Cladocopium Goreaui Research Articles

The growth and nitrogen utilization strategies in two dominant Symbiodiniaceae species facing nitrogen deficiency and enrichment

Symbiodiniaceae, a diverse group of unicellular dinoflagellates, are well known as endosymbionts of marine invertebrates (e.g., corals, giant clams and foraminiferans). Currently, how in vitro cultured Symbiodiniaceae cope with nitrogen (N) deficiency and enhancement remain largely unexplored. To address this knowledge gap, this study investigated the dynamics of growth, photosynthesis and crystalline guanine formation in response to differential N supplies in two dominant Symbiodiniaceae species: Durusdinium trenchii and Cladocopium goreaui. The results indicated growth rate and photosynthesis were closely related to N sources and concentrations. Under N deficiency, cell growth was inhibited. As N concentration increased, both D. trenchii and C. goreaui exhibited flexible strategies for utilizing different N sources. When provided with nitrate (NO3−), C. goreaui and D. trenchii showed an enhancement in the algal growth and photosynthetic efficiency (Fv/Fm). When ammonium (NH4+) was supplied, a moderate increase of NH4+ can benefit cell growth and photosynthesis, but excessive enrichment adversely affected algal growth. Additionally, Raman microscopy demonstrated that cellular crystalline guanine was formed by C. goreaui when exposed to N supply, but gradually decreased as N was consumed in medium. A similar phenomenon was observed in D. trenchii. We proposed that crystalline guanine may serve as an important N storage and utilization strategy. This study delved into the growth strategies and adaptability of Symbiodiniaceae to varying N nutritional environments, which contributes to understanding the symbiotic relationship between Symbiodiniaceae and corals.

Gene expression plasticity facilitates acclimatization of a long-lived Caribbean coral across divergent reef environments

Local adaptation can increase fitness under stable environmental conditions. However, in rapidly changing environments, compensatory mechanisms enabled through plasticity may better promote fitness. Climate change is causing devastating impacts on coral reefs globally and understanding the potential for adaptive and plastic responses is critical for reef management. We conducted a four-year, three-way reciprocal transplant of the Caribbean coral Siderastrea siderea across forereef, backreef, and nearshore populations in Belize to investigate the potential for environmental specialization versus plasticity in this species. Corals maintained high survival within forereef and backreef environments, but transplantation to nearshore environments resulted in high mortality, suggesting that nearshore environments present strong environmental selection. Only forereef-sourced corals demonstrated evidence of environmental specialization, exhibiting the highest growth in the forereef. Gene expression profiling 3.5 years post-transplantation revealed that transplanted coral hosts exhibited profiles more similar to other corals in the same reef environment, regardless of their source location, suggesting that transcriptome plasticity facilitates acclimatization to environmental change in S. siderea. In contrast, algal symbiont (Cladocopium goreaui) gene expression showcased functional variation between source locations that was maintained post-transplantation. Our findings suggest limited acclimatory capacity of some S. siderea populations under strong environmental selection and highlight the potential limits of coral physiological plasticity in reef restoration.

Phosphorus nutrition strategies in a Symbiodiniacean species: Implications in coral-alga symbiosis facing increasing phosphorus deficiency in future warmer oceans.

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.

Heat-evolved microalgal symbionts increase thermal bleaching tolerance of coral juveniles without a trade-off against growth

Global climate change is threatening the persistence of coral reefs as associated summer heatwaves trigger the loss of microalgal endosymbionts (Symbiodiniaceae) from the coral tissues, or coral bleaching. We infected aposymbiotic juveniles of the coral Acropora tenuis with either wildtype (WT10) or heat-evolved (SS1 or SS8) Symbiodiniaceae strains Cladocopium proliferum (formerly referred to as Cladocopium goreaui and Cladocopium C1acro). After 10 months at 27 °C, SS8-juveniles were 2 × larger than SS1- or WT10-juveniles. In response to a simulated heatwave (31 °C for 41 days), the WT10-juveniles bleached and showed a decline in respiration while cell densities and respiration in both SS-juvenile groups remained unchanged compared to the controls. These results reveal that some heat-evolved strains can increase the bleaching tolerance of juvenile corals without a trade-off against growth. This response is opposite to the lower nutrient provisioning often reported for naturally thermotolerant Symbiodiniaceae (e.g. genus Durusdinium), thereby offering enhanced fitness to the host without the ecological consequences of diminished growth.

