Comparing the effects of symbiotic algae (Symbiodinium) clades C1 and D on early growth stages of Acropora tenuis.
ABSTRACT: 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: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:BACKGROUND: Reef-building corals live in symbiosis with a diverse range of dinoflagellate algae (genus Symbiodinium) that differentially influence the fitness of the coral holobiont. The comparative role of symbiont type in holobiont fitness in relation to host genotype or the environment, however, is largely unknown. We addressed this knowledge gap by manipulating host-symbiont combinations and comparing growth, survival and thermal tolerance among the resultant holobionts in different environments. METHODOLOGY/PRINCIPAL FINDINGS: Offspring of the coral, Acropora millepora, from two thermally contrasting locations, were experimentally infected with one of six Symbiodinium types, which spanned three phylogenetic clades (A, C and D), and then outplanted to the two parental field locations (central and southern inshore Great Barrier Reef, Australia). Growth and survival of juvenile corals were monitored for 31-35 weeks, after which their thermo-tolerance was experimentally assessed. Our results showed that: (1) Symbiodinium type was the most important predictor of holobiont fitness, as measured by growth, survival, and thermo-tolerance; (2) growth and survival, but not heat-tolerance, were also affected by local environmental conditions; and (3) host population had little to no effect on holobiont fitness. Furthermore, coral-algal associations were established with symbiont types belonging to clades A, C and D, but three out of four symbiont types belonging to clade C failed to establish a symbiosis. Associations with clade A had the lowest fitness and were unstable in the field. Lastly, Symbiodinium types C1 and D were found to be relatively thermo-tolerant, with type D conferring the highest tolerance in A. millepora. CONCLUSIONS/SIGNIFICANCE: These results highlight the complex interactions that occur between the coral host, the algal symbiont, and the environment to shape the fitness of the coral holobiont. An improved understanding of the factors affecting coral holobiont fitness will assist in predicting the responses of corals to global climate change.
Project description:Ocean warming is a major threat to coral reefs, leading to an increasing frequency and amplitude of coral bleaching events, where the coral and its algal symbiont associations breakdown. Long-term change and resilience of a symbiont community in coral juveniles is thought to be one of the most important aspects for determining thermal tolerance of the coral holobionts; however, despite its importance, they are not well documented in both under elevated temperature and even under natural condition. Here we investigated changes in symbiont communities in juveniles of the coral Acropora tenuis under controlled heat stress conditions (30 °C, 31/32 °C) and natural variations in seawater temperatures (19-30 °C) for up to four months. Compared with the ambient temperature conditions, coral survival rates were higher when exposed to 30 °C, but survival rates decreased when exposed to 31/32 °C. Symbiodinium types A3, C1, and D1-4 were detected in the juveniles under all thermal conditions; however, in higher water temperatures (31/32 °C), both the prevalence of D1-4 Symbiodinium and the number of juveniles harboring only this type of symbiont increased after two to four months later. In contrast, colonies at lower temperatures (30 °C and ambient) harbored multiple clades of symbionts over the same experimental period. These results highlight the flexibility of the coral-Symbiodinium symbiosis for juvenile A. tenuis under variable thermal conditions. In particular, the benefit of the preferential association with type D1-4 can be considered as a response when under heat-stress conditions, and that could help corals to cope with ocean warming.
Project description:BACKGROUND: The symbiosis between reef-building corals and photosynthetic dinoflagellates (Symbiodinium) is an integral part of the coral reef ecosystem, as corals are dependent on Symbiodinium for the majority of their energy needs. However, this partnership is increasingly at risk due to changing climatic conditions. It is thought that functional diversity within Symbiodinium may allow some corals to rapidly adapt to different environments by changing the type of Symbiodinium with which they partner; however, very little is known about the molecular basis of the functional differences among symbiont groups. One group of Symbiodinium that is hypothesized to be important for the future of reefs is clade D, which, in general, seems to provide the coral holobiont (i.e., coral host and associated symbiont community) with elevated thermal tolerance. Using high-throughput sequencing data from field-collected corals we assembled, de novo, draft transcriptomes for Symbiodinium clades C and D. We then explore the functional basis of thermal tolerance in clade D by comparing rates of coding sequence evolution among the four clades of Symbiodinium most commonly found in reef-building corals (A-D). RESULTS: We are able to highlight a number of genes and functional categories as candidates for involvement in the increased thermal tolerance of clade D. These include a fatty acid desaturase, molecular chaperones and proteins involved in photosynthesis and the thylakoid membrane. We also demonstrate that clades C and D co-occur within most of the sampled colonies of Acropora hyacinthus, suggesting widespread potential for this coral species to acclimatize to changing thermal conditions via 'shuffling' the proportions of these two clades from within their current symbiont communities. CONCLUSIONS: Transcriptome-wide analysis confirms that the four main Symbiodinium clades found within corals exhibit extensive evolutionary divergence (18.5-27.3% avg. pairwise nucleotide difference). Despite these evolutionary distinctions, many corals appear to host multiple clades simultaneously, which may allow for rapid acclimatization to changing environmental conditions. This study provides a first step toward understanding the molecular basis of functional differences between Symbiodinium clades by highlighting a number of genes with signatures consistent with positive selection along the thermally tolerant clade D lineage.
