Among them, the biological processes of photosynthesis and chlorophyll biosynthesis were common in healthy corals, while pathways involved in gluconeogenesis and apoptosis were significantly enriched in bleached corals. Bacteria-mediated processes in healthy corals contribute to maintaining the basic functions of symbionts and resisting stress, whereas the proliferation of pathogenic bacteria in bleached corals leads to metabolic abnormalities of symbionts, showing enhanced energy metabolism and catalytic activity. In summary, the two omics analyzes revealed that bleaching caused enormous physiological damage to corals, and bacterial imbalance and dysfunction were the potential micro-ecological mechanisms underlying this event.IMPORTANCECoral reefs worldwide are facing rapid decline due to coral bleaching. However, knowledge of the physiological characteristics and molecular mechanisms of coral symbionts respond to stress is scarce. Here, metagenomic and metaproteomic approaches were utilized to shed light on the changes in the composition and functions of coral symbiotic bacteria during coral bleaching. The results demonstrated that coral bleaching significantly affected the composition of symbionts, with bacterial communities dominating in bleached corals. Through differential analyses of gene and protein expression, it becomes evident that symbionts experience functional disturbances in response to heat stress. These disturbances result in abnormal energy metabolism, which could potentially compromise the health and resilience of the symbionts. Furthermore, our findings highlighted the highly diverse microbial communities of coral symbionts, with beneficial bacteria providing critical services to corals in stress responses and pathogenic bacteria driving coral bleaching. This study provides comprehensive insights into the complex response mechanisms of coral symbionts under heat stress from the micro-ecological perspective and offers fundamental data for future monitoring of coral health.

Dinoflagellates in the order Suessiales include the family Symbiodiniaceae, which have essential roles as photosymbionts in corals, and their cold-adapted sister group, Polarella glacialis. These diverse taxa exhibit extensive genomic divergence, although their genomes are relatively small (haploid size < 3 Gbp) when compared with most other free-living dinoflagellates. Different strains of Symbiodiniaceae form symbiosis with distinct hosts and exhibit different regimes of gene expression, but intraspecific whole-genome divergence is poorly understood. Focusing on three Symbiodiniaceae species (the free-living Effrenium voratum and the symbiotic Symbiodinium microadriaticum and Durusdinium trenchii) and the free-living outgroup P. glacialis, for which whole-genome data from multiple isolates are available, we assessed intraspecific genomic divergence with respect to sequence and structure. Our analysis, based on alignment and alignment-free methods, revealed a greater extent of intraspecific sequence divergence in Symbiodiniaceae than in P. glacialis. Our results underscore the role of gene duplication in generating functional innovation, with a greater prevalence of tandemly duplicated single-exon genes observed in the genomes of free-living species than in symbionts. These results demonstrate the remarkable intraspecific genomic divergence in dinoflagellates under the constraint of reduced genome sizes, shaped by genetic duplications and symbiogenesis events during the diversification of Symbiodiniaceae.

Dinoflagellates of the family Symbiodiniaceae are predominantly essential symbionts of corals and other marine organisms. Recent research reveals extensive genome sequence divergence among Symbiodiniaceae taxa and high phylogenetic diversity hidden behind subtly different cell morphologies. Using an alignment-free phylogenetic approach based on sub-sequences of fixed length k (i.e. k-mers), we assessed the phylogenetic signal among whole-genome sequences from 16 Symbiodiniaceae taxa (including the genera of Symbiodinium, Breviolum, Cladocopium, Durusdinium and Fugacium) and two strains of Polarella glacialis as outgroup. Based on phylogenetic trees inferred from k-mers in distinct genomic regions (i.e. repeat-masked genome sequences, protein-coding sequences, introns and repeats) and in protein sequences, the phylogenetic signal associated with protein-coding DNA and the encoded amino acids is largely consistent with the Symbiodiniaceae phylogeny based on established markers, such as large subunit rRNA. The other genome sequences (introns and repeats) exhibit distinct phylogenetic signals, supporting the expected differential evolutionary pressure acting on these regions. Our analysis of conserved core k-mers revealed the prevalence of conserved k-mers (>95% core 23-mers among all 18 genomes) in annotated repeats and non-genic regions of the genomes. We observed 180 distinct repeat types that are significantly enriched in genomes of the symbiotic versus free-living Symbiodinium taxa, suggesting an enhanced activity of transposable elements linked to the symbiotic lifestyle. We provide evidence that representation of alignment-free phylogenies as dynamic networks enhances the ability to generate new hypotheses about genome evolution in Symbiodiniaceae. These results demonstrate the potential of alignment-free phylogenetic methods as a scalable approach for inferring comprehensive, unbiased whole-genome phylogenies of dinoflagellates and more broadly of microbial eukaryotes.

Coral-dwelling gall crabs (Cryptochiridae) are obligate symbionts of stony corals and occur on shallow and deep reefs across the tropical belt. The circumtropical genus Opecarcinus associates with Agariciidae corals, a dominant component of Mesophotic Coral Ecosystems (MCEs). Here, we report the first Red Sea mesophotic record, with 89 m as the deepest record to date, for Opecarcinus—collected from Leptoseris cf mycetoseroides—from the NEOM marine area in Saudi Arabia. This observation reconfirms the depth range flexibility of Opecarcinus species and highlights the need for further mesophotic explorations of reef-associated fauna.

