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Background: Cladocopium infistulum (Symbiodiniaceae) is a dinoflagellate specialized to live in symbiosis with western Pacific giant clams (Tridacnidae). Unlike coral-associated symbionts, which reside within the host cells, C. infistulum inhabits the extracellular spaces of the clam's digestive diverticula. It is phylogenetically basal to a large species complex of stress-tolerant Cladocopium, many of which are associated with important reef-building corals in the genus Porites. This close phylogenetic relationship may explain why C. infistulum exhibits high thermotolerance relative to other tridacnid symbionts. Moreover, past analyses of microsatellite loci indicated that Cladocopium underwent whole-genome duplication prior to the adaptive radiations that led to its present diversity. Results: A draft genome assembly of C. infistulum was produced using long- and short-read sequences to explore the genomic basis for adaptations underlying thermotolerance and extracellular symbiosis among dinoflagellates and to look for evidence of genome duplication. Comparison to three other Cladocopium genomes revealed no obvious over-representation of gene groups or families whose functions would be important for maintaining C. infistulum's unique physiological and ecological properties. Preliminary analyses support the existence of partial or whole-genome duplication among Cladocopium, but additional high-quality genomes are required to substantiate these findings. Conclusion: Although this investigation of Cladocopium infistulum revealed no patterns diagnostic of heat tolerance or extracellular symbiosis in terms of overrepresentation of gene functions or genes under selection, it provided a valuable genomic resource for comparative analyses. It also indicates that ecological divergence among Cladocopium species, and potentially among other dinoflagellates, is partially governed by mechanisms other than gene content. Thus, additional high-quality, multiomic data are needed to explore the molecular basis of key phenotypes among symbiotic microalgae. [ABSTRACT FROM AUTHOR]

In recent years, several studies have highlighted the high resilience of zoantharians to ocean warming. In particular, populations of Palythoa caribaeorum are proliferating and beginning to dominate the coastal ecosystems of the Canary Islands. This expansion has been associated with increasing sea surface temperatures (SSTs). Here, we provide new insights into the endosymbiont-P. caribaeorum associations during and after a heat stress experiment to understand the processes underlying their high resilience to elevated temperatures. For this purpose, 61 colonies collected in the Canary Islands were exposed to an increasing temperature gradient (from 24 to 32 °C) to assess their heat tolerance, and then transferred back to the control temperature (24 °C) to evaluate their resilience. Colonies performance was assessed by comparing host color changes (bleaching degree), analyzing their Symbiodiniaceae morphological condition, and determining the dominant lineage of Symbiodiniaceae using the psbAncr molecular marker. All colonies showed signs of bleaching during heat stress, evidenced by color loss and a decrease in healthy Symbiodiniaceae content. Nevertheless, P. caribaeorum showed high resistance to heat stress, as all colonies kept up to 30 °C were able to survive and significantly recover. Furthermore, as the experimental temperature increased, a new haplotype of the Cladocopium C1 lineage, not detected in the control and wild samples, emerged and dominated most of the colonies (59.09%). Our study demonstrates the resilience of P. caribaeorum to heat stress in the Canary Islands, raising important ecological concerns about the future of native macroalgae ecosystems in an ocean warming scenario. [ABSTRACT FROM AUTHOR]

Summary: Coral thermal bleaching resilience can be improved by enhancing photosymbiont thermal tolerance via experimental evolution. While successful for some strains, selection under stable temperatures was ineffective at increasing the thermal threshold of an already thermo‐tolerant photosymbiont (Durusdinium trenchii). Corals from environments with fluctuating temperatures tend to have comparatively high heat tolerance. Therefore, we investigated whether exposure to temperature oscillations can raise the upper thermal limit of D. trenchii.We exposed a D. trenchii strain to stable and fluctuating temperature profiles, which varied in oscillation frequency. After 2.1 yr (54–73 generations), we characterised the adaptive responses under the various experimental evolution treatments by constructing thermal performance curves of growth from 21 to 31°C for the heat‐evolved and wild‐type lineages. Additionally, the accumulation of extracellular reactive oxygen species, photophysiology, photosynthesis and respiration rates were assessed under increasing temperatures.Of the fluctuating temperature profiles investigated, selection under the most frequent oscillations (diurnal) induced the greatest widening of D. trenchii's thermal niche. Continuous selection under elevated temperatures induced the only increase in thermal optimum and a degree of generalism.Our findings demonstrate how differing levels of thermal homogeneity during selection drive unique adaptive responses to heat in a coral photosymbiont. [ABSTRACT FROM AUTHOR]

Guanosine Triphosphate (GTP)ases of Immunity Associated Proteins (GIMAP) are small G proteins that in vertebrates, regulate immunity, apoptosis, and autophagy. While previously thought to be limited to vertebrates and plants, this family of proteins was recently characterized in a diversity of dinoflagellates. However, information regarding the function of GIMAPs in dinoflagellates is lacking. Therefore, the goal of this study (conducted from March-November of 2022) was to assess the expression of GIMAPs in the cnidarian symbiont Breviolum minutum (formerly Symbiodinium minutum, referred to as Bm_GIMAPs) in response to low light (25 vs 8 μmol m−2 s−1 for 9 d), thermal stress (22 vs 28 °C for 48 h), and symbiotic state (cultured vs in hospite). These factors were selected due to their importance in the lifestyle of a photosynthetic symbiont and relevance to the ecologically important issue of coral bleaching. The results indicate Bm_GIMAP expression increased under both low light and elevated temperature, suggesting a role in the response to bleaching related stressors. Cultured B. minutum had lower baseline Bm_GIMAP expression than those in association with a cnidarian host, but a stronger response to thermal stress, suggesting their function is influenced by symbiosis. Lastly, further support for the responsiveness of GIMAPs to thermal stress was provided by a comparison with previously published RNA-seq data from cultured Symbiodiniaceae. Collectively, the results presented here represent the first functional investigation of GIMAPs in an ecologically important group of protists and provide a greater understanding of the molecular response of dinoflagellates to stressors related to bleaching. [ABSTRACT FROM AUTHOR]

The growth properties and environmental adaptability of different corals and symbionts vary. Therefore, insights from the adaptive mechanisms of Symbiodiniaceae in corals are very meaningful. In this study, we surveyed the seawater characteristics at three sites on Luhuitou fringing reef, Hainan Island (China), sampling three native corals Pocillopora damicornis, Acropora hyacinthus, and Galaxea fascicularis on 27 September 2021. The photo-physiological (Fv/Fm, Y(II), α, and rETR) were measured, and high-throughput sequencing of Symbiodiniaceae ITS was performed. The Luhuitou site had the lowest temperature (28.845 °C ± 0.01), salinity (33.967 ± 0.03), and pH (8.468 ± 0.05) among the three sites. The Sanya site contained significantly the highest ammonium (7.406 μmol/L ± 1, P < 0.05). The nitrate of the Xiaozhou site was 1.5 times significantly higher than the other two sites. Three corals and their Symbiodiniaceae were adapted differently. P. damicornis showed more plasticity and was dominant by Cladocopium sp. C1d at high-ammonium habitat. A. hyacinthus was dominated by Cladocopium (C3 and C1232) and they had the lowest Fv/Fm (0.595 ± 0.02) in poor integrated water quality environments (the Xiaozhou site) among three corals, suggesting that the less adaptation. G. fascicularis established a stable symbiotic relationship with Durusidinium sp. D1, and they had a more stable symbiotic system and were better suited for long-term reef restoration. Our results provide a deeper understanding of the environmental adaptations of three corals at the Luhuitou fringing reef. Meanwhile, it provides a perspective application for coral transplantation species selection in restoring local reef ecology in the future. [ABSTRACT FROM AUTHOR]

The aquaculture industry requires green solutions to solve several environmental challenges, including adequate wastewater remediation and natural drug applications to treat bacteria- and virus-related diseases. This study investigated the feasibility of cultivating the dinoflagellate Durusdinium glynnii in aquaculture wastewater from shrimp rearing in a synbiotic system (AWW-SS), with different dilutions of f/2 medium (FM). Interestingly, D. glynnii demonstrated enhanced growth in all AWW–SS treatments compared to the control (FM). The highest growth rates were achieved at AWW-SS:FM dilutions of 75:25 and 50:50. The removal of total nitrogen and total phosphorus reached 50.1 and 71.7%, respectively, of the crude AWW–SS. Biomass extracts of D. glynnii grown with AWW–SS were able to inhibit the growth of the bacteria Vibrio parahaemolyticus (inhibition zone of 10.0 ± 1.7 mm) and V. vulnificus (inhibition zone of 11.7 ± 1.5 mm). The presented results demonstrate that the dinoflagellate D. glynnii is a potential candidate for the development of circularity for sustainable aquaculture production, particularly by producing anti–Vibrio compounds at a near-zero cost. [ABSTRACT FROM AUTHOR]