Unraveling the metabolic effects of benzophenone-3 on the endosymbiotic dinoflagellate Cladocopium goreaui.

As a well-known pseudo-persistent environmental pollutant, oxybenzone (BP-3) and its related organic ultraviolet (UV) filters have been verified to directly contribute to the increasing mortality rate of coral reefs. Previous studies have revealed the potential role of symbiotic Symbiodiniaceae in protecting corals from the toxic effects of UV filters. However, the detailed protection mechanism(s) have not been explained. Here, the impacts of BP-3 on the symbiotic Symbiodiniaceae Cladocopium goreaui were explored. C. goreaui cells exhibited distinct cell growth at different BP-3 doses, with increasing growth at the lower concentration (2 mg L-1) and rapid death at a higher concentration (20 mg L-1). Furthermore, C. goreaui cells showed a significant BP-3 uptake at the lower BP-3 concentration. BP-3 absorbing cells exhibited elevated photosynthetic efficiency, and decreased cellular carbon and nitrogen contents. Besides, the derivatives of BP-3 and aromatic amino acid metabolism highly responded to BP-3 absorption and biodegradation. Our physiological and metabolic results reveal that the symbiotic Symbiodiniaceae could resist the toxicity of a range of BP-3 through promoting cell division, photosynthesis, and reprogramming amino acid metabolism. This study provides novel insights into the influences of organic UV filters to coral reef ecosystems, which urgently needs increasing attention and management.

Toxicological effects of oxybenzone on the growth and bacterial composition of Symbiodiniaceae

Oxybenzone, a common ultraviolet (UV) filter, is a growing environmental concern due to its ecotoxicological effects. However, the responses of Symbiodiniaceae and their bacterial communities to oxybenzone are largely unknown. In this study, the effects of oxybenzone on Effrenium voratum and Cladocopium goreaui were investigated. The results revealed that sensitivity of Symbiodiniaceae to oxybenzone was species-dependent. 50 μg L−1 of oxybenzone significantly impacted the cell density of C. goreaui, causing a 36.73% decrease. When oxybenzone concentration increased to 500 μg L−1 and 5000 μg L−1, cell division was completely suppressed; meanwhile, chl-a content declined to zero. Compared to C. goreaui, E. voratum had higher resistance to oxybenzone. There was no significant difference in cell density between 50 μg L−1 group and control group. At higher dosage of oxybenzone (500 μg L−1 and 5000 μg L−1), the cell density declined 32.02% and 45.45% compared to the control group, respectively. Additionally, we revealed that the diversity and structure of bacterial community were affected by oxybenzone. Briefly, 500 μg L−1 and 5000 μg L−1 of oxybenzone altered the diversity of bacterial community in C. goreau. Furthermore, the relative abundances of Costertonia, Roseitalea, Rhodopirellula, and Roseobacter were negatively affected by oxybenzone ranging 50 μg L−1 to 5000 μg L−1. Compare to C. goreaui, the bacterial community composition associated with E. voratum was more stable. As revealed by KEGG pathway analysis, oxybenzone affected energy metabolism and inhibited the metabolism of cofactors and vitamins in C. goreaui, while 5000 μg L−1 of oxybenzone significantly altered the carbohydrate metabolism, membrane transport and amino acid metabolism in E. voratum. The changes of bacterial composition may contribute to the variation in algal growth. These results indicated that oxybenzone pollution could injury Symbiodiniaceae, even threaten coral reef ecosystems.

Improved Cladocopium goreaui Genome Assembly Reveals Features of a Facultative Coral Symbiont and the Complex Evolutionary History of Dinoflagellate Genes.

