Transcriptomic changes with increasing algal symbiont reveal the detailed process underlying establishment of coral-algal symbiosis.
ABSTRACT: To clarify the establishment process of coral-algal symbiotic relationships, coral transcriptome changes during increasing algal symbiont densities were examined in juvenile corals following inoculation with the algae Symbiodinium goreaui (clade C) and S. trenchii (clade D), and comparison of their transcriptomes with aposymbiotic corals by RNA-sequencing. Since Symbiodinium clades C and D showed very different rates of density increase, comparisons were made of early onsets of both symbionts, revealing that the host behaved differently for each. RNA-sequencing showed that the number of differentially-expressed genes in corals colonized by clade D increased ca. two-fold from 10 to 20 days, whereas corals with clade C showed unremarkable changes consistent with a slow rate of density increase. The data revealed dynamic metabolic changes in symbiotic corals. In addition, the endocytosis pathway was also upregulated, while lysosomal digestive enzymes and the immune system tended to be downregulated as the density of clade D algae increased. The present dataset provides an enormous number of candidate symbiosis-related molecules that exhibit the detailed process by which coral-algal endosymbiosis is established.
Project description:Some reef-building corals have been shown to respond to environmental change by shifting the composition of their algal symbiont (genus Symbiodinium) communities. These shifts have been proposed as a potential mechanism by which corals might survive climate stressors, such as increased temperatures. Conventional molecular methods suggest this adaptive capacity may not be widespread because few (∼25%) coral species have been found to associate with multiple Symbiodinium clades. However, these methods can fail to detect low abundance symbionts (typically less than 10-20% of the total algal symbiont community). To determine whether additional Symbiodinium clades are present, but are not detected using conventional techniques, we applied a high-resolution, real-time PCR assay to survey Symbiodinium (in clades A-D) from 39 species of phylogenetically and geographically diverse scleractinian corals. This survey included 26 coral species thought to be restricted to hosting a single Symbiodinium clade ('symbiotic specialists'). We detected at least two Symbiodinium clades (C and D) in at least one sample of all 39 coral species tested; all four Symbiodinium clades were detected in over half (54%) of the 26 symbiotic specialist coral species. Furthermore, on average, 68 per cent of all sampled colonies within a given coral species hosted two or more symbiont clades. We conclude that the ability to associate with multiple symbiont clades is common in scleractinian (stony) corals, and that, in coral-algal symbiosis, 'specificity' and 'flexibility' are relative terms: specificity is rarely absolute. The potential for reef corals to adapt or acclimatize to environmental change via symbiont community shifts may therefore be more phylogenetically widespread than has previously been assumed.
Project description:With the increase in sea surface temperature (SST), scleractinian corals are exposed to bleaching threats but may possess certain flexibilities in terms of their associations with symbiotic algae. Previous studies have shown a close symbiosis between coral the and Symbiodinium; however, the spatial variation of the symbiosis and the attribution underlying are not well understood. In the present study, we examined coral-algal symbiosis in Galaxea fascicularis and Montipora spp. from three biogeographic regions across ~10° of latitude in the South China Sea. Analysis of similarities (ANOSIM) indicated a highly flexible coral-algal symbiosis in both G. fascicularis and Montipora spp. and canonical correspondence analysis (CCA) showed that temperature explained 83.2% and 60.1% of the explanatory subclade variations in G. fascicularis and Montipora spp., respectively, which suggested that temperature was the main environmental factor contributing to the diversity of Symbiodinium across the three regions. The geographic specificity of the Symbiodinium phylogeny was identified, revealing possible environmental selection across the three regions. These results suggest that scleractinian corals may have the ability to regulate Symbiodinium community structures under different temperatures and thus be able to adapt to gradual climate change.