Thermal stress triggers the breakdown of the obligate symbiosis between the cnidarian coral host and its autotrophic dinoflagellates of the family Symbiodiniaceae. This diverse family exhibits pronounced functional variation that has large implications for the survival of their coral host. In this study, we explored patterns of symbiont community composition and diversity in the coral Turbinaria reniformis, a turbid reef specialist, along a latitudinal and environmental gradient in Western Australia. Using metabarcoding of the internal transcribed spacer region 2, we explored symbiont community patterns, their environmental drivers, and potential associations with host genetic structure. Our findings reveal a predominance of Cladocopium across our study area, with distinct regional composition influenced primarily by sea surface temperature. Geographical distance and host genetic data did not align with symbiont community divergence, suggesting a complex interplay of environmental and genetic factors t shaping the community structure. This study underscores Cladocopium stability in Western Australia across large distances and strong environmental gradients. It also highlights the highly diversified lineage community that may explain T. reniformis ability to thrive in a wide range of environmental conditions. [ABSTRACT FROM AUTHOR]

Global warming can inhibit chlorophyll-based solar energy capturing of phytoplankton by decreasing nutrient supply through upwelling. However, species with proton-pump rhodopsin (PPR) can independently convert solar energy to cope with nutrient limitation. Besides prokaryotes, PPR has been documented in dinoflagellates and some species of other algal lineages, and its potential role in compensating for the deficiency of phosphorus has been demonstrated in dinoflagellates. However, PPR has not been studied in the coral reef endosymbiotic Symbiodiniaceae. Here, we report a PPR in Breviolum minutum (BmR). Both phylogenetic analysis and structure prediction results indicate that BmR resembles eukaryotic proton-pump rhodopsins, phylogenetically affiliated with the subgroup xanthorhodopsins. BmR contains the critical residues for proton pumping, retinal binding, and spectrum tuning for green absorption. To explore BmR's potential roles in responding to phosphorus limitation, we cultured B. minutum under different phosphorus conditions, and monitored physiological and BmR's transcriptional responses. Phosphorus limitation caused decreases in B. minutum population growth and photosynthesis efficiency. Meanwhile, our quantitative PCR showed that BmR expression was strongly upregulated under phosphorus limitation, showing a strong positive correlation with alkaline phosphatase activity and a negative correlation with photosynthetic efficiency. Our findings demonstrate that proton-pump rhodopsin occurs in Symbiodiniaceae and BmR has the potential to provide supplementary energy to support cell basal metabolisms when photosynthesis of B. minutum is impaired by phosphorus limitation, thereby enabling corals to better weather climate change. [ABSTRACT FROM AUTHOR]

The ecological success of shallow water corals hinges on their association with photosynthetic Symbiodiniaceae algae. This is affected by environmental drivers among which sea temperature is pivotal. In 2016, a prolonged heat wave challenged New Caledonia reefs triggering a severe bleaching event. Here, we tracked 72 coral colonies comprising two species of Pocillopora and Porites from a cross-shelf gradient during the event and subsequent recovery period. Symbiodiniaceae association over time was assessed using the ITS2 marker. Bleaching prevalence and photosynthetic efficiency showed that 83% of Pocillopora and 29% of Porites colonies were affected, with corals from a mid-shelf site having been most impacted. The majority of tracked colonies recovered by December 2016, with a recorded 33% mortality of Pocillopora, while Porites showed higher resilience. Consistent with previous studies, genotyping data suggest stable, species- and site-specific associations between corals and Symbiodiniaceae. [ABSTRACT FROM AUTHOR]

Symbiotic dinoflagellates in the genus Symbiodiniaceae play vital roles in promoting resilience and increasing stress tolerance in their coral hosts. While much of the world's coral succumb to the stresses associated with increasingly severe and frequent thermal bleaching events, live coral cover in Papua New Guinea (PNG) remains some of the highest reported globally despite the historically warm waters surrounding the country. Yet, in spite of the high coral cover in PNG and the acknowledged roles Symbiodiniaceae play within their hosts, these communities have not been characterized in this global biodiversity hotspot. Using high-throughput sequencing of the ITS2 rDNA gene, we profiled the endosymbionts of four coral species, Diploastrea heliopora, Pachyseris speciosa, Pocillopora acuta, and Porites lutea, across six sites in PNG. Our findings reveal patterns of Cladocopium and Durusdinium dominance similar to other reefs in the Coral Triangle, albeit with much greater intra- and intergenomic variation. Host- and site-specific variations in Symbiodiniaceae type profiles were observed across collection sites, appearing to be driven by environmental conditions. Notably, the extensive intra- and intergenomic variation, coupled with many previously unreported sequences, highlight PNG as a potential hotspot of symbiont diversity. This work represents the first characterization of the coral-symbiont community structure in the PNG marine biodiversity hotspot, serving as a baseline for future studies. [ABSTRACT FROM AUTHOR]

The thermal tolerance of symbiodiniacean photo-endosymbionts largely underpins the thermal bleaching resilience of their cnidarian hosts such as corals and the coral model Exaiptasia diaphana. While variation in thermal tolerance between species is well documented, variation between conspecific strains is understudied. We compared the thermal tolerance of three closely related strains of Breviolum minutum represented by two internal transcribed spacer region 2 profiles (one strain B1–B1o–B1g–B1p and the other two strains B1–B1a–B1b–B1g) and differences in photochemical and non-photochemical quenching, de-epoxidation state of photopigments, and accumulation of reactive oxygen species under rapid short-term cumulative temperature stress (26–40 °C). We found that B. minutum strains employ distinct photoprotective strategies, resulting in different upper thermal tolerances. We provide evidence for previously unknown interdependencies between thermal tolerance traits and photoprotective mechanisms that include a delicate balancing of excitation energy and its dissipation through fast relaxing and state transition components of non-photochemical quenching. The more thermally tolerant B. minutum strain (B1–B1o–B1g–B1p) exhibited an enhanced de-epoxidation that is strongly linked to the thylakoid membrane melting point and possibly membrane rigidification minimizing oxidative damage. This study provides an in-depth understanding of photoprotective mechanisms underpinning thermal tolerance in closely related strains of B. minutum. [ABSTRACT FROM AUTHOR]

Thermal stress causes the overproduction and toxic accumulation of reactive oxygen species (ROS), which seems to be correlated with coral bleaching and, ultimately, death. The reduction of ROS concentration within the coral holobiont could minimize the effects of thermal stress and support efforts to reduce coral decline globally. In the current study, we explored the physiological responses of Pocillopora damicornis to ROS-scavenging bacteria inoculation as well as the microbiome restructuring that correlates with P. damicornis's resilience to thermal stress after probiotic inoculation. Inoculation of corals with ROS-scavenging bacteria enhanced coral health and reduced ROS concentration. Furthermore, the enhanced coral thermal resistance promoted by ROS-scavenging bacteria was also correlated with an overall coral microbiome restructuring. In addition, the complex network relationships between bacteria and Symbiodiniaceae in corals after ROS-scavenging bacteria inoculation contributed to corals' resilience to high temperatures. Besides, coral heat tolerance bacterial biomarkers, such as Myxococcota, were enriched in corals with added ROS-scavenging bacteria. Collectively, our findings validate the selected ROS-scavenging bacteria as coral probiotics that could help corals resist thermal stress on a short timescale. Additionally, our data contribute to our understanding of the potential interactions between different members of the coral holobiont and the use of probiotics as tools to aid coral restoration efforts. [ABSTRACT FROM AUTHOR]

Sedimentation is a major cause of global near-shore coral reef decline. Although the negative impacts of sedimentation on coral reef community composition have been well-documented, the effects of sedimentation on coral metabolism in situ have received comparatively little attention. Using transcriptomics, we identified gene expression patterns changing across a previously defined sedimentation threshold that was deemed critical due to changes in coral cover and community composition. We identified genes, pathways, and molecular processes associated with this transition that may allow corals, such as Porites lobata, to tolerate chronic, severe sedimentation and persist in turbid environments. Alternative energy generation pathways may help P. lobata maintain a persistent stress response to survive when the availability of light and oxygen is diminished. We found evidence for the expression of genes linked to increased environmental sensing and cellular communication that likely allow P. lobata to efficiently respond to sedimentation stress and associated pathogen challenges. Cell damage increases under stress; consequently, we found apoptosis pathways over-represented under severe sedimentation, a likely consequence of damaged cell removal to maintain colony integrity. The results presented here provide a framework for the response of P. lobata to sedimentation stress under field conditions. Testing this framework and its related hypotheses using multi-omics approaches can deepen our understanding of the metabolic plasticity and acclimation potential of corals to sedimentation and their resilience in turbid reef systems. [ABSTRACT FROM AUTHOR]