Dinoflagellates of the family Symbiodiniaceae are crucial photosymbionts in corals and other marine organisms. Of these, Cladocopium goreaui is one of the most dominant symbiont species in the Indo-Pacific. Here, we present an improved genome assembly of C. goreaui combining new long-read sequence data with previously generated short-read data. Incorporating new full-length transcripts to guide gene prediction, the C. goreaui genome (1.2 Gb) exhibits a high extent of completeness (82.4% based on BUSCO protein recovery) and better resolution of repetitive sequence regions; 45,322 gene models were predicted, and 327 putative, topologically associated domains of the chromosomes were identified. Comparison with other Symbiodiniaceae genomes revealed a prevalence of repeats and duplicated genes in C. goreaui, and lineage-specific genes indicating functional innovation. Incorporating 2,841,408 protein sequences from 96 taxonomically diverse eukaryotes and representative prokaryotes in a phylogenomic approach, we assessed the evolutionary history of C. goreaui genes. Of the 5246 phylogenetic trees inferred from homologous protein sets containing two or more phyla, 35–36% have putatively originated via horizontal gene transfer (HGT), predominantly (19–23%) via an ancestral Archaeplastida lineage implicated in the endosymbiotic origin of plastids: 10–11% are of green algal origin, including genes encoding photosynthetic functions. Our results demonstrate the utility of long-read sequence data in resolving structural features of a dinoflagellate genome, and highlight how genetic transfer has shaped genome evolution of a facultative symbiont, and more broadly of dinoflagellates.

Interactive effects of acidification and copper exposure on the reproduction and metabolism of coral endosymbiont Cladocopium goreaui

Ocean acidification resulting from increased CO2 and pollution from land-sourced toxicants such as copper have been linked to coral cover declines in coastal reef ecosystems. The impacts of ocean acidification and copper pollution on corals have been intensively investigated, whereas research on their effects on coral endosymbiont Symbiodiniaceae is limited. In this study, reproduction, photosynthetic parameters, nutrient accumulation and metabolome of Symbiodiniaceae Cladocopium goreaui were investigated after a weeklong treatment with acute CO2-induced acidification and copper ion. Acidification promoted algal reproduction through increased nutrients assimilation, upregulated citrate cycle and biomolecular biosynthesis pathway, while copper exposure repressed algal reproduction through toxic effects. The combined acidification and copper exposure caused the same decline in algal reproduction as copper exposure alone, but the upregulation of pentose phosphate pathway and the downregulation of aromatic amino acid biosynthesis. These results suggest that copper pollution could override the positive effects of acidification on the symbiodiniacean reproduction.

Differential Affinities of a Pocillopora damicornis Galectin to Five Genera of Symbiodiniaceae at Different Temperatures

The symbiosis of coral-Symbiodiniaceae is the quintessential basis of the coral reef ecosystem, and its breakdown results in coral bleaching, one of the most severe ecological catastrophes in the ocean. Critical to the establishment of the symbiosis is the host’s specific recognition of the symbionts through the binding of the coral host’s pattern recognition receptors (PRRs) to the symbiont cell surface’s glycoconjugates. However, the molecular basis for this recognition process is poorly understood. The present study investigated the binding affinities of the coral galectin PdGLT-1 to different symbiodiniacean species under different temperatures. At 25°C, the PdGLT-1 recombinant protein (rPdGLT-1) exhibited different binding affinities to different symbiodiniacean species from five genera, with a significantly higher binding affinity (p < 0.05) to Fugacium kawagutii (2.6-fold) and Cladocopium goreaui (1.9-fold) than Symbiodinium microadriaticum. The binding topology of rPdGLT-1 differed among the five symbiodiniacean species; for S. microadriaticum, Breviolum minutum, and Durusdinium trenchii, the binding was on some specific sites on the cell surface, whereas for C. goreaui and F. kawagutii, the binding signals were detected over the whole cell surface. Interestingly, PdGLT-1 binding induced agglutination of F. kawagutii cells but not of C. goreaui, explaining why C. goreaui was the most dominant symbiodiniacean symbionts in corals. Moreover, the affinity of rPdGLT-1 to Symbiodiniaceae was affected by temperature, and the highest binding affinities were observed at 30, 20, 30, 35, and 30°C for S. microadriaticum, B. minutum, C. goreaui, D. trenchii, and F. kawagutii, respectively. The optimal binding temperatures were consistent with the current understanding that D. trenchii was the most thermal resistant among these species. These results suggest that the binding affinity of the PRR PdGLT-1 may determine the specificity of host-symbiont pairing and explain why Cladocopium is the dominant symbionts of coral P. damicornis at normal temperature, and corals with Durusdinium symbionts may survive better at high temperature.