Background: Large-scale coral bleaching events have become increasingly frequent in recent years. This process occurs when corals are exposed to high temperatures and intense light stress, leading to an overproduction of reactive oxygen species (ROS) by their endosymbiotic dinoflagellates. The ROS buildup prompts corals to expel these symbiotic microalgae, resulting in the corals' discoloration. Reducing ROS production and enhancing detoxification processes in these microalgae are crucial to prevent the collapse of coral reef ecosystems. However, research into the cell physiology and genetics of coral symbiotic dinoflagellates has been hindered by challenges associated with cloning these microalgae. Results: A procedure for cloning coral symbiotic dinoflagellates was developed in this study. Several species of coral symbionts were successfully cloned, with two of them further characterized. Experiments with the two species isolated from Turbinaria sp. showed that damage from light intensity at 340 μmol photons/m2/s was more severe than from high temperature at 36 °C. Additionally, preincubation in high salinity conditions activated their endogenous tolerance to bleaching stress. Pretreatment at 50 ppt salinity reduced the percentage of cells stained for ROS by 59% and 64% in the two species under bleaching stress compared to those incubated at 30 ppt. Furthermore, their Fv'/Fm' during the recovery period showed a significant improvement compared to the controls. Conclusions: These findings suggest that intense light plays a more important role than high temperatures in coral bleaching by enhancing ROS generation in the symbiotic dinoflagellates. The findings also suggest the genomes of coral symbiotic dinoflagellates have undergone evolutionary processes to develop mechanisms, regulated by gene expression, to mitigate damages caused by high temperature and high light stress. Understanding this gene expression regulation could contribute to strengthening corals' resilience against the impact of global climate change. [ABSTRACT FROM AUTHOR]

Symbiont genotype plays a vital role in the ability of a coral host to tolerate rising ocean temperatures, with some members of the family Symbiodiniaceae possessing more thermal tolerance than others. While existing studies on genetic structure in symbiont populations have focused on broader scales of 10–100 s of km, there is a noticeable gap in understanding the seascape genetics of coral symbionts at finer—yet ecologically and evolutionarily relevant—scales. Here, we mapped short reads from 271 holobiont genome libraries of individual Acropora hyacinthus colonies to protein coding genes from the chloroplast genome to identify patterns of symbiont population genetic structure. Utilizing this low‐pass method, we assayed over 13,000 bases from every individual, enabling us to discern genetic variation at a finer geographic scale than previously reported at the population level. We identified five common Cladocopium chloroplast SNP profiles present across Palau, with symbiont structure varying between Northern, mid‐lagoon, and Southern regions, and inshore–offshore gradients. Although symbiont populations within reefs typically contained significant genetic diversity, we also observed genetic structure between some nearby reefs. To explore whether coral hosts retain their symbionts post‐transplantation, we experimentally moved 79 corals from their native reefs to transplant sites with both different and similar chloroplast SNP profiles. Over 12 months, we observed 12 instances where transplanted corals changed profiles, often transitioning to a profile present in adjacent corals. Symbiont genetic structure between reefs suggests either low dispersal of symbionts or environmental selection against dispersers, both resulting in the potential for significant adaptive differentiation across reef environments. The extent to which local corals and their symbionts are co‐adapted to environments on a reef‐by‐reef scale is currently poorly known. Chloroplast sequences offer an additional tool for monitoring symbiont genetics and coral–symbiont interactions when assisted migration is used in restoration. [ABSTRACT FROM AUTHOR]

Modern microbial taxonomy generally relies on the use of single marker genes or sets of concatenated genes to generate a framework for the delineation and classification of organisms at different taxonomic levels. However, given that DNA is the 'blueprint of life', and hence the ultimate arbiter of taxonomy, classification systems should attempt to use as much of the blueprint as possible to capture a comprehensive phylogenetic signal. Recent analysis of whole-genome sequences from coral reef symbionts (dinoflagellates of the family Symbiodiniaceae) and other microalgal groups has uncovered extensive divergence not recognised by current algal taxonomic approaches. In the era of 'sequence everything', we argue that whole-genome data are pivotal to guide informed taxonomic inference, particularly for microbial eukaryotes. Whole-genome sequences are increasingly used as molecular evidence for classifying microbial lineages. Dinoflagellate microalgae of the family Symbiodiniaceae are critical symbionts in coral reefs. Recent studies of symbiodiniacean whole-genome sequences reveal extensive divergence and phylogenetic diversity hidden behind subtly different morphology. Divergence of whole-genome sequences can be used to inform taxonomic classification of microbial eukaryotes. Alignment-free methods capture comprehensive, more-informative phylogenetic signal from whole-genome sequences, compared to phylogenetic analysis using conventional marker genes. [ABSTRACT FROM AUTHOR]

The Symbiodiniaceae have been coral symbionts for over 200 million years, yet they retain a facultative lifestyle because both the symbiotic and free-living stages offer unique selective advantages that ensure persistence of the algal lineage. There exists a dynamic competition and interaction between the coral host and algal symbionts that ensures survival of both under fluctuating environmental conditions. If algal symbiont-derived redox stress does not explain coral host bleaching, then it is possible that either or both partners generate a chemical cue that precipitates algal expulsion independent of malfunctions in their electron transport chains. We propose the 'stepping-stone model' as an explanation for the long-term and successful association between coral animals and their facultative algal symbionts, which in a stepwise manner creates novel Symbiodiniaceae lineages worldwide. The photosynthetic symbionts of corals sustain biodiverse reefs in nutrient-poor, tropical waters. Recent genomic data illuminate the evolution of coral symbionts under genome size constraints and suggest that retention of the facultative lifestyle, widespread among these algae, confers a selective advantage when compared with a strict symbiotic existence. We posit that the coral symbiosis is analogous to a 'bioreactor' that selects winner genotypes and allows them to rise to high numbers in a sheltered habitat prior to release by the coral host. Our observations lead to a novel hypothesis, the 'stepping-stone model', which predicts that local adaptation under both the symbiotic and free-living stages, in a stepwise fashion, accelerates coral alga diversity and the origin of endemic strains and species. [ABSTRACT FROM AUTHOR]