The intracellular coral–dinoflagellate symbiosis is the engine that underpins the success of coral reefs, one of the most diverse ecosystems on the planet. However, the breakdown of the symbiosis and the loss of the microalgal symbiont (i.e. coral bleaching) due to environmental changes are resulting in the rapid degradation of coral reefs globally. There is an urgent need to understand the cellular physiology of coral bleaching at the mechanistic level to help develop solutions to mitigate the coral reef crisis. Here, at an unprecedented scope, we present novel models that integrate putative mechanisms of coral bleaching within a common framework according to the triggers (initiators of bleaching, e.g. heat, cold, light stress, hypoxia, hyposalinity), cascades (cellular pathways, e.g. photoinhibition, unfolded protein response, nitric oxide), and endpoints (mechanisms of symbiont loss, e.g. apoptosis, necrosis, exocytosis/vomocytosis). The models are supported by direct evidence from cnidarian systems, and indirectly through comparative evolutionary analyses from non‐cnidarian systems. With this approach, new putative mechanisms have been established within and between cascades initiated by different bleaching triggers. In particular, the models provide new insights into the poorly understood connections between bleaching cascades and endpoints and highlight the role of a new mechanism of symbiont loss, i.e. 'symbiolysosomal digestion', which is different from symbiophagy. This review also increases the approachability of bleaching physiology for specialists and non‐specialists by mapping the vast landscape of bleaching mechanisms in an atlas of comprehensible and detailed mechanistic models. We then discuss major knowledge gaps and how future research may improve the understanding of the connections between the diverse cascade of cellular pathways and the mechanisms of symbiont loss (endpoints). [ABSTRACT FROM AUTHOR]

The symbiotic relationship between corals and their associated microorganisms is crucial for the health of coral reef eco-environmental systems. Recently, there has been a growing interest in unraveling how the manipulation of symbiont nutrient cycling affects the stress tolerance in the holobiont of coral reefs. However, most studies have primarily focused on coral–Symbiodiniaceae–bacterial interactions as a whole, neglecting the interactions between Symbiodiniaceae and bacteria, which remain largely unexplored. In this study, we proposed a hypothesis that there exists an inner symbiotic loop of Symbiodiniaceae and bacteria within the coral symbiotic loop. We conducted experiments to demonstrate how metabolic exchanges between Symbiodiniaceae and bacteria facilitate the nutritional supply necessary for cellular growth. It was seen that the beneficial bacterium, Ruegeria sp., supplied a nitrogen source to the Symbiodiniaceae strain Durusdinium sp., allowing this dinoflagellate to thrive in a nitrogen-free medium. The Ruegeria sp.–Durusdinium sp. interaction was confirmed through 15N-stable isotope probing–single cell Raman spectroscopy, in which 15N infiltrated into the bacterial cells for intracellular metabolism, and eventually the labeled nitrogen source was traced within the macromolecules of Symbiodiniaceae cells. The investigation into Symbiodiniaceae loop interactions validates our hypothesis and contributes to a comprehensive understanding of the intricate coral holobiont. These findings have the potential to enhance the health of coral reefs in the face of global climate change. [ABSTRACT FROM AUTHOR]

Coral growth depends on the partnership between the animal hosts and their intracellular, photosynthetic dinoflagellate symbionts. In this study, we used the sea anemone Aiptasia, a laboratory model for coral biology, to investigate the poorly understood mechanisms that mediate symbiosis establishment and maintenance. We found that initial colonization of both adult polyps and larvae by a compatible algal strain was more effective when the algae were able to photosynthesize and that the long-term maintenance of the symbiosis also depended on photosynthesis. In the dark, algal cells were taken up into host gastrodermal cells and not rapidly expelled, but they seemed unable to reproduce and thus were gradually lost. When we used confocal microscopy to examine the interaction of larvae with two algal strains that cannot establish stable symbioses with Aiptasia, it appeared that both pre- and post-phagocytosis mechanisms were involved. With one strain, algae entered the gastric cavity but appeared to be completely excluded from the gastrodermal cells. With the other strain, small numbers of algae entered the gastrodermal cells but appeared unable to proliferate there and were slowly lost upon further incubation. We also asked if the exclusion of either incompatible strain could result simply from their cells' being too large for the host cells to accommodate. However, the size distributions of the compatible and incompatible strains overlapped extensively. Moreover, examination of macerates confirmed earlier reports that individual gastrodermal cells could expand to accommodate multiple algal cells. This article is part of the theme issue 'Sculpting the microbiome: how host factors determine and respond to microbial colonization'. [ABSTRACT FROM AUTHOR]

Black corals (Hexacorallia: Antipatharia) are a major component of mesophotic and deep marine ecosystems. Due to their preference for light deprived environments, black corals have historically been considered azooxanthellate, yet recent works have found them in association with dinoflagellates of the family Symbiodiniaceae down to 396 m depth. While corals and Symbiodiniaceae generally establish a symbiotic relationship in shallow water environments, the implications of this association is less well understood at deeper depths, where low light penetration cannot sustain efficient photosynthetic activity for the algae. However, Symbiodinaceae are not obligate autotrophs, and their capacity for heterotrophic feeding categorizes themas mixotrophs. In this study, we investigated the presence and diversity of Symbiodiniaceae associated with the deep-sea black coral Bathypathes thermophila (Antipatharia: Schizopathidae), collected from 204 to 655 m depth in the Saudi Arabian Red Sea. Using high-throughput sequencing of the ITS2 region, we report (1) the deepest record to date of Symbiodiniaceae associated with an anthozoan from 655 m, and (2) the first Red Sea record of Antipatharia in association with Symbiodiniaceae. Our analyses revealed that 14 out of 27 colonies of B. thermophila were associated with Symbiodiniaceae of the genera Cladocopium and Durusdinium. We unveiled 16 novel ITS2 type profiles, possibly unique to black corals and/or to these depths, along with seven profiles that were already known from shallow-water hard corals. No significant pattern was detected in terms of community diversity in relation to depth or sampling locality. Our study supports the existence of black corals-Symbiodiniaceae association and warrants further research to better understand the evolutionary processes and physiological mechanisms driving this association, specifically in light deprived environments. [ABSTRACT FROM AUTHOR]

ABSTRACT Reef-building corals depend on symbiosis with photosynthetic algae that reside within their cells. As important as this relationship is for maintaining healthy reefs, it is strikingly delicate. When ocean temperatures briefly exceed the average summer maximum, corals can bleach, losing their endosymbionts. Although the mechanisms governing bleaching are unknown, studies implicate uncoupling of coral and algal cell divisions at high temperatures. Still, little is known regarding the coordination of host and algal cell divisions. Control of nutrient exchange is one likely mechanism. Both nitrogen and phosphate are necessary for dividing cells, and although nitrogen enrichment is known to increase symbiont density in the host, the consequences of phosphate enrichment are poorly understood. Here, we examined the effects of phosphate depletion on symbiont growth in culture and compared the physiology of phosphate-starved symbionts in culture to symbionts that were freshly isolated from a host. We found that available phosphate is as low in freshly isolated symbionts as it is in phosphate-starved cultures. Furthermore, RNAseq revealed that phosphate-limited and freshly isolated symbionts have similar patterns of gene expression for phosphate-dependent genes, most notably upregulation of phosphatases, which is consistent with phosphate recycling. Similarly, lipid profiling revealed a substantial decrease in phospholipid abundance in both phosphate-starved cultures and freshly isolated symbionts. These findings are important because they suggest that limited access to phosphate controls algal cell divisions within a host.IMPORTANCEThe corals responsible for building tropical reefs are disappearing at an alarming rate as elevated sea temperatures cause them to bleach and lose the algal symbionts they rely on. Without these symbionts, corals are unable to harvest energy from sunlight and, therefore, struggle to thrive or even survive in the nutrient-poor waters of the tropics. To devise solutions to address the threat to coral reefs, it is necessary to understand the cellular events underpinning the bleaching process. One model for bleaching proposes that heat stress impairs algal photosynthesis and transfer of sugar to the host. Consequently, the host’s demands for nitrogen decrease, increasing nitrogen availability to the symbionts, which leads to an increase in algal proliferation that overwhelms the host. Our work suggests that phosphate may play a similar role to nitrogen in this feedback loop.