Regulation of the Coral-Associated Bacteria and Symbiodiniaceae in Acropora valida Under Ocean Acidification.

Ocean acidification is one of many stressors that coral reef ecosystems are currently contending with. Thus, understanding the response of key symbiotic microbes to ocean acidification is of great significance for understanding the adaptation mechanism and development trend of coral holobionts. Here, high-throughput sequencing technology was employed to investigate the coral-associated bacteria and Symbiodiniaceae of the ecologically important coral Acropora valida exposed to different pH gradients. After 30 days of acclimatization, we set four acidification gradients (pH 8.2, 7.8, 7.4, and 7.2, respectively), and each pH condition was applied for 10 days, with the whole experiment lasting for 70 days. Although the Symbiodiniaceae density decreased significantly, the coral did not appear to be bleached, and the real-time photosynthetic rate did not change significantly, indicating that A. valida has strong tolerance to acidification. Moreover, the Symbiodiniaceae community composition was hardly affected by ocean acidification, with the C1 subclade (Cladocopium goreaui) being dominant among the Symbiodiniaceae dominant types. The relative abundance of the Symbiodiniaceae background types was significantly higher at pH 7.2, indicating that ocean acidification might increase the stability of the community composition by regulating the Symbiodiniaceae rare biosphere. Furthermore, the stable symbiosis between the C1 subclade and coral host may contribute to the stability of the real-time photosynthetic efficiency. Finally, concerning the coral-associated bacteria, the stable symbiosis between Endozoicomonas and coral host is likely to help them adapt to ocean acidification. The significant increase in the relative abundance of Cyanobacteria at pH 7.2 may also compensate for the photosynthesis efficiency of a coral holobiont. In summary, this study suggests that the combined response of key symbiotic microbes helps the whole coral host resist the threats of ocean acidification.

Toxicity thresholds of nine herbicides to coral symbionts (Symbiodiniaceae)

Over 30 herbicides have been detected in catchments and waters of the Great Barrier Reef (GBR) and their toxicity to key tropical species, including the coral endosymbiotic algae Symbiodiniaceae, is not generally considered in current water quality guideline values (WQGVs). Mutualistic symbionts of the family Symbiodiniaceae are essential for the survival of scleractinian corals. We tested the effects of nine GBR-relevant herbicides on photosynthetic efficiency (ΔF/Fm′) and specific growth rate (SGR) over 14 days of cultured coral endosymbiont Cladocopium goreaui (formerly Symbiodinium clade C1). All seven Photosystem II (PSII) herbicides tested inhibited ΔF/Fm′ and SGR, with toxicity thresholds for SGR ranging between 2.75 and 320 µg L−1 (no effect concentration) and 2.54–257 µg L−1 (EC10). There was a strong correlation between EC50s for ΔF/Fm′ and SGR for all PSII herbicides indicating that inhibition of ΔF/Fm′ can be considered a biologically relevant toxicity endpoint for PSII herbicides to this species. The non-PSII herbicides haloxyfop and imazapic did not affect ΔF/Fm′ or SGR at the highest concentrations tested. The inclusion of this toxicity data for Symbiodiniaceae will contribute to improving WQGVs to adequately inform risk assessments and the management of herbicides in tropical marine ecosystems.

Cell wall proteomic analysis of the cnidarian photosymbionts Breviolum minutum and Cladocopium goreaui.