Project description:Reef-building corals switch endosymbiotic algae of the genus Symbiodinium during their early growth stages and during bleaching events. Clade C Symbiodinium algae are dominant in corals, although other clades - including A and D - have also been commonly detected in juvenile Acroporid corals. Previous studies have been reported that only molecular data of Symbiodinium clade were identified within field corals. In this study, we inoculated aposymbiotic juvenile polyps with cultures of clades C1 and D Symbiodinium algae, and investigated the different effect of these two clades of Symbiodinium on juvenile polyps. Our results showed that clade C1 algae did not grow, while clade D algae grew rapidly during the first 2 months after inoculation. Polyps associated with clade C1 algae exhibited bright green fluorescence across the body and tentacles after inoculation. The growth rate of polyp skeletons was lower in polyps associated with clade C1 algae than those associated with clade D algae. On the other hand, antioxidant activity (catalase) of corals was not significantly different between corals with clade C1 and clade D algae. Our results suggested that clade D Symbiodinium algae easily form symbiotic relationships with corals and that these algae could contribute to coral growth in early symbiosis stages.
Project description:Dinoflagellates from the genus Symbiodinium form a mutualistic symbiotic relationship with reef-building corals. Here we applied massively parallel Illumina sequencing to assess genetic similarity and diversity among four phylogenetically diverse dinoflagellate clades (A, B, C and D) that are commonly associated with corals. We obtained more than 30,000 predicted genes for each Symbiodinium clade, with a majority of the aligned transcripts corresponding to sequence data sets of symbiotic dinoflagellates and <2% of sequences having bacterial or other foreign origin. We report 1053 genes, orthologous among four Symbiodinium clades, that share a high level of sequence identity to known proteins from the SwissProt (SP) database. Approximately 80% of the transcripts aligning to the 1053 SP genes were unique to Symbiodinium species and did not align to other dinoflagellates and unrelated eukaryotic transcriptomes/genomes. Six pathways were common to all four Symbiodinium clades including the phosphatidylinositol signaling system and inositol phosphate metabolism pathways. The list of Symbiodinium transcripts common to all four clades included conserved genes such as heat shock proteins (Hsp70 and Hsp90), calmodulin, actin and tubulin, several ribosomal, photosynthetic and cytochrome genes and chloroplast-based heme-containing cytochrome P450, involved in the biosynthesis of xanthophylls. Antioxidant genes, which are important in stress responses, were also preserved, as were a number of calcium-dependent and calcium/calmodulin-dependent protein kinases that may play a role in the establishment of symbiosis. Our findings disclose new knowledge about the genetic uniqueness of symbiotic dinoflagellates and provide a list of homologous genes important for the foundation of coral-algal symbiosis.
Project description:Reef-building corals form an obligate symbiosis with photosynthetic microalgae in the family Symbiodiniaceae that meet most of their energy requirements. This symbiosis is under threat from the unprecedented rate of ocean warming as well as the simultaneous pressure of local stressors such as poor water quality. Only 1°C above mean summer sea surface temperatures (SSTs) on the Great Barrier Reef (GBR) can trigger the loss of Symbiodiniaceae from the host, and very low concentrations of the most common herbicide, diuron, can disrupt the photosynthetic activity of microalgae. In an era of rapid environmental change, investigation into the assisted evolution of the coral holobiont is underway in an effort to enhance the resilience of corals. Apicomplexan-like microalgae were discovered in 2008 and the Phylum Chromerida (chromerids) was created. Chromerids have been isolated from corals and contain a functional photosynthetic plastid. Their discovery therefore opens a new avenue of research into the use of alternative/additional photosymbionts of corals. However, only two studies to-date have investigated the symbiotic nature of Chromera velia with corals and thus little is known about the coral-chromerid relationship. Furthermore, the response of chromerids to environmental stressors has not been examined. Here we tested the performance of four chromerid strains and the common dinoflagellate symbiont Cladocopium goreaui (formerly Symbiodinium goreaui, ITS2 type C1) in response to elevated temperature, diuron and their combined exposure. Three of the four chromerid strains exhibited high thermal tolerances and two strains showed exceptional herbicide tolerances, greater than observed for any photosynthetic microalgae, including C. goreaui. We also investigated the onset of symbiosis between the chromerids and larvae of two common GBR coral species under ambient and stress conditions. Levels of colonization of coral larvae with the chromerid strains were low compared to colonization with C. goreaui. We did not observe any overall negative or positive larval fitness effects of the inoculation with chromerid algae vs. C. goreaui. However, we cannot exclude the possibility that chromerid algae may have more important roles in later coral life stages and recommend this be the focus of future studies.