Outbreaks of crown-of-thorn starfish (COTS) have caused dramatic declines in reefs through predation on corals, but the post-bloom effects of COTS may still potentially threaten the environment and living organisms due to massive organic decomposition. This stimulation experiment showed that the decomposition of COTS debris triggered an extra mineralization process and resulted in acidifying, hypoxic, and eutrophic seawater. Consequently, the photosynthetic efficiency of coral symbionts decreased by 83%, and coral bleached after removing the stress within two days, then the coral skeleton dissolved at rates of 0.02–0.05 mg cm−2 day−1. Within two weeks, the photosynthesis and growth of benthic algae were suppressed by 27–86% and 1.5–16%, respectively. The mortality of turf algae and coralline algae indicated compromised primary productivity and limited coral recruitment, respectively. However, macroalgae, as coral competitors, became the only survivors, with increasing chlorophyll content. This study suggests a continuing decline of reefs during the collapse phase of COTS outbreaks and highlights the need for improving control strategies for the COTS population. [ABSTRACT FROM AUTHOR]

Coral symbionts are important members of the coral holobiont, and coral bacterial flora are essential in host health maintenance and coral conservation. Coral symbionts are affected by various environmental factors, such as seawater temperature, pH, and salinity. Although physicochemical and chemical factors have been highlighted as possible causes of these effects, the effects of water flow and the co-culture of different species corals have not been elucidated. In this study, we designed an artificial rearing environment to examine the impact of environmental and biological factors on Acropora tenuis, one of the major coral species in Okinawa, and Montipora digitata, during their co-culture. We intervened with the water flow to reveal that the movement of the rearing environment alters the bacterial flora of A. tenuis. During the rearing under captive environment, the alpha diversity of the coral microbiota increased, suggesting the establishment of rare bacteria from the ocean. No differences in the bacterial composition between the control and water flow groups were observed under the rearing conditions. However, the structure of the bacterial flora was significantly different in the co-culture group. Comparison of bacterial community succession strongly suggested that the differences observed were due to the suppressed transmission of bacteria from the ocean in the co-culture group. These results enhance our understanding of interactions between corals and shed light on the importance of regional differences and bacterial composition of coral flora. [ABSTRACT FROM AUTHOR]

The heat tolerance of corals is largely determined by their microbial photosymbionts, and manipulating these symbiont communities may enhance the ability of corals to survive summer heatwaves. Experimental evolution of Symbiodiniaceae cultures under elevated temperatures has been successfully used to enhance the upper thermal tolerance of both symbiont cultures in vitro and corals following inoculation. Novel culturing, upscaling, and biodiversity monitoring techniques are required to deliver experimentally evolved coral symbionts at scale, and success requires learning from, or directly utilising, adjacent industries (e.g., biotechnology for algae-based commodities). This intervention has transitioned from stakeholder engagement to regulatory approval for risk assessments via small-scale field trials, which is an essential step on the path to implementation. The heat tolerance of corals is largely determined by their microbial photosymbionts (Symbiodiniaceae, colloquially known as zooxanthellae). Therefore, manipulating symbiont communities may enhance the ability of corals to survive summer heatwaves. Although heat-tolerant and -sensitive symbiont species occur in nature, even corals that harbour naturally tolerant symbionts have been observed to bleach during summer heatwaves. Experimental evolution (i.e., laboratory selection) of Symbiodiniaceae cultures under elevated temperatures has been successfully used to enhance their upper thermal tolerance, both in vitro and, in some instances, following their reintroduction into corals. In this review, we present the state of this intervention and its potential role within coral reef restoration, and discuss the next critical steps required to bridge the gap to implementation. [ABSTRACT FROM AUTHOR]

Coral's susceptibility to bleaching is determined by the strength of the intricate mutual relationships among coral symbionts. However, there is limited knowledge about how the symbiotic members of the scleractinian coral Echinopora gemmacea respond to changes in their surrounding environmental conditions. In this study, we conducted a survey of seawater characteristics in the south and north zones of Wuzhizhou (WZZ) Island, measured symbiotic microalgal density and chlorophyll-a content in the corals, and performed metabarcoding of the Symbiodiniaceae and bacteria communities within coral tissue. Our findings demonstrated that the seawater in the north zone of WZZ Island had higher levels of turbidity, temperature, salinity, and dissolved oxygen content compared to the south zone. This indicated that the corals in the two zones were subjected to distinctive environmental conditions. Analysis of the Symbiodiniaceae composition revealed that Cladocopium sp. C1 and Cladocopium sp. C17 were the dominant species in the southern E. gemmacea, whereas Durusdinium sp. D1a and Cladocopium sp. C17 prevailed in the northern E. gemmacea. Consequently, symbiotic microalgal density and chlorophyll-a content were diminished in the northern E. gemmacea. Furthermore, correlation network analysis revealed the presence of intricate bacterial interactions that potentially mediate coral's adaptation to environmental stress. This study provides insights into the differences in symbiotic members, including Symbiodiniaceae and bacteria, within E. gemmacea, and contributes to fundamental knowledge for coral conservation efforts. [ABSTRACT FROM AUTHOR]