The algal cell wall is an important cellular component that functions in defense, nutrient utilization, signaling, adhesion, and cell–cell recognition—processes important in the cnidarian–dinoflagellate symbiosis. The cell wall of symbiodiniacean dinoflagellates is not well characterized. Here, we present a method to isolate cell walls of Symbiodiniaceae and prepare cell‐wall‐enriched samples for proteomic analysis. Label‐free liquid chromatography–electrospray ionization tandem mass spectrometry was used to explore the surface proteome of two Symbiodiniaceae species from the Great Barrier Reef: Breviolum minutum and Cladocopium goreaui. Transporters, hydrolases, translocases, and proteins involved in cell‐adhesion and protein–protein interactions were identified, but the majority of cell wall proteins had no homologues in public databases. We propose roles for some of these proteins in the cnidarian–dinoflagellate symbiosis. This work provides the first proteomics investigation of cell wall proteins in the Symbiodiniaceae and represents a basis for future explorations of the roles of cell wall proteins in Symbiodiniaceae and other dinoflagellates.

Cell surface carbohydrates of symbiotic dinoflagellates and their role in the establishment of cnidarian\u2013dinoflagellate symbiosis

Symbiodiniaceae algae are often photosymbionts of reef-building corals. The establishment of their symbiosis resembles a microbial infection where eukaryotic pattern recognition receptors (e.g. lectins) are thought to recognize a specific range of taxon-specific microbial-associated molecular patterns (e.g. glycans). The present study used the sea anemone, Exaiptasia diaphana and three species of Symbiodiniaceae (the homologous Breviolum minutum, the heterologous-compatible Cladocopium goreaui and the heterologous-incompatible Fugacium kawagutii) to compare the surface glycomes of three symbionts and explore the role of glycan–lectin interactions in host–symbiont recognition and establishment of symbiosis. We identified the nucleotide sugars of the algal cells, then examined glycans on the cell wall of the three symbiont species with monosaccharide analysis, lectin array technology and fluorescence microscopy of the algal cell decorated with fluorescently tagged lectins. Armed with this inventory of possible glycan moieties, we then assayed the ability of the three Symbiodiniaceae to colonize aposymbiotic E. diaphana after modifying the surface of one of the two partners. The Symbiodiniaceae cell-surface glycome varies among algal species. Trypsin treatment of the alga changed the rate of B. minutum and C. goreaui uptake, suggesting that a protein-based moiety is an essential part of compatible symbiont recognition. Our data strongly support the importance of D-galactose (in particular β-D-galactose) residues in the establishment of the cnidarian–dinoflagellate symbiosis, and we propose a potential involvement of L-fucose, D-xylose and D-galacturonic acid in the early steps of this mutualism.

Experimental evolution of the coral algal endosymbiont, Cladocopium goreaui: lessons learnt across a decade of stress experiments to enhance coral heat tolerance

Projected increases in sea surface temperatures will exceed corals' ability to withstand heat stress within this century. Experimental evolution of cultured symbionts (Symbiodiniaceae) at high temperatures followed by reintroduction into corals can enhance coral heat tolerance. Several studies have selected for enhanced tolerance in Cladocopium goreaui (C1) over multiple time scales and then compared the performance of coral juveniles infected with the heat‐tolerant C1 selected strain (SS) to the performance of juveniles infected with the C1 wild type (WT). To derive lessons about host benefits when symbionts are experimentally selected, here we compare the performance of SS‐ and WT‐juveniles after 21 cell generations of heat selection versus longer periods (73–131) in recently published experiments. After 21 generations, we found rapid improvement in heat tolerance of SS through an overall shift in the mean tolerance to temperature. This did not translate to improved growth and survivorship of the coral. Specifically, survival did not differ significantly between juveniles of Acropora tenuis hosting WT versus SS at any temperature. Juveniles infected with WT exhibited greater skeletal growth than those infected with SS at 27 and 31°C but not at 32.5°C. SS‐juvenile symbiont cell densities increased significantly at 27°C relative to SS‐juveniles in the 31 and 32.5°C. Photosynthetic efficiencies in SS‐juveniles were higher compared to WT‐juveniles at 31°C, equal at 27°C, and lower at 32.5°C. These results suggest that selection over longer generation (>130) times will be needed to confer host benefits and will be dependent on the stability of this association being maintained in nature.