Abstract Background Global warming is causing large-scale disruption of cnidarian-Symbiodiniaceae symbioses fundamental to major marine ecosystems, such as coral reefs. However, the mechanisms by which heat stress perturbs these symbiotic partnerships remain poorly understood. In this context, the upside-down jellyfish Cassiopea has emerged as a powerful experimental model system. Results We combined a controlled heat stress experiment with isotope labeling and correlative SEM-NanoSIMS imaging to show that host starvation is a central component in the chain of events that ultimately leads to the collapse of the Cassiopea holobiont. Heat stress caused an increase in catabolic activity and a depletion of carbon reserves in the unfed host, concurrent with a reduction in the supply of photosynthates from its algal symbionts. This state of host starvation was accompanied by pronounced in hospite degradation of algal symbionts, which may be a distinct feature of the heat stress response of Cassiopea. Interestingly, this loss of symbionts by degradation was concealed by body shrinkage of the starving animals, resulting in what could be referred to as “invisible” bleaching. Conclusions Overall, our study highlights the importance of the nutritional status in the heat stress response of the Cassiopea holobiont. Compared with other symbiotic cnidarians, the large mesoglea of Cassiopea, with its structural sugar and protein content, may constitute an energy reservoir capable of delaying starvation. It seems plausible that this anatomical feature at least partly contributes to the relatively high stress tolerance of these animals in rapidly warming oceans. Video Abstract

The thermal bleaching percentage of coral holobionts shows inte rspecific differences under heat-stress conditions, which are closely related to the coral-associated microbiome. However, the ecological effects of community dynamics and interactions between Symbiodiniaceae and fungi on coral thermal bleaching susceptibility remain unclear. In this study, we analyzed the diversity, community structure, functions, and potential interaction of Symbiodiniaceae and fungi among 18 coral species from a high thermal bleaching risk atoll using next-generation sequencing. The results showed that heat-tolerant C3u sub-clade and Durusdinium dominated the Symbiodiniaceae community of corals and that there were no core amplicon sequence variants in the coral-associated fungal community. Fungal richness and the abundance of confirm ed functional animal-plant pathogens were significantly positively correlated with the coral thermal bleaching percentage. Fungal indicators, including Didymellaceae, Chaetomiaceae, Schizophyllum, and Colletotrichum, were identified in corals. Each coral species had a complex Symbiodiniaceae-fungi interaction network (SFIN), which was driven by the dominant Symbiodiniaceae sub-clades. The SFINs of coral holobionts with low thermal bleaching susceptibility exhibited low complexity and high betweenness centrality. These results indicate that the extra heat tolerance of coral in Huangyan Island may be linked to the high abundance of heat-tolerant Symbiodiniaceae. Fungal communities have high interspecific flexibility, and the increase of fungal diversity and pathogen abundance was correlated with higher thermal bleaching susceptibility of corals. Moreover, fungal indicators were associated with the degrees of coral thermal bleaching susceptibility, including both high and intermediate levels. The topological properties of SFINs suggest that heat-tolerant coral have limited fungal parasitism and strong microbial network resilience. IMPORTANCE Global warming and enhanced marine heatwaves have led to a rapid decline in coral reef ecosystems worldwide. Several studies have focused on the impact of coral-associated microbiomes on thermal bleaching susceptibility in corals; however, the ecological functions and interactions between Symbiodiniaceae and fungi remain unclear. We investigated the microbiome dynamics and potential interactions of Symbiodiniaceae and fungi among 18 coral species in Huangyan Island. Our study found that the Symbiodiniaceae community of corals was mainly composed of heattolerant C3u sub-clade and Durusdinium. The increase in fungal diversity and pathogen abundance has close associations with higher coral thermal bleaching susceptibility. We first constructed an interaction network between Symbiodiniaceae and fungi in corals, which indicated that restricting fungal parasitism and strong interaction network resilience would promote heat acclimatization of corals. Accordingly, this study provides insights into the role of microorganisms and their interaction as drivers of inte rspecific differences in coral thermal bleaching. [ABSTRACT FROM AUTHOR]

Reef-building corals are a fundamental pillar of coral reef ecosystems in tropical and subtropical shallow environments. Corals harbor symbiotic dinoflagellates belonging to the family Symbiodiniaceae, commonly known as zooxanthellae. Extensive research has been conducted on this symbiotic relationship, yet the fundamental information about the distribution and localization of Symbiodiniaceae cells in corals is still limited. This information is crucial to understanding the mechanism underlying the metabolite exchange between corals and their algal symbionts, as well as the metabolic flow within holobionts. To examine the distribution of Symbiodiniaceae cells within corals, in this study, we used fluorescence imaging and matrix-assisted laser desorption/ionization (MALDI) mass spectrometry imaging (MS-Imaging) on branches of the Acropora tenuis coral. We successfully prepared frozen sections of the coral for molecular imaging without fixing or decalcifying the coral branches. By combining the results of MS-Imaging with that of the fluorescence imaging, we determined that the algal Symbiodiniaceae symbionts were not only localized in the tentacle and surface region of the coral branches but also inhabited the in inner parts. Therefore, the molecular imaging technique used in this study could be valuable to further investigate the molecular dynamics between corals and their symbionts. [ABSTRACT FROM AUTHOR]

Establishment of the coral–algal symbiosis begins during early ontogeny when juveniles acquire a mix of algae from their environment that often differs from the adults' algal assemblages. Despite the importance of the type of Symbiodiniaceae to this symbiosis, it is largely unknown how coral host identity and environment affect symbiosis establishment and is affected by the genetic composition of the symbionts. Here, we reciprocally transplanted planulae of the octocoral Rhytisma fulvum (Forskål, 1775) across depths and monitored the algal assemblages in the developing juveniles for 11 months. We then compared these to adult assemblages using ITS2 metabarcoding. Juveniles were consistently dominated by Symbiodinium, in addition to multiple Cladocopium species, which shifted in dominance with the juvenile age but maintained high similarity across depths. The type of Symbiodiniaceae environmentally available thus likely contributes to the algal symbionts that are initially acquired, while host identity may play a significant role in selecting for symbionts that are maintained during juvenile development. [ABSTRACT FROM AUTHOR]

Introduction: In the upside-down jellyfish, Cassiopea xamachana (Cnidaria: Scyphozoa), the establishment of photosymbiosis with dinoflagellates (family Symbiodiniaceae) is necessary for the sessile polyp to undergo metamorphosis (strobilation) into a free-swimming adult. C. xamachana has the capacity to associate with a wide variety of dinoflagellate species and representatives of divergent genera. While some studies have looked at the successful induction of symbiosis, none to date have examined the lasting effect of diverse symbiont taxa on host survivorship and development, which is needed to assess the fitness costs of such symbioses. Methods: Our study exposes C. xamachana polyps to 22 different cultured Symbiodinaceae strains representing 13 species from 5 genera. We analyzed the time to strobilation, the number of ephyra (juvenile medusa) produced, and the proportion of ephyra that died prematurely. Results: Here we show that C. xamachana strobilation can be induced by nearly each symbiodinacean strain we tested, with the exception of free-living species (i.e., unknown to establish symbiosis with any other marine host). Additionally, ephyrae did not display morphological variation or survivorship differences with varying symbionts. However, we observed intraspecific variation in time to induce strobilation with different cultured dinoflagellate strains. Discussion: This work expands the known symbiont species that can form stable mutualisms with C. xamachana, primarily in the genera Symbiodinium and Breviolum. Additionally, we provide evidence of differences in ability of cultured symbiodiniaceans to establish symbiosis with a host, which suggests population-level differences in dinoflagellate cultures impact their symbiosis success. By utilizing an animal like C. xamachana with flexible symbiont uptake, we are able to explore how symbiont diversity can influence the timing and success of symbiosis-driven development. [ABSTRACT FROM AUTHOR]