SUMMARY: The total pool of coral lipids consists of lipids produced by both the coral host and its symbiotic dinoflagellates of the family Symbiodiniaceae. Betaine lipids (BL) are characteristic of plasma membranes of microalgae. Composition of such BL as 1,2‐diacylglyceryl‐3‐O‐carboxy‐(hydroxymethyl)‐choline (DGCC) that occur in coral symbionts may depend on either Symbiodiniaceae species or coral species. Membrane‐forming lipids DGCC have a zwitterion structure similar to that of phosphatidylcholine (PC). They can substitute for each other to a substantial extent, certainly in relation to membrane functions. In the present study, the profiles of DGCC and diacyl PC molecular species of symbiotic dinoflagellates from Acropora sp., Millepora platyphylla and Sinularia flexibilis were determined by high‐performance liquid chromatography with high‐resolution mass‐spectrometry. Colonies of Acropora sp. were characterized by higher contents of DGCC with eicosapentaenoic acid (20:5n‐3) and C28 polyunsaturated fatty acids; S. flexibilis, by a higher content of DGCC with palmitic acid (16:0); and M. platyphylla, by a higher content of DGCC with docosahexaenoic acid (22:6n‐3). Although the DGCC profile of the corals under study has distinctive features, it shows both similarities with and differences from the DGCC profiles of previously studied corals. Probably, each coral symbiont species has its own specific DGCC molecular species profile that is additionally modified in a certain way depending on environmental conditions created by the coral host. Molecular species DGCC and PC profiles were different. The most abundant PC molecular species were 16:0/22:5 and 38:4 in Acropora sp.; 39:5 and 38:4 in S. flexibilis; and 38:6, 16:0/22:5 and 18:0/22:6 in M. platyphylla. Thus, there is no clear evidence for any compensation or interchangeability between PC and DGCC. [ABSTRACT FROM AUTHOR]

Global warming is causing the loss of coral symbionts and their bleaching. Researches of coral recovery are very important for the conservation of coral reefs. The lipidomic approach can provide detailed information about the processes that take place in the coral during bleaching and recovery. Using supercritical fluid chromatography coupled with mass spectrometry, the dynamics of the main classes of storage lipids, triacylglycerols (TG) and monoalkyldiacylglycerols (MADAG), during the recovery of the octocoral Sinularia heterospiculata after heat stress (32°C) was examined. It was shown that MADAG plays a key role in the energy balance of S. heterospiculata after heat stress. Under stress, the coral S. heterospiculata primarily consumed saturated MADAG molecular species. Changes in the profile of TG molecular species occurred only on day 16 of the experiment. Probably, the stressed octocoral S. heterospiculata changes its energy strategy during recovery; therefore, the qualitative composition of storage lipids is rearranged during the recovery period. [ABSTRACT FROM AUTHOR]

Coral reef fauna is imperiled by the loss of coral cover due to increased mass bleaching. However, few studies have focused on the immediate effects of bleaching on the closely coral-associated fauna. Here, we investigated the impact of a coral bleaching event due to abnormally cold waters in the Gulf of California on Pocillopora-associated fauna. We focused on the cryptobenthic reef fishes (CRFs) and crustacean coral symbionts that are likely the most sensitive to habitat degradation because of their poor mobility. We found that a moderate bleaching event (~ 50% of Pocillopora cover) did not affect the occurrence of crustaceans. In contrast, bleaching was significantly associated with a decrease in CRFs numbers, particularly for the non-gobiids, revealing a shift in assemblage composition. Our study highlights that the CRFs, essential for reef functioning, are very sensitive to early signs of habitat alteration. [ABSTRACT FROM AUTHOR]

Coral reefs in Sanya Bay have been degrading in recent decades under climate change and human activities. To identify physiological changes of scleractinian corals and corresponding influencing factors, aquatic environmental factors and physiological parameters of Pocillopora damicornis, Porites pukoensis and their symbiotic zooxanthellae were examined in four Sanya Bay coral reef areas in December 2020 (winter) and July 2021 (summer). The density and chlorophyll a+c2 content of the symbiotic zooxanthellae were significantly high in winter and low in summer. Superoxide dismutase and caspase3 activities of corals and zooxanthellae were high in summer and low in winter, whereas catalase activity showed the opposite pattern. The variations were consistent for both coral symbionts. Water temperature and salinity were the main factors affecting the physiological variations of corals. Compared with winter, the high temperature/low salinity aquatic environment in summer reduced the density and chlorophyll a+c2 content of zooxanthellae, resulting in high superoxide dismutase and caspase3 activities in the corals and zooxanthellae. In addition, turbidity was an important factor affecting the physiological characteristics of coral–zooxanthellae symbionts among the four coral reef areas. Our results have important implications for understanding the changes in coral reef communities in Sanya Bay and coral reef protection. [ABSTRACT FROM AUTHOR]

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. A study part of the Tara Pacific Expedition that surveyed newly sequenced and publicly available metagenomes and genomes revealed pervasive non-retroviral dinoflagellate-infecting endogenous +ssRNA viral elements within coral symbionts. [ABSTRACT FROM AUTHOR]

