Climate change promotes parasitism in a coral symbiosis.

Coastal oceans are increasingly eutrophic, warm and acidic through the addition of anthropogenic nitrogen and carbon, respectively. Among the most sensitive taxa to these changes are scleractinian corals, which engineer the most biodiverse ecosystems on Earth. Corals' sensitivity is a consequence of their evolutionary investment in symbiosis with the dinoflagellate alga, Symbiodinium. Together, the coral holobiont has dominated oligotrophic tropical marine habitats. However, warming destabilizes this association and reduces coral fitness. It has been theorized that, when reefs become warm and eutrophic, mutualistic Symbiodinium sequester more resources for their own growth, thus parasitizing their hosts of nutrition. Here, we tested the hypothesis that sub-bleaching temperature and excess nitrogen promotes symbiont parasitism by measuring respiration (costs) and the assimilation and translocation of both carbon (energy) and nitrogen (growth; both benefits) within Orbicella faveolata hosting one of two Symbiodinium phylotypes using a dual stable isotope tracer incubation at ambient (26 °C) and sub-bleaching (31 °C) temperatures under elevated nitrate. Warming to 31 °C reduced holobiont net primary productivity (NPP) by 60% due to increased respiration which decreased host %carbon by 15% with no apparent cost to the symbiont. Concurrently, Symbiodinium carbon and nitrogen assimilation increased by 14 and 32%, respectively while increasing their mitotic index by 15%, whereas hosts did not gain a proportional increase in translocated photosynthates. We conclude that the disparity in benefits and costs to both partners is evidence of symbiont parasitism in the coral symbiosis and has major implications for the resilience of coral reefs under threat of global change

Building consensus around the assessment and interpretation of Symbiodiniaceae diversity

Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.journal articl

Building consensus around the assessment and interpretation of Symbiodiniaceae diversity

Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships

Part 1 of a 2 part manipulative experiment to investigate the existence of cooperative synergy in defensive behaviors of ‘guard’ crustaceans at Gump Research Station, Moorea, French Polynesia from July 2006 (CDD_in_Reef_Fish project)

Dataset: McKeon_et_al_2012 Multiple Defender EffectsPart 1 of a 2 part manipulative experiment to investigate the existence of cooperative synergy in defensive behaviors of ‘guard’ crustaceans at Gump Research Station, Moorea, French Polynesia from July 2006 (CDD_in_Reef_Fish project). For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/727093NSF Division of Ocean Sciences (NSF OCE) OCE-024231

Competition and succession among coral endosymbionts

Host species often support a genetically diverse guild of symbionts, the identity and performance of which can determine holobiont fitness under particular environmental conditions. These symbiont communities are structured by a complex set of potential interactions, both positive and negative, between the host and symbionts and among symbionts. In reef‐building corals, stable associations with specific symbiont species are common, and we hypothesize that this is partly due to ecological mechanisms, such as succession and competition, which drive patterns of symbiont winnowing in the initial colonization of new generations of coral recruits. We tested this hypothesis using the experimental framework of the de Wit replacement series and found that competitive interactions occurred among symbionts which were characterized by unique ecological strategies. Aposymbiotic octocoral recruits within high‐ and low‐light environments were inoculated with one of three Symbiodiniaceae species as monocultures or with cross‐paired mixtures, and we tracked symbiont uptake using quantitative genetic assays. Priority effects, in which early colonizers excluded competitive dominants, were evidenced under low light, but these early opportunistic species were later succeeded by competitive dominants. Under high light, a more consistent competitive hierarchy was established in which competitive dominants outgrew and limited the abundance of others. These findings provide insight into mechanisms of microbial community organization and symbiosis breakdown and recovery. Furthermore, transitions in competitive outcomes across spatial and temporal environmental variation may improve lifetime host fitness. Reef‐building corals rely on a genetically diverse group of dinoflagellate symbionts to meet their nutritional needs. The ecological mechanisms that regulate symbiont communities are not well understood. Here, we show that competition and succession among symbiont species are important in the early stages of the symbiosis

Comparative growth rates of cultured marine dinoflagellates in the genus Symbiodinium and the effects of temperature and light.