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

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

Dual RNA-sequencing analyses of a coral and its native symbiont during the establishment of symbiosis.

Despite the ecological significance of the mutualistic relationship between Symbiodiniaceae and reef-building corals, the molecular interactions during establishment of this relationship are not well understood. This is particularly true of the transcriptional changes that occur in the symbiont. In the current study, a dual RNA-sequencing approach was used to better understand transcriptional changes on both sides of the coral-symbiont interaction during the colonization of Acropora tenuis by a compatible Symbiodiniaceae strain (Cladocopium goreaui; ITS2 type C1). Comparison of transcript levels of the in hospite symbiont 3, 12, 48 and 72hr after exposure to those of the same strain in culture revealed that extensive and generalized down-regulation of symbiont gene expression occurred during the infection process. Included in this "symbiosis-derived transcriptional repression" were a range of stress response and immune-related genes. In contrast, a suite of symbiont genes implicated in metabolism was upregulated in the symbiotic state. The coral data support the hypothesis that immune-suppression and arrest of phagosome maturation play important roles during the establishment of compatible symbioses, and additionally imply the involvement of some SCRiP family members in the colonization process. Consistent with previous ecological studies, the transcriptomic data suggest that active translocation of metabolites to the host may begin early in the colonization process, and thus that the mutualistic relationship can be established at the larval stage. This dual RNA-sequencing study provides insights into the transcriptomic remodelling that occurs in C.goreaui during transition to a symbiotic lifestyle and the novel coral genes implicated in symbiosis.

Competitive traits of coral symbionts may alter the structure and function of the microbiome

In the face of global warming and unprecedented coral bleaching, a new avenue of research is focused on relatively rare algal symbionts and their ability to confer thermal tolerance to their host by association. Yet, thermal tolerance is just one of many physiological attributes inherent to the diversity of symbiodinians, a result of millions of years of competition and niche partitioning. Here, we revealed that competition among cocultured symbiodinians alters nutrient assimilation and compound production with species-specific responses. For Cladocopium goreaui, a species ubiquitous within stable coral associations, temperature stress increased sensitivity to competition eliciting a shift toward investment in cell replication, i.e., putative niche exploitation. Meanwhile, competition led Durusdinium trenchii, a thermally tolerant “background” symbiodinian, to divert resources from immediate growth to storage. As such, competition may be driving the dominance of C. goreaui outside of temperature stress, the destabilization of symbioses under thermal stress, the repopulation of coral tissues by D. trenchii following bleaching, and ultimately undermine the efficacy of symbiont turnover as an adaptive mechanism.

Unlocking the black‐box of inorganic carbon‐uptake and utilization strategies among coral endosymbionts (Symbiodiniaceae)

AbstractDinoflagellates within the family Symbiodiniaceae are widespread and fuel metabolism of reef‐forming corals through photosynthesis. Adaptation in capacity to harvest and utilize light, and “safely” process photosynthetically generated energy is a key factor regulating their broad ecological success. However, whether such adaptive capacity similarly extends to how Symbiodiniaceae species and genotypes assimilate inorganic carbon (Ci) remains unexplored. We build on recent approaches exploring functional diversity of fitness traits to identify whether Ci uptake and incorporation could be reconciled with evolutionary adaptation among Symbiodiniaceae. We examined phylogenetically diverse Symbiodiniaceae cultures (23 isolates, 6 genera) to track how carbon was invested into cellular uptake, excretion, and growth (cell size, division, storage). Gross carbon uptake rates (GPC) over 1 h varied among isolates grown at 26°C (0.63–3.08 pg C [cell h]−1) with no evident pattern with algal phylogeny. Intriguingly, net carbon uptake rates (24 h) were often higher (1.01–5.54 pg C [cell h]−1) than corresponding values of GPC—we discuss how such GPC measurements may reflect highly conserved biological characteristics for cultured cells linked to high metabolic dependency on photorespiration and heterotrophy. Three isolates from different genera (Cladocopium goreaui, Durusdinium trenchii, and Effrenium voratum) were additionally grown at 20°C and 30°C. Here, Ci uptake consistently decreased with temperature‐driven declines in growth rate, suggesting environmental regulation outweighs phylogenetic organization of carbon assimilation capacity among Symbiodiniaceae. Together, these data demonstrate environmental regulation and ecological success among Symbiodiniaceae likely rests on plasticity of upstream photosynthetic processes (light harvesting, energy quenching, etc.) to overcome evolutionary‐conserved limitations in Ci functioning.