Corals are habitat-forming organisms on tropical and sub-tropical reefs, often displaying diverse phenotypic behaviors that challenge field-based monitoring and assessment efforts. Symbiont chlorophyll (Chl) is a long-recognized indicator of intra- and inter-specific variation in coral's response to environmental variability and stress, but the quantitative Chl assessment of corals at the reef scale continues to prove challenging. We integrated field, airborne, and laboratory techniques to test and apply the use of reflectance spectroscopy for in situ and reef-scale estimation of Chl a and Chl c2 concentrations in a shallow reef environment of Kāne'ohe Bay, O'ahu. High-fidelity spectral signatures (420–660 nm) derived from field and airborne spectroscopy quantified Chl a and Chl c2 concentrations with demonstrable precision and accuracy. Airborne imaging spectroscopy revealed a 10-fold range of Chl concentrations across the reef ecosystem. We discovered a differential pattern of Chl a and Chl c2 use in symbiont algae in coexisting corals indicative of a physiological response to decreasing light levels with increasing water depth. The depth-dependent ratio of Chl c2:a indicated the presence of two distinct light-driven habitats spanning just 5 m of water depth range. Our findings provide a pathway for further study of coral pigment responses to environmental conditions using field and high-resolution airborne imaging spectroscopy. [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]

Microalgae, small photosynthetic unicells, are of great interest to ecology, ecotoxicology and biotechnology and there is a growing need to investigate the ability of cells to photosynthesize under variable conditions. Current strategies involve handoperated pulse-amplitude-modulated (PAM) chlorophyll fluorimeters, which can provide detailed insights into the photophysiology of entire populations- or individual cells of microalgae but are typically limited in their throughput. To increase the throughput of a commercially available MICROSCOPY-PAM system, we present the PAM Automation Control Manager (‘PACMan’), an open-source Python software package that automates image acquisition, microscopy stage control and the triggering of external hardware components. PACMan comes with a user-friendly graphical user interface and is released together with a stand-alone tool (PAMalysis) for the automated calculation of per-cell maximum quantum efficiencies (= Fv/Fm). Using these two software packages, we successfully tracked the photophysiology of >1000 individual cells of green algae (Chlamydomonas reinhardtii) and dinoflagellates (genus Symbiodiniaceae) within custom-made microfluidic devices. Compared to the manual operation of MICROSCOPY-PAM systems, this represents a 10-fold increase in throughput. During experiments, PACMan coordinated the movement of the microscope stage and triggered the MICROSCOPY-PAM system to repeatedly capture high-quality image data across multiple positions. Finally, we analyzed single-cell Fv/Fm with the manufacturer-supplied software and PAMalysis, demonstrating a median difference <0.5% between both methods. We foresee that PACMan, and its auxiliary software package will help increase the experimental throughput in a range of microalgae studies currently relying on hand-operated MICROSCOPY-PAM technologies. [ABSTRACT FROM AUTHOR]

Background: Global warming is causing large-scale disruption of cnidarian-Symbiodiniaceae symbioses fundamental to major marine ecosystems, such as coral reefs. However, the mechanisms by which heat stress perturbs these symbiotic partnerships remain poorly understood. In this context, the upside-down jellyfish Cassiopea has emerged as a powerful experimental model system. Results: We combined a controlled heat stress experiment with isotope labeling and correlative SEM-NanoSIMS imaging to show that host starvation is a central component in the chain of events that ultimately leads to the collapse of the Cassiopea holobiont. Heat stress caused an increase in catabolic activity and a depletion of carbon reserves in the unfed host, concurrent with a reduction in the supply of photosynthates from its algal symbionts. This state of host starvation was accompanied by pronounced in hospite degradation of algal symbionts, which may be a distinct feature of the heat stress response of Cassiopea. Interestingly, this loss of symbionts by degradation was concealed by body shrinkage of the starving animals, resulting in what could be referred to as “invisible” bleaching. Conclusions: Overall, our study highlights the importance of the nutritional status in the heat stress response of the Cassiopea holobiont. Compared with other symbiotic cnidarians, the large mesoglea of Cassiopea, with its structural sugar and protein content, may constitute an energy reservoir capable of delaying starvation. It seems plausible that this anatomical feature at least partly contributes to the relatively high stress tolerance of these animals in rapidly warming oceans. 7jQYTVpxtJyVhU5epTFb61 Video Abstract [ABSTRACT FROM AUTHOR]

This article discusses the use of the model organism Aiptasia in coral symbiosis research. Coral reefs are facing global decline, and understanding the interactions between corals and their microbial symbionts is crucial for their survival. Aiptasia, a small sea anemone, has been adopted as a model system for studying cnidarian symbiosis. Researchers have made progress in studying various aspects of Aiptasia, but there are still challenges to overcome. The article highlights recent studies on algal density, genetic tools, and bacterial communities associated with Aiptasia, contributing to our understanding of coral-dinoflagellate symbiosis and coral reef conservation. The document is a list of references cited in an article about the symbiotic relationship between cnidarians and dinoflagellates, covering various topics related to this symbiosis. The references provide a comprehensive overview of current research in this field and can be used as a starting point for further investigation. [Extracted from the article]

Stony coral tissue loss disease (SCTLD) has spread throughout the entirety of Florida's Coral Reef (FCR) and across the Caribbean, impacting at least 30 coral species. The threatened hermatypic coral, Orbicella faveolata, demonstrates intraspecific variation in SCTLD affectedness with some colonies experiencing chronic disease lesions, while other nearby O. faveolata colonies appear unaffected with no disease signs over long monitoring periods. This study evaluated potential genotypic underpinnings of variable disease responses to SCTLD by monitoring and sampling 90 O. faveolata colonies from southeast Florida and the lower Florida Keys. High resolution analyses of >11,000 single nucleotide polymorphisms (SNPs) generated from 2bRAD sequencing indicated there were no SNP loci or genetic lineages significantly associated with O. faveolata SCTLD affectedness. Genotypic differences may still contribute to SCTLD susceptibility; however, these differences were not captured using this reduced representation sequencing approach. Algal symbiont community structure characterized from 2bRAD data revealed that the presence of Durusdinium spp. corresponded with SCTLD-affected colonies as compared to unaffected colonies, suggesting that algal symbiont community make-up may play some role in SCTLD resistance. Data generated by this study will be combined with complementary molecular and physiological approaches to further investigate the complex drivers of intraspecific SCTLD susceptibility and resilience. [ABSTRACT FROM AUTHOR]

The mitigation of coral bleaching requires adaptation of its endosymbionts to rising ocean temperatures, acidity, and ultra-violet radiation. While genetic transformation may offer a means for enhancing endosymbiont resilience to these environmental stressors, the opportunity for doing so in dinoflagellates is likely hampered, in part, by their armored cortex, which may present a formidable barrier to intracellular delivery. Here, using Breviolum minutum (Clade B Symbiodiniaceae) as a model, we show that this barrier may be moderated by first disrupting the outer plasma membrane with the detergent octyl β-D-glucopyranoside, followed by enzymatic digestion of the underlying cellulose with Cellulase RS and Macerozyme R-10. Treatment using this new protocol results in 61% reduction in calcofluor-based cell wall staining (i.e., 25% staining for protocol vs. 64% for control), thus demonstrating the ability for considerable cell wall digestion. Furthermore, protoplasts isolated thereby exhibit rapid cell wall recovery, as well as comparable PSII activity and cell growth as the control, thus suggesting that the protocol minimally affects acute- and long-term cellular function. Finally, the isolated protoplasts also show a potentially slight increase in permeability to a model exogenous cargo after electroporation with a non-optimized protocol. Collectively, this constitutes the first known successful generation of viable B. minutum protoplasts, and thus, serves as a foundation for future studies seeking to lower the barrier for transformation of these and possibly other Symbiodiniaceae. [ABSTRACT FROM AUTHOR]

Human-induced climate change is causing ocean warming that triggers the breakdown of the coral–algal symbiosis. The proximate cause of this phenomenon, known as coral bleaching, is commonly attributed to the overproduction of reactive oxygen species (ROS) by the thermally stressed photosynthetic algal symbionts. However, direct evidence that algal ROS production (e.g., in the form of H2O2) and coral physiological stress are the ultimate cause of bleaching remains ambiguous. Here, we investigated the temporal dynamics of H2O2 and oxygen (O2) concentrations during thermally induced coral bleaching to disentangle cause from consequence. Microsensors at the tissue interface of Pocillopora damicornis measured H2O2 and O2 concentrations while exposing single nubbins to baseline temperatures (30 °C) and to minor (33 °C), moderate (36 °C), and high (39 °C) levels of acute heat stress using the Coral Bleaching Automated Stress System (CBASS). We show that a temporary decline in O2 concentration, accompanied by a declining photosynthetic efficiency and loss of Symbiodiniaceae and pigmentation, is the initial response to moderate thermal stress. This response was neither provoked nor followed by an increased H2O2 concentration at the coral tissue interface. A steady light-independent increase of H2O2 was only detected during high heat stress, resulting in the complete and permanent loss of photosynthetic activity. Our findings do not support a direct connection between algal photodamage and an increase in H2O2 concentration during thermally induced bleaching and suggest that more research on the function of H2O2 is warranted. This notion is further substantiated by the observation of an additional source of H2O2, likely oxidative bursts, that were common at the baseline temperature and under minor heat stress, while their occurrence decreased at moderate and high heat stress. Resolving the multifaceted and dynamic roles of H2O2 in coral bleaching is critical to better understand the response of the coral holobiont to thermal stress and identifying the processes underlying the breakdown of the coral–algal symbiosis. [ABSTRACT FROM AUTHOR]