Context: Primary production on coral reefs varies under changing conditions such as light and nutrient availability. This variation causes changes in basal stable isotopes as photosynthetic and nutrient pathways change. Aims: This study provides a preliminary baseline of nitrogen (δ15N) and carbon (δ13C) stable isotope profiles in Symbiodinium and macroalgae at a spatial scale and along a depth gradient around an island. Methods: Coral fragments and macroalgae were collected at depths from the surface to 26 m. δ15N and δ13C stable isotope values were assessed for Symbiodinium relative to cell density per surface area. Key results: δ15N values showed a uniform nutrient profile across primary producers. However, chlorophyll- a and Symbiodinium density from Montipora stellata had higher concentrations on the southern side of the island. δ15N values of Symbiodinium from Stylophora pistillata and macroalgae did not change with depth. Depth was associated with a significant decrease in Symbiodinium density, and δ13C values in macroalgae. Conclusions: We attribute these findings to Symbiodinium from S. pistillata as depth increases, decreasing cell density but maintaining chlorophyll- a concentration to satisfy the coral-host nutrient requirements. Implications: This study sets the scene for future, more comprehensive research on detecting carbon and nitrogen stable isotope values on primary producers in coral reefs. This study assessed nutrient variations in coral, coral symbionts and algae in relation to depth using nitrogen (δ15N) and carbon (δ13C) stable isotope analysis. Depth was associated with a decrease in symbiont density and δ13C in macroalgae. δ15N did not change with depth for corals, symbionts or macroalgae. We propose that the symbionts may be compensating for nutrient changes associated with depth to satisfy the coral–host requirements. [ABSTRACT FROM AUTHOR]

Corals provide an important habitat for diverse fauna. The habitat is especially rich in branching species. Each colony harbors several species and dozens of individuals, forming an integrated symbiotic community. Factors affecting the diversity and abundance of coral symbionts are poorly understood. The present study tested experimentally the relationship between the population density of coral Pocillopora verrucosa and the diversity and abundance of symbionts in planted coral fragments exposed for three months. Colony size and bleaching were also considered as two additional factors. We demonstrated that, even at the early stage of colony formation, the diversity of obligate symbionts on planted corals in Nha Trang Bay was higher than the diversity of any other studied local faunas of the world's ocean. Species richness and the abundance of symbionts were positively related to colony size and density, while no impact of bleaching was found. Species richness and the abundance of obligate symbionts increased with host population density, while in facultative symbionts, these indices decreased. We hypothesized that the negative effect of host population density on species richness and the abundance of facultative symbionts is caused by the competitive pressure of obligates, which increases with their abundance. The reasons for the different responses of obligate and facultative symbionts to host density were considered. [ABSTRACT FROM AUTHOR]

We explicitly tested for spatial changes in Pocillopora damicornis -associated invertebrates across several spatial scales in the southern Mexican Pacific. Sorting of invertebrates from 40 coral heads along 882 km of the coast yielded 325 taxa, 283% more than any other Pocillopora spp. coral host study to date, but estimators signals that richness might be 17–39% larger than the current number. Permutation, ordination, and regression analysis indicate that the composition and abundance of invertebrates vary in response to the spatial distance among coral heads: high similarity and variation occur among coral heads within localities (<500 m), probably related to faunal homogenization, but progressively modest reduction in similarity and variation as spatial distance increases suggesting a weak role for environmental sorting across southern Mexican Pacific coral reefs. Future studies should explicitly explore spatial, environmental, and historical biogeography processes that regulate and maintain community structure and biodiversity on eastern Pacific reefs. [Display omitted] • Pocillopora harbors at least 283% more invertebrate species than previously thought. • Coral-associated fauna varies in response to the spatial distance among coral heads. • Demography, interactions and chance drive invertebrate changes within coral heads. • Weak role for environmental variability across southern Mexican Pacific coral reefs. [ABSTRACT FROM AUTHOR]

Matthew Nitschke grows coral symbionts in a slowly warming tank to prepare reef life for climate change. [ABSTRACT FROM AUTHOR]

"Bacteria-zooxanthellae-coral" is a pair of typical triangular relationships in the marine ecosystem. There are complex flows of material, information, and energy in this system. The balance and stability of the symbionts is an important guarantee for maintaining the health of coral reef ecosystems. Many studies have been conducted on the interaction of coral symbionts in the past 20 years, which help clarify the material metabolism and nutrient exchange between "bacteria-zooxanthellae-coral" and their interaction with the environment. Due to the complexity of this symbiotic system, the mechanisms of some phenomena are still not well understood, especially for the communication among the symbionts. The interaction mediated by signal molecules is the internal driving force for the homeostatic maintenance and efficient operation of coral symbionts. In this review, we tried to summarize the latest research progress by focusing on the chemical signaling molecules in coral symbiotic system, including the communications between the bacteria and bacteria, bacteria and corals, bacteria and zooxanthellae, and zooxanthellae and corals. The main signals molecules include quorum sensing (QS) molecules, dimethylsulfoniopropionate (DMSP), glycans signals, lipid signals, and the noncoding RNAs. We focused on the functional mode and ecological significance of signal molecules in symbionts, and selectively exemplified microbial cooperation and competition mediated by QS signals, the interaction between bacteria and corals under the regulation of DMSP, and the response process of corals and zooxanthellae to noncoding RNAs under environmental stresses. We proposed the future research focus and possible directions, including the expansion of research dimensions, the application of new technologies and new methods, and the construction of ecological models. This work would help improve the understanding of interactions between " bacteria-zooxanthellae-coral ". The exploration about the ways based on communication language would provide new ideas for the restoration and protection of coral reef ecosystems. [ABSTRACT FROM AUTHOR]