Project description:Photoinhibition, exacerbated by elevated temperatures, underlies coral bleaching, but sensitivity to photosynthetic loss differs among various phylotypes of Symbiodinium, their dinoflagellate symbionts. Symbiodinium is a common symbiont in many cnidarian species including corals, jellyfish, anemones, and giant clams. Here, we provide evidence that most members of clade A Symbiodinium, but not clades B-D or F, exhibit enhanced capabilities for alternative photosynthetic electron-transport pathways including cyclic electron transport (CET). Unlike other clades, clade A Symbiodinium also undergo pronounced light-induced dissociation of antenna complexes from photosystem II (PSII) reaction centers. We propose these attributes promote survival of most cnidarians with clade A symbionts at high light intensities and confer resistance to bleaching conditions that conspicuously impact deeper dwelling corals that harbor non-clade A Symbiodinium.
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:Many reef-building corals form symbioses with dinoflagellates from the diverse genus Symbiodinium. There is increasing evidence of functional significance to Symbiodinium diversity, which affects the coral holobiont's response to changing environmental conditions. For example, corals hosting Symbiodinium from the clade D taxon exhibit greater resistance to heat-induced coral bleaching than conspecifics hosting the more common clade C. Yet, the relatively low prevalence of clade D suggests that this trait is not advantageous in non-stressful environments. Thus, clade D may only be able to out-compete other Symbiodinium types within the host habitat when conditions are chronically stressful. Previous studies have observed enhanced photosynthesis and fitness by clade C holobionts at non-stressful temperatures, relative to clade D. Yet, carbon-centered metrics cannot account for enhanced growth rates and patterns of symbiont succession to other genetic types when nitrogen often limits reef productivity. To investigate the metabolic costs of hosting thermally tolerant symbionts, we examined the assimilation and translocation of inorganic (15)N and (13)C in the coral Acropora tenuis experimentally infected with either clade C (sub-type C1) or D Symbiodinium at 28 and 30 °C. We show that at 28 °C, C1 holobionts acquired 22% more (15)N than clade D. However, at 30 °C, C1 symbionts acquired equivalent nitrogen and 16% less carbon than D. We hypothesize that C1 competitively excludes clade D in hospite via enhanced nitrogen acquisition and thus dominates coral populations despite warming oceans.
Project description:The success of coral reef ecosystems largely depends on mutualistic symbiosis between scleractinian corals and the dinoflagellate photosymbiont Symbiodinium spp. However, further investigation is needed to elucidate the flexibility of coral-algae associations in response to environmental changes. In this study, we applied a molecular method (high-throughput internal transcribed spacer 2 region of ribosomal RNA gene amplicon sequencing) to explore diversity and flexibility of Symbiodinium associated with Galaxea fascicularis, an ecologically important scleractinian coral species collected at five locations around Hainan Island, South China Sea. The results revealed a high diversity of Symbiodinium subclades with C2r and D17 being dominant in G. fascicularis. Clade D Symbiodinium occurred most frequently in habitats where the annual average sea surface temperatures are the highest, suggesting that temperature is an important factor in determining Symbiodinium D abundance in G. fascicularis. The distribution of coral-Symbiodinium associations are possibly mediated by trade-off mechanisms which change the relative abundance of Symbiodinium clades/subclades under different environmental conditions. These findings provide further evidence that reef-building corals such as G. fascicularis can shuffle their symbionts to cope with environmental changes, and have implications for our understanding of the ecology of flexible coral-algal symbiosis.
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.
Project description:Symbiodinium is best-known as the photosynthetic symbiont of corals, but some clades are symbiotic in other organisms or include free-living forms. Identifying similarities and differences among these clades can help us understand their relationship with corals, and thereby inform on measures to manage coral reefs in a changing environment. Here, using sequences from 24 publicly available transcriptomes and genomes of Symbiodinium, we assessed 78,389 gene families in Symbiodinium clades and the immediate outgroup Polarella glacialis, and identified putative overrepresented functions in gene families that (1) distinguish Symbiodinium from other members of Order Suessiales, (2) are shared by all of the Symbiodinium clades for which we have data, and (3) based on available information, are specific to each clade. Our findings indicate that transmembrane transport, mechanisms of response to reactive oxygen species, and protection against UV radiation are functions enriched in all Symbiodinium clades but not in P. glacialis. Enrichment of these functions indicates the capability of Symbiodinium to establish and maintain symbiosis, and to respond and adapt to its environment. The observed differences in lineage-specific gene families imply extensive genetic divergence among clades. Our results provide a platform for future investigation of lineage- or clade-specific adaptation of Symbiodinium to their environment.