Phenotypic plasticity is defined as a property of individual genotypes to produce different phenotypes when exposed to different environmental conditions. This ability may be expressed at behavioral, biochemical, physiological, and/or developmental levels, exerting direct influence over species' demographic performance. In reef-building corals, a group critically threatened by global change in the Anthropocene, non-genetic mechanisms (i.e., epigenetic and microbiome variation) have been shown to participate in plastic physiological responses to environmental change. Yet, the precise way in which these mechanisms interact, contribute to such responses, and their adaptive potential is still obscure. The present work aims to fill this gap by using a multi-omics approach to elucidate the contribution and interconnection of the mechanisms modulating phenotypic plasticity in staghorn coral (Acropora cervicornis) clones subject to different depth conditions. Results show changes in lipidome, epigenome and transcriptome, but not in symbiotic and microbial communities. In addition, a potential shift toward a more heterotrophic feeding behavior was evidenced in corals at the deeper site. These observations are consistent with a multi-mechanism modulation of rapid acclimation in corals, underscoring the complexity of this process and the importance of a multifactorial approach to inform potential intervention to enhance coral adaptive capacity. [ABSTRACT FROM AUTHOR]

The aquaculture industry requires green solutions to solve several environmental challenges, including adequate wastewater remediation and natural drug applications to treat bacteria- and virus-related diseases. This study investigated the feasibility of cultivating the dinoflagellate Durusdinium glynnii in aquaculture wastewater from shrimp rearing in a synbiotic system (AWW-SS), with different dilutions of f/2 medium (FM). Interestingly, D. glynnii demonstrated enhanced growth in all AWW–SS treatments compared to the control (FM). The highest growth rates were achieved at AWW-SS:FM dilutions of 75:25 and 50:50. The removal of total nitrogen and total phosphorus reached 50.1 and 71.7%, respectively, of the crude AWW–SS. Biomass extracts of D. glynnii grown with AWW–SS were able to inhibit the growth of the bacteria Vibrio parahaemolyticus (inhibition zone of 10.0 ± 1.7 mm) and V. vulnificus (inhibition zone of 11.7 ± 1.5 mm). The presented results demonstrate that the dinoflagellate D. glynnii is a potential candidate for the development of circularity for sustainable aquaculture production, particularly by producing anti–Vibrio compounds at a near-zero cost.

Unlocking how coral endosymbionts (Symbiodiniaceae) regulate the susceptibility of corals to thermal stress-induced bleaching has been the focus of experimental heat stress studies on laboratory-maintained isolates for over 30 years. Multiple protocols to induce heat stress have been used, but the extent to which data can be reconciled across protocols remains unknown. We therefore first analysed past published heat stress studies on Symbiodiniaceae (Jan 1980–Jan 2023) to identify the range of protocols (ramping rate derived from time taken to reach the target heat stress temperatures from the initial ambient temperature, time retained under the target heat stress temperature, etc.) commonly used for experimentation. Temperature differences between ambient and maximum experimental temperatures spanned from 3 °C to 17 °C (mean = 6.8 °C), and only 41% of all studies reported a ramping rate, ranging from instantaneous to 0.02 °C/h (mean = 0.62 °C/h). Experiment length at the treatment temperature varied from < 24 h to > 2 months. We next experimentally quantified if the rate of heating impacted the observed physiological outcome for three Symbiodiniaceae taxa with differences in heat tolerance—Durusdinium trenchii, Breviolum psygmophilum and Breviolum minutum. Five experimental treatments were performed with different temperature ramping rates from 26 °C to 32 °C: 1 °C/1 h, 1 °C/12 h, 1 °C/1 d, 1 °C/2 d and 1 °C/3 d, spanning relatively acute to chronic. Changes in physiology were quantified daily as the maximum photochemical efficiency (Fv/Fm). Heating commonly induced decreases in Fv/Fm, and the change between the start and end of experiment (∆Fv/Fm) linearly increased with ramping rates. Our data suggests that slower ramping exacerbates thermal stress, though with varying magnitude across taxa as B. minutum, and D. trenchii proved less resilient than B. pysgmophilum. We discuss how these outcomes potentially impact the capacity to integrate biological responses observed from past experiments and highlights the need for more standardised experimental protocols. [ABSTRACT FROM AUTHOR]

Typical (peridinin-containing) dinoflagellates possess plastid genomes composed of small plasmids named "minicircles". Despite the ecological importance of dinoflagellate photosynthesis in corals and marine ecosystems, the structural characteristics, replication dynamics, and evolutionary forcing of dinoflagellate plastid genomes remain poorly understood. Here, we sequenced the plastid genome of the symbiodiniacean species Fugacium kawagutii and conducted comparative analyses. We identified psbT -coding minicircles, features previously not found in Symbiodiniaceae. The copy number of F. kawagutii minicircles showed a strong diel dynamics, changing between 3.89 and 34.3 copies/cell and peaking in mid-light period. We found that F. kawagutii minicircles are the shortest among all dinoflagellates examined to date. Besides, the core regions of the minicircles are highly conserved within genus in Symbiodiniaceae. Furthermore, the codon usage bias of the plastid genomes in Heterocapsaceae, Amphidiniaceae, and Prorocentraceae species are greatly influenced by selection pressure, and in Pyrocystaceae, Symbiodiniaceae, Peridiniaceae, and Ceratiaceae species are influenced by both natural selection pressure and mutation pressure, indicating a family-level distinction in codon usage evolution in dinoflagellates. Phylogenetic analysis using 12 plastid-encoded proteins and five nucleus-encoded plastid proteins revealed accelerated evolution trend of both plastid- and nucleus-encoded plastid proteins in peridinin- and fucoxanthin-dinoflagellate plastids compared to plastid proteins of nondinoflagellate algae. These findings shed new light on the structure and evolution of plastid genomes in dinoflagellates, which will facilitate further studies on the evolutionary forcing and function of the diverse dinoflagellate plastids. The accelerated evolution documented here suggests plastid-encoded sequences are potentially useful for resolving closely related dinoflagellates. [ABSTRACT FROM AUTHOR]

Coral-associated dinoflagellates (Symbiodiniaceae) are photosynthetic endosymbionts that influence coral acclimation, as indicated by photo-endosymbiotic phenotypic variance across different environmental conditions. Symbiont shuffling (shifts in endosymbiont community composition), changes in endosymbiont cell density, and cellular plasticity have all been proposed as acclimation mechanisms. However, few studies have been able to partition which of the three strategies were responsible for observed phenotypic variance. Using a combination of metabarcoding and flow cytometry, we simultaneously characterized Acropora pulchra-associated Symbiodiniaceae assemblages at the community, population, and individual level under natural environmental conditions to deduce whether seasonal phenotypic change and site-related phenotypic variation of Symbiodiniaceae assemblages is a product of symbiont shuffling or cellular plasticity. Symbiodiniaceae assemblages displayed season-specific phenotypic variance, while Symbiodiniaceae community composition was geographically structured and cell density showed limited data structure. Based on these patterns, we reveal that cellular plasticity of Symbiodiniaceae was the source of a phenotypic variation, thus indicating that cellular plasticity is a mechanism for acclimation to mild environmental change. [ABSTRACT FROM AUTHOR]