Scleractinian corals provide habitats for a broad variety of cryptofauna, which in turn may contribute to the overall functioning of coral symbiomes. Among these invertebrates, hydrozoans belonging to the genus Zanclea represent an increasingly known and ecologically important group of coral symbionts. In this study, we analysed 321 Zanclea colonies associated with 31 coral genera collected from 11 localities across the Indo-Pacific and Caribbean regions, and used a multi-disciplinary approach to shed light on the evolution and biogeography of the group. Overall, we found high genetic diversity of hydrozoans that spans nine clades corresponding to cryptic or pseudo-cryptic species. All but two clades are associated with one or two coral genera belonging to the Complex clade, whereas the remaining ones are generalists associated with both Complex and Robust corals. Despite the observed specificity patterns, no congruence between Zanclea and coral phylogenies was observed, suggesting a lack of coevolutionary events. Most Zanclea clades have a wide distribution across the Indo-Pacific, including a generalist group extending also into the Caribbean, while two host-specific clades are possibly found exclusively in the Red Sea, confirming the importance of this peripheral region as an endemicity hotspot. Ancestral state reconstruction suggests that the most recent common ancestor of all extant coral-associated Zanclea was a specialist species with a perisarc, occurring in what is now known as the Indo-Pacific. Ultimately, a mixture of geography- and host-related diversification processes is likely responsible for the observed enigmatic phylogenetic structure of coral-associated Zanclea. [ABSTRACT FROM AUTHOR]

[Display omitted] • Corals support coral reef biodiversity by acting as hosts for symbionts. • Four major taxa of coral parasites were compared for their host specificity. • Totals of 203 coral-associated invertebrates and 335 host coral species were recorded. • Coral barnacles and gall crabs are more host-specific than serpulids and date mussels. • Coral symbionts in the Indo-Pacific are more host-specific than those in the Atlantic region. Coral-associated fauna predominantly consists of invertebrates and constitutes an important component of coral reef biodiversity. The symbionts depend on their hosts for food, shelter and substrate. They may act as parasites by feeding on their hosts, by overgowing their polyps, or by excavating their skeletons. Because some of these species partly reside inside their hosts, they may be cryptic and can easily be overlooked in biodiversity surveys. Since no quantitative overview is available about these inter-specific relationships, this present study adresses variation in host ranges and specificity across four large coral-associated taxa and between the Atlantic and Indo-Pacific oceans. These taxa are: coral barnacles (Pyrgomatidae, n = 95), coral gall crabs (Cryptochiridae, n = 54), tubeworms (Serpulidae, n = 31), and date mussels (Lithophaginae, n = 23). A total of 335 host coral species was recorded. An index of host specificity (S TD) was calculated per symbiont species, based on distinctness in taxonomic host range levels (species, genus, family, etc.). Mean indices were statistically compared among the four associated taxa and the two oceanic coral reef regions. Barnacles were the most host-specific, tubeworms the least. Indo-Pacific associates were approximately 10 times richer in species and two times more host-specific than their Atlantic counterparts. Coral families varied in the number of associates, with some hosting none. This variation could be linked to host traits (coral growth form, maximum host size) and is most probably also a result of the evolutionary history of the interspecific relationships. [ABSTRACT FROM AUTHOR]

This article presents a synthesis of information about the massive oil spill in Brazil (2019/2020). The event affected 11 states; however, the majority of the oil residue was collected (~ 5380 tons) near nine states (99.8%) in northeastern Brazil. This spill was not the largest in volume (between 5000 m3 and 12,000 m3) recorded in tropical oceans, but it was the most extensive (2890 km). This spill develops an overwashed tar that remains mostly in the undersurface drift (non-floating oil plume) below 17 m of depth while on the continental shelf. Ten ecosystems were impacted, with potentially more severe effects in mangroves and seagrasses. Certain negative effects are still understudied, such as effects on tropical reefs and rhodolith beds. A total of 57 protected areas in seven management categories were affected, most of which (60%) were characterized as multiple-use regions. The spill affected at least 34 threatened species, with impacts detected on plankton and benthic communities. Acute impacts were reported on echinoderms, coral symbionts, polychaetes, and sponges with evidence of oil ingestion. Socioeconomic impacts were detected in food security, public health, lodging, gender equality, tourism, and fishing, with reduced sales, prices, tourist attractiveness, gross domestic product, and employment. Moreover, chemical contamination was detected in some states by toxic metals (Hg, As, Cd, Pb, and Zn) and polycyclic aromatic hydrocarbons (acenaphthalene, fluoranthene, fluorene, naphthalene, and phenanthrene). This summary aims to aid in the design of science-based strategies to understand the impacts and develop strategies for the most extensive spill observed in tropical oceans. [ABSTRACT FROM AUTHOR]

This document is an editorial published in Frontiers in Microbiology titled "Women in microbial symbioses: 2022/2023." The editorial highlights the need to address gender imbalances in STEM fields and focuses on the contributions of women in the study of symbiotic relationships with microorganisms. It discusses various research topics related to microbial symbiosis, including the effects of global warming on coral symbionts, the impact of microbiome disturbance on host gene expression in jellyfish, the presence of viruses in bacterial genomes in the rhizosphere, and the composition of the vaginal microbiota in females. The editorial emphasizes the importance of understanding these relationships for human health and medical treatments. [Extracted from the article]