Project description:The adaptative bleaching hypothesis (ABH) states that, depending on the symbiotic flexibility of coral hosts (i.e., the ability of corals to "switch" or "shuffle" their algal symbionts), coral bleaching can lead to a change in the composition of their associated Symbiodinium community and, thus, contribute to the coral's overall survival. In order to determine the flexibility of corals, molecular tools are required to provide accurate species delineations and to detect low levels of coral-associated Symbiodinium. Here, we used highly sensitive quantitative (real-time) PCR (qPCR) technology to analyse five common coral species from Moorea (French Polynesia), previously screened using only traditional molecular methods, to assess the presence of low-abundance (background) Symbiodinium spp. Similar to other studies, each coral species exhibited a strong specificity to a particular clade, irrespective of the environment. In addition, however, each of the five species harboured at least one additional Symbiodinium clade, among clades A-D, at background levels. Unexpectedly, and for the first time in French Polynesia, clade B was detected as a coral symbiont. These results increase the number of known coral-Symbiodinium associations from corals found in French Polynesia, and likely indicate an underestimation of the ability of the corals in this region to associate with and/or "shuffle" different Symbiodinium clades. Altogether our data suggest that corals from French Polynesia may favor a trade-off between optimizing symbioses with a specific Symbiodinium clade(s), maintaining associations with particular background clades that may play a role in the ability of corals to respond to environmental change.
Project description:Ocean acidification (OA) is expected to negatively affect coral reefs, however little is known about how OA will change the coral-algal symbiosis on which reefs ultimately depend. This study investigated whether there would be differences in coral Symbiodinium types in response to OA, potentially improving coral performance. We used denaturing gradient gel electrophoresis (DGGE) of the internal transcribed spacer 2 (ITS2) region of ribosomal DNA to investigate the dominant types of Symbiodinium associating with six species of scleractinian coral that were exposed to elevated partial pressures of carbon dioxide (pCO2) in situ from settlement and throughout their lives. The study was conducted at three naturally occurring volcanic CO2 seeps (pCO2 ?500 to 900 ppm, pHTotal 7.8 - 7.9) and adjacent control areas (pCO2 ?390 ppm, pHTotal ?8.0 - 8.05) in Papua New Guinea. The Symbiodinium associated with corals living in an extreme seep site (pCO2 >1000 ppm) were also examined. Ten clade C types and three clade D types dominated the 443 coral samples. Symbiodinium types strongly contrasted between coral species, however, no differences were observed due to CO2 exposure. Within five species, 85 - 95% of samples exhibited the same Symbiodinium type across all sites, with remaining rare types having no patterns attributable to CO2 exposure. The sixth species of coral displayed site specific differences in Symbiodinium types, unrelated to CO2 exposure. Symbiodinium types from the coral inhabiting the extreme CO2 seep site were found commonly throughout the moderate seeps and control areas. Our finding that symbiotic associations did not change in response to CO2 exposure suggest that, within the six coral hosts, none of the investigated 13 clade C and D Symbiodinium types had a selective advantage at high pCO2. Acclimatisation through changing symbiotic association therefore does not seem to be an option for Indo-Pacific corals to deal with future OA.