Many dinoflagellate microalgae of the genus Symbiodinium form successful symbioses with a large group of metazoans and selected protists. Yet knowledge of growth kinetics of these endosymbionts and their ecological and evolutionary implications is limited. We used a Bayesian biphasic generalized logistic model to estimate key parameters of the growth of five strains of cultured Symbiodinium, S. microadriaticum (cp-type A194; strain 04-503), S. microadriaticum (cp-type A194; strain CassKB8), S. minutum (cp-type B184; strain Mf 1.05b.01.SCI.01), S. psygmophilum (cp-type B224; strain Mf 11.05b.01) and S. trenchii (cp-type D206; strain Mf 2.2b), grown in four different combinations of temperature and light. Growth kinetics varied among Symbiodinium strains and across treatments. Biphasic growth was especially evident for S. minutum and S. psygmophilum across all treatments. Monophasic growth was more common when final asymptotic densities were relatively low (~ 200 million cells ml-1). All species tended to grow faster and / or reached a higher asymptote at 26°C than at 18°C. The fastest growth was exhibited by S. minutum, with an approximate four-fold increase in estimated cell density after 60 days. The strongest effect of light was seen in S. trenchii, in which increasing light levels resulted in a decrease in initial growth rate, and an increase in asymptotic density, time when growth rate was at its maximum, final growth rate, and maximum growth rate. Results suggest that Symbiodinium species have different photokinetic and thermal optima, which may affect their growth-related nutritional physiology and allow them to modify their response to environmental changes

Additional file 1 of Nutrient dynamics in coral symbiosis depend on both the relative and absolute abundance of Symbiodiniaceae species

Additional file 1: Table S1. Nutrient and isotopic compositions of artificial seawater media used for each stage of the experiment. Concentrations were based on Tanaka et al. (2006). All compounds were manufactured and purchased from Sigma-Aldrich ® (St. Louis, MO, USA). Fig. S1. Isotope baseline and dark controls. A set of recruits was tested to provide a baseline isotope value and to confirm that symbionts were the primer drivers of inorganic carbon and nitrogen into the symbiosis. Baseline recruits were sampled prior to the start of the experiment, Dark Enriched samples were exposed to isotopically enriched enriched nutriens but kept in the dark to inhibit photosynthesis; Enriched samples show the cumulative data from the final experiment. Fig. S2. The significant interaction effect of symbiont ratio and symbiont density on atom percent 13C values of symbiont tissues was examined by plotting the marginal effect of symbiont ratio (S.m.:B.m.) as moderated by symbiont density (cells/recruit). Green bar indicates the range of symbiont densities in which there is a significant positive effect of symbiont ratio on AP13Csym. Gray area shows the 95% CI. Fig. S3. The significant interaction effect of symbiont ratio and symbiont density on atom percent 15N values of host tissues was examined by plotting the marginal effect of symbiont density as moderated by symbiont ratio (S.m.:B.m.). Red bar indicates the range of symbiont ratios in which there is a significant negative effect of symbiont density on AP15Nhost. Gray area shows 95% CI. Fig. S4. The significant interaction effect of symbiont ratio and symbiont density on atom percent 15N values of symbiont tissues was examined by plotting the marginal effect of symbiont ratio (S.m.:B.m.) as moderated by symbiont density (cells/recruit). Red bar indicates the range of symbiont densities in which there is a significant negative effect of symbiont ratio on AP15Nsym. Gray area shows the 95% CI. Fig. S5. The significant interaction effect of symbiont ratio and symbiont density on atom percent 15N values of symbiont tissues was examined by plotting the marginal effect of symbiont density as moderated by symbiont ratio (S.m.:B.m.). Red bar indicates the range of symbiont ratios in which there is a significant negative effect of symbiont density on AP15Nsym. Gray area shows 95% CI. Fig. S6. The significant interaction effect of symbiont ratio and symbiont density on total assimilated nitrogen (mg/recruit) was examined by plotting the marginal effect of symbiont density as moderated by symbiont ratio (S.m.:B.m.). Red bar indicates the range of symbiont ratios in which there is a significant negative effect of symbiont density on total assimialted nitrogen. Gray area shows 95% CI

cp23s fragment analysis

Raw fragment length data for cp32s-rDN

The reef-building coral Galaxea fascicularis: a new model system for coral symbiosis research

Reef-building corals owe their evolutionary success to their symbiosis with unicellular algae (Symbiodiniaceae). However, increasingly frequent heat waves lead to coral mass-bleaching events and pose a serious threat to the survival of reef ecosystems. Despite significant efforts, a mechanistic understanding of coral–algal symbiosis functioning, what leads to its breakdown and what can prevent it, remains incomplete. The main obstacles are low amenability of corals to experimental handling and, owing to its obligatory nature, the difficulties of manipulating the coral–algal association. Indeed, many studies on the symbiotic partnership are conducted on other cnidarian model organisms and their results may therefore not be fully transferable to tropical reef-building corals. Here, we identify the tropical stony coral species Galaxea fascicularis as a novel candidate coral model system. Individual polyps of this species can be separated, enabling highly replicated genotype studies, and are well suited to experimental investigation of the symbiosis as they can be easily and effectively rid of their algal symbionts (bleached). We show that bleached adult individuals can reestablish symbiosis with non-native symbionts, and we report the completion of the gametogenic cycle ex situ, with the successful spawning in aquaria over multiple years. These achievements help overcome several of the major limitations to direct research on corals and highlight the potential of G. fascicularis as an important new model system for investigations of symbiosis functioning and manipulation