Heat stress and other factors cause the loss of endosymbiotic dinoflagellates by corals, and is known as coral bleaching. Coral reef bleaching is a global environmental problem. To better understand corals' responses and adaptability to stressful conditions, we applied a lipidomic approach in combination with cytometry and microscopy to study the coral bleaching of Acropora aspera under heat stress (32 °C) and subsequent recovery. For eight days of bleaching, the coral lost 50% of its symbiont population and 100% after a week of recovery. It took 126 days to fully recover the symbiont population, content of chlorophyll a and reserve lipids. There were degradations in symbionts' thylakoids and disruption of thylakoid lipid homeostasis. Variations in the content of phosphatidylinositols involved in apoptosis and autophagy and changes in the molecular profile of glycosylceramides that may be involved in the sphingosine rheostat were observed. However, upon A. aspera bleaching, the loss of symbionts was compensated by increased mucociliary nutrition. An increase in the content of hydroxylated ceramideaminoethylphosphonates for membrane stabilization and a decrease in ether phosphatidylethanolamines for providing protection from oxidative stress may have been used as adaptation mechanisms by the coral host. Thus, the coral undergoes physiological and biochemical changes during heat stress that are aimed at mitigating the adverse destructive effects, which may be key to successful recovery. [ABSTRACT FROM AUTHOR]

The marine microbiome arouses an increasing interest, aimed at better understanding coral reef biodiversity, coral resilience, and identifying bioindicators of ecosystem health. The present study is a microbiome mining of three environmentally contrasted sites along the Hermitage fringing reef of La Réunion Island (Western Indian Ocean). This mining aims to identify bioindicators of reef health to assist managers in preserving the fringing reefs of La Réunion. The watersheds of the fringing reefs are small, steeply sloped, and are impacted by human activities with significant land use changes and hydrological modifications along the coast and up to mid-altitudes. Sediment, seawater, and coral rubble were sampled in austral summer and winter at each site. For each compartment, bacterial, fungal, microalgal, and protist communities were characterized by high throughput DNA sequencing methodology. Results show that the reef microbiome composition varied greatly with seasons and reef compartments, but variations were different among targeted markers. No significant variation among sites was observed. Relevant bioindicators were highlighted per taxonomic groups such as the Firmicutes:Bacteroidota ratio (8.4%:7.0%), the genera Vibrio (25.2%) and Photobacterium (12.5%) dominating bacteria; the Ascomycota:Basidiomycota ratio (63.1%:36.1%), the genera Aspergillus (40.9%) and Cladosporium (16.2%) dominating fungi; the genus Ostreobium (81.5%) in Chlorophyta taxon for microalgae; and the groups of Dinoflagellata (63.3%) and Diatomea (22.6%) within the protista comprising two dominant genera: Symbiodinium (41.7%) and Pelagodinium (27.8%). This study highlights that the identified bioindicators, mainly in seawater and sediment reef compartments, could be targeted by reef conservation stakeholders to better monitor La Réunion Island's reef state of health and to improve management plans. [ABSTRACT FROM AUTHOR]

Identifying processes that promote coral reef recovery and resilience is crucial as ocean warming becomes more frequent and severe. Sexual reproduction is essential for the replenishment of coral populations and maintenance of genetic diversity; however, the ability for corals to reproduce may be impaired by marine heatwaves that cause coral bleaching. In 2014 and 2015, the Hawaiian Islands experienced coral bleaching with differential bleaching susceptibility in the species Montipora capitata, a dominant reef-building coral in the region. We tested the hypothesis that coral bleaching resistance enhances reproductive capacity and offspring performance by examining the reproductive biology of colonies that bleached and recovered (B) and colonies that did not bleach (NB) in 2015 in the subsequent spawning seasons. The proportion of colonies that spawned was higher in 2016 than in 2017. Regardless of parental bleaching history, we found eggs with higher abnormality and bundles with fewer eggs in 2016 than 2017. While reproductive output was similar between B and NB colonies in 2016, survivorship of offspring that year were significantly influenced by the parental bleaching history (egg donor × sperm donor: B × B, B × NB, NB × B, and NB × NB). Offspring produced by NB egg donors had the highest survivorship, while offspring from previously bleached colonies had the lowest survivorship, highlighting the negative effects of bleaching on parental investment and offspring performance. While sexual reproduction continues in M. capitata post-bleaching, gametes are differentially impacted by recovery time following a bleaching event and by parental bleaching resistance. Our results demonstrate the importance of identifying bleaching resistant individuals during and after heating events. This study further highlights the significance of maternal effects through potential egg provisioning for offspring survivorship and provides a baseline for human-assisted intervention (i.e., selective breeding) to mitigate the effects of climate change on coral reefs. [ABSTRACT FROM AUTHOR]

Background: Evolutionary tradeoffs between life-history strategies are important in animal evolution. Because microbes can influence multiple aspects of host physiology, including growth rate and susceptibility to disease or stress, changes in animal-microbial symbioses have the potential to mediate life-history tradeoffs. Scleractinian corals provide a biodiverse, data-rich, and ecologically-relevant host system to explore this idea. Results: Using a comparative approach, we tested if coral microbiomes correlate with disease susceptibility across 425 million years of coral evolution by conducting a cross-species coral microbiome survey (the "Global Coral Microbiome Project") and combining the results with long-term global disease prevalence and coral trait data. Interpreting these data in their phylogenetic context, we show that microbial dominance predicts disease susceptibility, and traced this dominance-disease association to a single putatively beneficial symbiont genus, Endozoicomonas. Endozoicomonas relative abundance in coral tissue explained 30% of variation in disease susceptibility and 60% of variation in microbiome dominance across 40 coral genera, while also correlating strongly with high growth rates. Conclusions: These results demonstrate that the evolution of Endozoicomonas symbiosis in corals correlates with both disease prevalence and growth rate, and suggest a mediating role. Exploration of the mechanistic basis for these findings will be important for our understanding of how microbial symbioses influence animal life-history tradeoffs. [ABSTRACT FROM AUTHOR]