Project description:The profound mutualistic symbiosis between corals and their endosymbiotic counterparts, Symbiodiniaceae algae, has been threatened by the increase in seawater temperatures, leading to breakdown of the symbiotic relationship-coral bleaching. To characterize the heat-stress response of the holobiont, we generated vital apo-symbiotic Euphyllia paradivisa corals that lacked the endosymbiotic algae. Using RNA sequencing, we analyzed the gene expression of these apo-symbionts vs. symbiotic ones, to test the effect of the algal presence on the tolerance of the coral. We utilized literature-derived lists of "symbiosis differentially expressed genes" and "coral heat-stress genes" in order to compare between the treatments. The symbiotic and apo-symbiotic samples were segregated into two separate groups with several different enriched gene ontologies. Our findings suggest that the presence of endosymbionts has a greater negative impact on the host than the environmental temperature conditions experienced by the holobiont. The peak of the stress reaction was identified as 28 °C, with the highest number of differentially expressed genes. We suggest that the algal symbionts increase coral holobiont susceptibility to elevated temperatures. Currently, we can only speculate whether coral species, such as E. paradivisa, with the plasticity to also flourish as apo-symbionts, may have a greater chance to withstand the upcoming global climate change challenge.
Project description:Coral reefs are based on the symbiotic relationship between corals and photosynthetic dinoflagellates of the genus Symbiodinium. We followed gene expression of coral larvae of Acropora palmata and Montastraea faveolata after exposure to Symbiodinium strains that differed in their ability to establish symbioses. We show that the coral host transcriptome remains almost unchanged during infection by competent symbionts, but is massively altered by symbionts that fail to establish symbioses. Our data suggest that successful coral-algal symbioses depend mainly on the symbionts' ability to enter the host in a stealth manner rather than a more active response from the coral host. Acropora palmata Samples: Three biological replicates of pooled larvae from each species and condition (i.e. untreated control, inoculated with competent Symbiodinium strain, inoculated with incompetent Symbiodinium strain) for both time points were hybridized against a pooled reference. Pooled references were constructed by combining equal amounts of aRNA from all control samples from A. palmata. References were labeled with Cy3, samples with Cy5. Montastraea faveolata Samples: Three biological replicates of pooled larvae from each species and condition (i.e. untreated control, inoculated with competent Symbiodinium strain, inoculated with incompetent Symbiodinium strain) for both time points were hybridized against a pooled reference. Pooled references were constructed by combining equal amounts of aRNA from all control samples from M. faveolata. References were labeled with Cy3, samples with Cy5. Symbiodinium sp. CassKB8: competent strain Symbiodinium sp. EL1: incompetent strain Symbiodinium sp. Mf1.05b: competent strain
Project description:Symbioses are widespread in nature and occur along a continuum from parasitism to mutualism. Coral-dinoflagellate symbioses are defined as mutualistic because both partners receive benefit from the association via the exchange of nutrients. This successful interaction underpins the growth and formation of coral reefs. The symbiotic dinoflagellate genus Symbiodinium is genetically diverse containing eight divergent lineages (clades A-H). Corals predominantly associate with clade C Symbiodinium and to a lesser extent with clades A, B, D, F, and G. Variation in the function and interactive physiology of different coral-dinoflagellate assemblages is virtually unexplored but is an important consideration when developing the contextual framework of factors that contribute to coral reef resilience. In this study, we present evidence that clade A Symbiodinium are functionally less beneficial to corals than the dominant clade C Symbiodinium and may represent parasitic rather than mutualistic symbionts. Our hypothesis is supported by (i) a significant correlation between the presence of Symbiodinium clade A and health-compromised coral; (ii) a phylogeny and genetic diversity within Symbiodinium that suggests a different evolutionary trajectory for clade A compared with the other dominant Symbiodinium lineages; and (iii) a significantly lower amount of carbon fixed and released by clade A in the presence of a coral synthetic host factor as compared with the dominant coral symbiont lineage, clade C. Collectively, these data suggest that along the symbiotic continuum the interaction between clade A Symbiodinium and corals may be closer to parasitism than mutualism.