Ocean warming has caused coral mass bleaching and mortality worldwide and the persistence of symbiotic reef‐building corals requires rapid acclimation or adaptation. Experimental evolution of the coral's microalgal symbionts followed by their introduction into coral is one potential method to enhance coral thermotolerance. Heat‐evolved microalgal symbionts of the generalist species, Cladocopium proliferum (strain SS8), were exposed to elevated temperature (31°C) for ~10 years, and were introduced into four genotypes of chemically bleached adult fragments of the scleractinian coral, Galaxea fascicularis. Two of the four coral genotypes acquired SS8. The new symbionts persisted for the 5 months of the experiment and enhanced adult coral thermotolerance, compared with corals that were inoculated with the wild‐type C. proliferum strain. Thermotolerance of SS8‐corals was similar to that of coral fragments from the same colony hosting the homologous symbiont, Durusdinium sp., which is naturally heat tolerant. However, SS8‐coral fragments exhibited faster growth and recovered cell density and photochemical efficiency more quickly following chemical bleaching and inoculation under ambient temperature relative to Durusdinium‐corals. Mass spectrometry imaging suggests that algal pigments involved in photobiology and oxidative stress were the greatest contributors to the thermotolerance differences between coral hosting heat‐evolved versus wild‐type C. proliferum. These pigments may have increased photoprotection in the heat‐evolved symbionts. This is the first laboratory study to show that thermotolerance of adult corals (G. fascicularis) can be enhanced via the uptake of exogenously supplied, heat‐evolved symbionts, without a trade‐off against growth under ambient temperature. Importantly, heat‐evolved C. proliferum remained in the corals in moderate abundance 2 years after first inoculation, suggesting long‐term stability of this novel symbiosis and potential long‐term benefits to coral thermotolerance. [ABSTRACT FROM AUTHOR]

Coral reefs thrive in the oligotrophic ocean and rely on symbiotic algae to acquire nutrients. Global warming is projected to intensify surface ocean nutrient deficiency and anthropogenic discharge of wastes with high nitrogen (N): phosphorus (P) ratios can exacerbate P nutrient limitation. However, our understanding on how symbiotic algae cope with P deficiency is limited. Here, we investigated the responses of a coral symbiotic species of Symbiodiniaceae, Cladocopium goreaui, to P‐limitation by examining its physiological performance and transcriptomic profile. Under P stress, C. goreaui exhibited decreases in algal growth, photosynthetic efficiency, and cellular P content but enhancement in carbon fixation, N assimilation, N:P ratio, and energy metabolism, with downregulated expression of carbohydrate exporter genes. Besides, C. goreaui showed flexible mechanisms of utilizing different dissolved organic phosphorus to relieve P deficiency. When provided glycerol phosphate, C. goreaui hydrolyzed it extracellularly to produce phosphate for uptake. When grown on phytate, in contrast, C. goreaui upregulated the endocytosis pathway while no dissolved inorganic phosphorus was released into the medium, suggesting that phytate was transported into the cell, potentially via the endocytosis pathway. This study sheds light on the survival strategies of C. goreaui and potential weakening of its role as an organic carbon supplier in P‐limited environments, underscoring the importance of more systematic investigation on future projections of such effects. [ABSTRACT FROM AUTHOR]

Corals' endosymbiotic algae (Symbiodiniaceae) supply much of the energetic demands of the host, and some symbionts, such as Durusdinium spp., may confer higher thermal tolerance than others. However, there may be physiological tradeoffs during non-bleaching periods or across environmental gradients. The common Hawaiian reef-building coral, Montipora capitata, hosts the symbionts Cladocopium C31 and/or Durusdinium glynnii. Here, we measured growth of these holobionts over two months to test whether the higher heat tolerance of D. glynnii involved a tradeoff of lower growth, which could impact survivorship and competition for space on the reef. Additionally, we tested whether any such tradeoffs were modulated by light, which is a major driver of the ecological distribution of these symbionts in Kāneʻohe Bay. During the first month, when water temperatures were warmer (median 25.5 °C), there was no effect of symbiont on growth. However, over the cooler second month (median 23.4 °C), C31-dominated corals grew up to 77% faster than D. glynnii-dominated corals, and this growth advantage increased in higher light treatments (up to a daily light integral of 3.8 mol m−2 d−1, corresponding to 3.8–6.4 m depth). This advantage may explain why C31-dominated colonies are more prevalent at most depths; however, their increasing advantage at higher light levels is not reflected in the shallowest parts of Kāneʻohe Bay, where D. glynnii-dominated colonies become more prevalent. This may indicate that in these warmer surface waters, D. glynnii's higher heat tolerance outweighs the growth advantage that would otherwise favor C31 during the cooler parts of the year, providing a net ecological benefit. As oceans continue to warm, understanding how symbionts and the environment mediate coral performance outcomes will help predict reef futures and inform conservation interventions where coral stocks are selected for specific traits or symbionts. [ABSTRACT FROM AUTHOR]

Reef-building corals host diverse dinoflagellate algal symbionts (Family Symbiodiniaceae) whose identity can influence host thermotolerance and whose relative abundance can be dynamic. Breakdown in this symbiosis during "bleaching" events can promote changes in symbiont communities in favour of thermotolerant types, particularly in the genus Durusdinium. We employed experimental bleaching to manipulate the symbiont communities of three common Caribbean reef-building species (Montastraea cavernosa, Orbicella faveolata, and Siderastrea siderea) and tested whether seasonal differences in the corals' symbiont communities at the time of their collection affected their responses to manipulation. In O. faveolata and S. siderea, a minimum threshold of initial background proportion Durusdinium trenchii shaped recovery from bleaching with mainly Durusdinium. In contrast, in M. cavernosa, Durusdinium became highly dominant after recovery even when it was undetectable prior to bleaching. Seasonal changes were also detected in M. cavernosa and S. siderea dominated by Cladocopium, with significant increases and decreases, respectively, in symbionts per host cell in October (following annual temperature maxima) compared to the previous April (following temperature minima). These results demonstrate how background symbionts and seasonal differences in symbiont density can affect the disturbance and recovery dynamics of algal symbiont communities in different coral species, and prompt further research into how seasonal changes in algal symbiosis might inform projected future bleaching, which is increasingly relevant in light of predicted winter warming and prolonged warm summer temperatures under climate change. [ABSTRACT FROM AUTHOR]

Background: The positive effects of exposing corals to microorganisms have been reported though how the benefits are conferred are poorly understood. Here, we isolated an actinobacterial strain (SCSIO 13291) from Pocillopora damicornis with capabilities to synthesize antioxidants, vitamins, and antibacterial and antiviral compounds supported with phenotypic and/or genomic evidence. Strain SCSIO 13291 was labeled with 5 (and − 6)-carboxytetramethylrhodamine, succinimidyl ester and the labeled cell suspension directly inoculated onto the coral polyp tissues when nubbins were under thermal stress in a mesocosm experiment. We then visualized the labelled bacterial cells and analyzed the coral physiological, transcriptome and microbiome to elucidate the effect this strain conferred on the coral holobiont under thermal stress. Results: Subsequent microscopic observations confirmed the presence of the bacterium attached to the coral polyps. Addition of the SCSIO 13291 strain reduced signs of bleaching in the corals subjected to heat stress. At the same time, alterations in gene expression, which were involved in reactive oxygen species and light damage mitigation, attenuated apoptosis and exocytosis in addition to metabolite utilization, were observed in the coral host and Symbiodiniaceae populations. In addition, the coral associated bacterial community altered with a more stable ecological network for samples inoculated with the bacterial strain. Conclusions: Our results provide insights into the benefits of a putative actinobacterial probiotic strain that mitigate coral bleaching signs. This study suggests that the inoculation of bacteria can potentially directly benefit the coral holobiont through conferring metabolic activities or through indirect mechanisms of suppling additional nutrient sources. [ABSTRACT FROM AUTHOR]

Reef corals have been threatened by climate change, with more frequent and intense bleaching events leading to extensive coral mortality and loss of coral cover worldwide. In the face of this, the corals' photosymbiont assemblages have received special attention as a key to better understand the bleaching process and its recovery. To assess the effects of thermal anomalies, the coral Mussismilia harttii and the hydrocoral Millepora alcicornis were monitored through the El Niño 2015/2016 at a Southwestern Atlantic (SWA) coral reef. A severe bleaching event (57% of colonies bleached) was documented, triggered by a < 3 °C-week heatwave, but no mortality was detected. The hydrocoral was more susceptible than the scleractinian, displaying bleaching symptoms earlier and experiencing a longer and more intense bleaching event. The composition of photosymbionts in the M. alcicornis population was affected only at the rare biosphere level (< 5% relative abundance), with the emergence of new symbionts after bleaching. Conversely, a temporary dysbiosis was observed in the M. harttii population, with one of the dominant symbiodiniaceans decreasing in relative abundance at the peak of the bleaching, which negatively affected the total β-diversity. After colonies' complete recovery, symbiodiniaceans' dominances returned to normal levels in both hosts. These results highlight critical differences in how the two coral species cope with bleaching and contribute to the understanding of the role of photosymbionts throughout the bleaching-recovery process. [ABSTRACT FROM AUTHOR]