Marine heatwaves are starting to occur several times a decade, yet we do not understand the effect this has on corals across biological scales. This study combines tissue-, organism-, and community-level analyses to investigate the effects of a marine heatwave on reef-building corals. Adjacent conspecific pairs of coral colonies of Montipora capitata and Porites compressa that showed contrasting phenotypic responses (i.e., bleached vs. not bleached) were first identified during a marine heatwave that occurred in 2015 in Kāne'ohe Bay, Hawai' i. These conspecific pairs of bleaching-resistant and bleaching-susceptible colonies were sampled for histology and photographed before, during, and after a subsequent marine heatwave that occurred in 2019. Histology samples were quantified for: (i) abundance of mesenterial filaments, (ii) tissue structural integrity, (iii) clarity of epidermis, and (iv) cellular integrity (lack of necrosis/granulation) on a 1–5 scale and averaged for an overall tissue integrity score. Tissue integrity scores revealed a significant decline in overall tissue health during the 2019 heatwave relative to the months prior to the heatwave for individuals of both species, regardless of past bleaching history in 2015 or bleaching severity during the 2019 heatwave. Coral tissue integrity scores were then compared to concurrent colony bleaching severity, which revealed that tissue integrity was significantly correlated with colony bleaching severity and suggests that the stability of the symbiosis is related to host tissue health. Colony partial mortality was also quantified as the cumulative proportion of each colony that appeared dead 2.5 years following the 2019 bleaching event, and tissue integrity during the heatwave was found to be strongly predictive of the extent of partial mortality following the heatwave for M. capitata but not P. compressa, the latter of which suffered little to no mortality. Surprisingly, bleaching severity and partial mortality were not significantly correlated for either species, suggesting that tissue integrity was a better predictor of mortality than bleaching severity in M. capitata. Despite negative effects of heat stress at the tissue- and colony-level, no significant changes in coral cover were detected, indicating resilience at the community level. However, declines in tissue integrity in response to heat stress that are not accompanied by a visible bleaching response may still have long-term consequences for fitness, and this is an important area of future investigation as heat stress is commonly associated with long-term decreases in coral fecundity and growth. Our results suggest that histology is a valuable tool for revealing the harmful effects of marine heatwaves on corals before they are visually evident as bleaching, and may thus improve the predictability of ecosystem changes following climate change-driven heat stress by providing a more comprehensive assessment of coral health. [ABSTRACT FROM AUTHOR]

Dinoflagellates are a diverse and ecologically important group of single-celled eukaryotes. Many are photosynthetic autotrophs while others are predatory, parasitic, or symbiotic. One major group — the Symbiodiniaceae — is well known for its role as coral symbionts that provide the coral host with vital nutrients. While genetic transformation protocols have been published for some non-symbiotic dinoflagellate species, robust methods for genetic manipulation of coral symbionts are lacking, hindering a detailed molecular understanding of this critical symbiotic interaction. Here, we describe the successful transformation of coral symbiont Breviolum minutum (strain SSB01). Using Golden Gate modular plasmid assembly and electroporation, we drove transient NLS-GFP expression from an endogenous dinoflagellate virus nuclear protein (DVNP) promoter and successfully targeted GFP to the dinoflagellate nucleus. We further determined that puromycin can efficiently select transformed cells using the puromycin N-acetyltransferase (pac) resistance gene. Transformed cells could be maintained under antibiotic selection for at least 12 months without losing resistance, albeit with slowly attenuating fluorescence signal. We thus tested the expression of hybrid GFP-2A-PAC polypeptides under the control of a single promoter sequence to overcome loss of fluorescence, but lack of efficient 2A cleavage seemingly hindered antibiotic selection interfering GFP function. Despite this, our transformation approach now allows unanswered questions of dinoflagellate biology to be addressed, as well as fundamental aspects of dinoflagellate-coral symbiosis.

Analysis of bacterial carbohydrate-active enzymes (CAZymes) contributes significantly to comprehending the response exhibited by coral symbionts to the external environment. This study explored the impact of bleaching on the bacteria and their CAZymes in coral Favites sp. through metagenomic sequencing. Notably, principal coordinates analysis (PCoA) unveiles substantial difference in bacterial communities between bleached and unbleached corals. Proteobacteria, Actinobacteria, Acidobacteria, Bacteroidota, and Chloroflexi, exhibit noteworthy alterations during coral bleaching. CAZymes profiles in bleached coral disclosed a significant increase in Glycosyltransferases (GTs) abundance, suggesting an intensified biosynthesis of polysaccharides. Conversely, there is a marked reduction in other CAZymes abundance in bleached coral. Proteobacteria, Bacteroidota, Chlorobi, and Planctomycetota exhibit greater contributions to CAZymes in bleached corals, with Rhodobacterales, Cytophagales, Burkholderiales, Caulobacterales, and Hyphomicrobiales being the main contributors. While Acidobacteria, Actinobacteria, and Chloroflexi demonstrate higher contributions to CAZymes in unbleached corals. The changes in bacteria and their CAZymes reflect the ecological adaptability of coral holobionts when facing environmental stress. The alterations in CAZymes composition caused by bleaching events may have profound impacts on coral nutrient absorption and ecosystem stability. Therefore, understanding the dynamic changes in CAZymes is crucial for assessing the health and recovery potential of coral ecosystems. • Substantial difference in bacterial communities between bleached and unbleached corals. • A significant increase in the abundance of GT in bleached coral. • Marked reduction in the abundance of GH, CE, AA, CBM, and PL in bleached coral. • Proteobacteria, Bacteroidota, Chlorobi, and Planctomycetota exhibit greater contributions to CAZymes in bleached corals. [ABSTRACT FROM AUTHOR]