Assessing the role of historical temperature regime and algal symbionts on the heat tolerance of coral juveniles.

ABSTRACTThe rate of coral reef degradation from climate change is accelerating and, as a consequence, a number of interventions to increase coral resilience and accelerate recovery are under consideration. Acropora spathulata coral colonies that survived mass bleaching in 2016 and 2017 were sourced from a bleaching-impacted and warmer northern reef on the Great Barrier Reef (GBR). These individuals were reproductively crossed with colonies collected from a recently bleached but historically cooler central GBR reef to produce pure and crossbred offspring groups (warm–warm, warm–cool and cool–warm). We tested whether corals from the warmer reef produced more thermally tolerant hybrid and purebred offspring compared with crosses produced with colonies sourced from the cooler reef and whether different symbiont taxa affect heat tolerance. Juveniles were infected with Symbiodinium tridacnidorum, Cladocopium goreaui and Durusdinium trenchii and survival, bleaching and growth were assessed at 27.5°C and 31°C. The contribution of host genetic background and symbiont identity varied across fitness traits. Offspring with either both or one parent from the northern population exhibited a 13- to 26-fold increase in survival odds relative to all other treatments where survival probability was significantly influenced by familial cross identity at 31°C but not 27.5°C (Kaplan–Meier P=0.001 versus 0.2). If in symbiosis with D. trenchii, a warm sire and cool dam provided the best odds of juvenile survival. Bleaching was predominantly driven by Symbiodiniaceae treatment, where juveniles hosting D. trenchii bleached significantly less than the other treatments at 31°C. The greatest overall fold-benefits in growth and survival at 31°C occurred in having at least one warm dam and in symbiosis with D. trenchii. Juveniles associated with D. trenchii grew the most at 31°C, but at 27.5°C, growth was fastest in juveniles associated with C. goreaui. In conclusion, selective breeding with warmer GBR corals in combination with algal symbiont manipulation can assist in increasing thermal tolerance on cooler but warming reefs. Such interventions have the potential to improve coral fitness in warming oceans.This article has an associated First Person interview with the first author of the paper.

Molecular mechanisms of acclimation to long-term elevated temperature exposure in marine symbioses.

Seawater temperature rise in French Polynesia has repeatedly resulted in the bleaching of corals and giant clams. Because giant clams possess distinctive ectosymbiotic features, they represent a unique and powerful model for comparing molecular pathways involved in (a) maintenance of symbiosis and (b) acquisition of thermotolerance among coral reef organisms. Herein, we explored the physiological and transcriptomic responses of the clam hosts and their photosynthetically active symbionts over a 65day experiment in which clams were exposed to either normal or environmentally relevant elevated seawater temperatures. Additionally, we used metabarcoding data coupled with in situ sampling/survey data to explore the relative importance of holobiont adaptation (i.e., a symbiont community shift) versus acclimation (i.e., physiological changes at the molecular level) in the clams' responses to environmental change. We finally compared transcriptomic data to publicly available genomic datasets for Symbiodiniaceae dinoflagellates (both cultured and in hospite with the coral Pocillopora damicornis) to better tease apart the responses of both hosts and specific symbiont genotypes in this mutualistic association. Gene module preservation analysis revealed that the function of the symbionts' photosystem II was impaired at high temperature, and this response was also found across all holobionts and Symbiodiniaceae lineages examined. Similarly, epigenetic modulation appeared to be a key response mechanism for symbionts in hospite with giant clams exposed to high temperatures, and such modulation was able to distinguish thermotolerant from thermosensitive Cladocopium goreaui ecotypes; epigenetic processes may, then, represent a promising research avenue for those interested in coral reef conservation in this era of changing global climate.