Black corals (Hexacorallia: Antipatharia) are a major component of mesophotic and deep marine ecosystems. Due to their preference for light deprived environments, black corals have historically been considered azooxanthellate, yet recent works have found them in association with dinoflagellates of the family Symbiodiniaceae down to 396 m depth. While corals and Symbiodiniaceae generally establish a symbiotic relationship in shallow water environments, the implications of this association is less well understood at deeper depths, where low light penetration cannot sustain efficient photosynthetic activity for the algae. However, Symbiodinaceae are not obligate autotrophs, and their capacity for heterotrophic feeding categorizes them as mixotrophs. In this study, we investigated the presence and diversity of Symbiodiniaceae associated with the deep-sea black coral Bathypathes thermophila (Antipatharia: Schizopathidae), collected from 204 to 655 m depth in the Saudi Arabian Red Sea. Using high-throughput sequencing of the ITS2 region, we report (1) the deepest record to date of Symbiodiniaceae associated with an anthozoan from 655 m, and (2) the first Red Sea record of Antipatharia in association with Symbiodiniaceae. Our analyses revealed that 14 out of 27 colonies of B. thermophila were associated with Symbiodiniaceae of the genera Cladocopium and Durusdinium. We unveiled 16 novel ITS2 type profiles, possibly unique to black corals and/or to these depths, along with seven profiles that were already known from shallow-water hard corals. No significant pattern was detected in terms of community diversity in relation to depth or sampling locality. Our study supports the existence of black corals-Symbiodiniaceae association and warrants further research to better understand the evolutionary processes and physiological mechanisms driving this association, specifically in light deprived environments.

IntroductionIn the upside-down jellyfish, Cassiopea xamachana (Cnidaria: Scyphozoa), the establishment of photosymbiosis with dinoflagellates (family Symbiodiniaceae) is necessary for the sessile polyp to undergo metamorphosis (strobilation) into a free-swimming adult. C. xamachana has the capacity to associate with a wide variety of dinoflagellate species and representatives of divergent genera. While some studies have looked at the successful induction of symbiosis, none to date have examined the lasting effect of diverse symbiont taxa on host survivorship and development, which is needed to assess the fitness costs of such symbioses.MethodsOur study exposes C. xamachana polyps to 22 different cultured Symbiodinaceae strains representing 13 species from 5 genera. We analyzed the time to strobilation, the number of ephyra (juvenile medusa) produced, and the proportion of ephyra that died prematurely.ResultsHere we show that C. xamachana strobilation can be induced by nearly each symbiodinacean strain we tested, with the exception of free-living species (i.e., unknown to establish symbiosis with any other marine host). Additionally, ephyrae did not display morphological variation or survivorship differences with varying symbionts. However, we observed intraspecific variation in time to induce strobilation with different cultured dinoflagellate strains.DiscussionThis work expands the known symbiont species that can form stable mutualisms with C. xamachana, primarily in the genera Symbiodinium and Breviolum. Additionally, we provide evidence of differences in ability of cultured symbiodiniaceans to establish symbiosis with a host, which suggests population-level differences in dinoflagellate cultures impact their symbiosis success. By utilizing an animal like C. xamachana with flexible symbiont uptake, we are able to explore how symbiont diversity can influence the timing and success of symbiosis-driven development.

Coral reefs are essential for marine ecology and biodiversity. Global climate change has resulted in severe coral reef degradation, partly via coral bleaching, which is caused by rising sea temperatures and solar light intensity. In this study, we examined the impact of strong light (300 µmol.m−2.s−1) and high temperature (33°C) on the growth, immunity, and gene expression of Galaxea fascicularis. Strong light caused coral bleaching in the absence of high sea temperatures, while no obvious bleaching was observed under high temperature alone. The effect of strong light on calcification rate of G. fascicularis is significantly weaker than that of high temperature. Both strong light and high temperatures significantly affected the immune enzyme activity of G. fascicularis symbionts, with the former having a strong effect on their photosystem. Temperature affected the digestive system, replication and repair, and cell growth and death of coral hosts, as indicated by transcriptomics analysis. These results provide a valuable for strategies to mitigate coral bleaching. Teaser: We explored the effects of strong light exposure and high temperature on coral reefs and their symbiont algae.

Abstract Background Ocean warming is a leading cause of increasing episodes of coral bleaching, the dissociation between coral hosts and their dinoflagellate algal symbionts in the family Symbiodiniaceae. While the diversity and flexibility of Symbiodiniaceae is presumably responsible for variations in coral response to physical stressors such as elevated temperature, there is little data directly comparing physiological performance that accounts for symbiont identity associated with the same coral host species. Here, using Pocillopora damicornis harboring genotypically distinct Symbiodiniaceae strains, we examined the physiological responses of the coral holobiont and the dynamics of symbiont community change under thermal stress in a laboratory-controlled experiment. Results We found that P. damicornis dominated with symbionts of metahaplotype D1-D4-D6 in the genus Durusdinium (i.e., PdD holobiont) was more robust to thermal stress than its counterpart with symbionts of metahaplotype C42-C1-C1b-C1c in the genus Cladocopium (i.e., PdC holobiont). Under ambient temperature, however, the thermally sensitive Cladocopium spp. exhibited higher photosynthetic efficiency and translocated more fixed carbon to the host, likely facilitating faster coral growth and calcification. Moreover, we observed a thermally induced increase in Durusdinium proportion in the PdC holobiont; however, this “symbiont shuffling” in the background was overwhelmed by the overall Cladocopium dominance, which coincided with faster coral bleaching and reduced calcification. Conclusions These findings support that lineage-specific symbiont dominance is a driver of distinct coral responses to thermal stress. In addition, we found that “symbiont shuffling” may begin with stress-forced, subtle changes in the rare biosphere to eventually trade off growth for increased resilience. Furthermore, the flexibility in corals’ association with thermally tolerant symbiont lineages to adapt or acclimatize to future warming oceans should be viewed with conservative optimism as the current rate of environmental changes may outpace the evolutionary capabilities of corals. Video Abstract

In reef-building corals (order Scleractinia) and giant clams (phylum Molluca), V-type H+-ATPase (VHA) in host cells is part of a carbon concentrating mechanism (CCM) that regulates photosynthetic rates of their symbiotic algae. Here, we show that VHA plays a similar role in the sea anemone Anemonia majano, a member of the order Actinaria and sister group to the Scleractinia, which in contrast to their colonial calcifying coral relatives is a solitary, soft-bodied taxa. Western blotting and immunofluorescence revealed that VHA was abundantly present in the host-derived symbiosome membrane surrounding the photosymbionts. Pharmacological inhibition of VHA activity in individual anemones resulted in an approximately 80% decrease of photosynthetic O2 production. These results extend the presence of a host-controlled VHA-dependent CCM to non-calcifying cnidarians of the order Actiniaria, suggesting it is widespread among photosymbiosis between aquatic invertebrates and Symbiodiniaceae algae.

The symbiotic relationship between corals and their associated microorganisms is crucial for the health of coral reef eco-environmental systems. Recently, there has been a growing interest in unraveling how the manipulation of symbiont nutrient cycling affects the stress tolerance in the holobiont of coral reefs. However, most studies have primarily focused on coral–Symbiodiniaceae–bacterial interactions as a whole, neglecting the interactions between Symbiodiniaceae and bacteria, which remain largely unexplored. In this study, we proposed a hypothesis that there exists an inner symbiotic loop of Symbiodiniaceae and bacteria within the coral symbiotic loop. We conducted experiments to demonstrate how metabolic exchanges between Symbiodiniaceae and bacteria facilitate the nutritional supply necessary for cellular growth. It was seen that the beneficial bacterium, Ruegeria sp., supplied a nitrogen source to the Symbiodiniaceae strain Durusdinium sp., allowing this dinoflagellate to thrive in a nitrogen-free medium. The Ruegeria sp.–Durusdinium sp. interaction was confirmed through 15N-stable isotope probing–single cell Raman spectroscopy, in which 15N infiltrated into the bacterial cells for intracellular metabolism, and eventually the labeled nitrogen source was traced within the macromolecules of Symbiodiniaceae cells. The investigation into Symbiodiniaceae loop interactions validates our hypothesis and contributes to a comprehensive understanding of the intricate coral holobiont. These findings have the potential to enhance the health of coral reefs in the face of global climate change.