Optimal nutrient exchange and immune responses operate in partner specificity in the cnidarian-dinoflagellate symbiosis.
ABSTRACT: The relationship between corals and dinoflagellates of the genus Symbiodinium is fundamental to the functioning of coral ecosystems. It has been suggested that reef corals may adapt to climate change by changing their dominant symbiont type to a more thermally tolerant one, although the capacity for such a shift is potentially hindered by the compatibility of different host-symbiont pairings. Here we combined transcriptomic and metabolomic analyses to characterize the molecular, cellular, and physiological processes that underlie this compatibility, with a particular focus on Symbiodinium trenchii, an opportunistic, thermally tolerant symbiont that flourishes in coral tissues after bleaching events. Symbiont-free individuals of the sea anemone Exaiptasia pallida (commonly referred to as Aiptasia), an established model system for the study of the cnidarian-dinoflagellate symbiosis, were colonized with the "normal" (homologous) symbiont Symbiodinium minutum and the heterologous S. trenchii Analysis of the host gene and metabolite expression profiles revealed that heterologous symbionts induced an expression pattern intermediate between the typical symbiotic state and the aposymbiotic state. Furthermore, integrated pathway analysis revealed that increased catabolism of fixed carbon stores, metabolic signaling, and immune processes occurred in response to the heterologous symbiont type. Our data suggest that both nutritional provisioning and the immune response induced by the foreign "invader" are important factors in determining the capacity of corals to adapt to climate change through the establishment of novel symbioses.
Project description:Reef corals and sea anemones form symbioses with unicellular symbiotic dinoflagellates. The molecular circumventions that underlie the successful intracellular colonization of hosts by symbionts are still largely unknown. We conducted proteomic analyses to determine molecular differences of Exaiptasia pallida anemones colonized by physiologically different symbiont species, in comparison with symbiont-free (aposymbiotic) anemones. We compared one homologous species, Symbiodinium linucheae, that is natively associated with the clonal Exaiptasia strain (CC7) to another heterologous species, Durusdinium trenchii, a thermally tolerant species that colonizes numerous coral species. This approach allowed the discovery of a core set of host genes that are differentially regulated as a function of symbiosis regardless of symbiont species. The findings revealed that symbiont colonization at higher densities requires circumvention of the host cellular immunological response, enhancement of ammonium regulation, and suppression of phagocytosis after a host cell in colonized. Furthermore, the heterologous symbionts failed to duplicate the same level of homologous colonization within the host, evidenced by substantially lower symbiont densities. This reduced colonization of D. trenchii correlated with its inability to circumvent key host systems including autophagy-suppressing modulators, cytoskeletal alteration, and isomerase activity. The larger capability of host molecular circumvention by homologous symbionts could be the result of a longer evolutionary history of host/symbiont interactions, which translates into a more finely tuned symbiosis. These findings are of great importance within the context of the response of reef corals to climate change since it has been suggested that coral may acclimatize to ocean warming by changing their dominant symbiont species.
Project description:The acquisition of thermally tolerant algal symbionts by corals has been proposed as a natural or assisted mechanism of increasing coral reef resilience to anthropogenic climate change, but the cell-level processes determining the performance of new symbiotic associations are poorly understood. We used liquid chromatography-mass spectrometry to investigate the effects of an experimentally induced symbiosis on the host proteome of the model sea anemone Exaiptasia pallida. Aposymbiotic specimens were colonised by either the homologous dinoflagellate symbiont (Breviolum minutum) or a thermally tolerant, ecologically invasive heterologous symbiont (Durusdinium trenchii). Anemones containing D. trenchii exhibited minimal expression of Niemann-Pick C2 proteins, which have predicted biochemical roles in sterol transport and cell recognition, and glutamine synthetases, which are thought to be involved in nitrogen assimilation and recycling between partners. D. trenchii-colonised anemones had higher expression of methionine-synthesising betaine-homocysteine S-methyltransferases and proteins with predicted oxidative stress response functions. Multiple lysosome-associated proteins were less abundant in both symbiotic treatments compared with the aposymbiotic treatment. The differentially abundant proteins are predicted to represent pathways that may be involved in nutrient transport or resource allocation between partners. These results provide targets for specific experiments to elucidate the mechanisms underpinning compensatory physiology in the coral-dinoflagellate symbiosis.
Project description:Human-induced environmental changes have ushered in the rapid decline of coral reef ecosystems, particularly by disrupting the symbioses between reef-building corals and their photosymbionts. However, escalating stressful conditions enable some symbionts to thrive as opportunists. We present evidence that a stress-tolerant "zooxanthella" from the Indo-Pacific Ocean, Symbiodinium trenchii, has rapidly spread to coral communities across the Greater Caribbean. In marked contrast to populations from the Indo-Pacific, Atlantic populations of S. trenchii contained exceptionally low genetic diversity, including several widespread and genetically similar clones. Colonies with this symbiont tolerate temperatures 1-2 °C higher than other host-symbiont combinations; however, calcification by hosts harboring S. trenchii is reduced by nearly half, compared with those harboring natives, and suggests that these new symbioses are maladapted. Unforeseen opportunism and geographical expansion by invasive mutualistic microbes could profoundly influence the response of reef coral symbioses to major environmental perturbations but may ultimately compromise ecosystem stability and function.
Project description:The 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.
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:The ability of corals and other cnidarians to survive climate change depends partly on the composition of their endosymbiont communities. The dinoflagellate family Symbiodiniaceae is genetically and physiologically diverse, and one proposed mechanism for cnidarians to acclimate to rising temperatures is to acquire more thermally tolerant symbionts. However, cnidarian-dinoflagellate associations vary in their degree of specificity, which may limit their capacity to alter symbiont communities. Here, we inoculated symbiont-free polyps of the sea anemone Exaiptasia pallida (commonly referred to as 'Aiptasia'), a model system for the cnidarian-dinoflagellate symbiosis, with simultaneous or sequential mixtures of thermally tolerant and thermally sensitive species of Symbiodiniaceae. We then monitored symbiont success (relative proportional abundance) at normal and elevated temperatures across two to four weeks. All anemones showed signs of bleaching at high temperature. During simultaneous inoculations, the native, thermally sensitive Breviolum minutum colonized polyps most successfully regardless of temperature when paired against the non-native but more thermally tolerant Symbiodinium microadriaticum or Durusdinium trenchii. Furthermore, anemones initially colonized with B. minutum and subsequently exposed to S. microadriaticum failed to acquire the new symbiont. These results highlight how partner specificity may place strong limitations on the ability of certain cnidarians to acquire more thermally tolerant symbionts, and hence their adaptive potential under climate change.
Project description:The physiological response to individual and combined stressors of elevated temperature and pCO2 were measured over a 24-day period in four Pacific corals and their respective symbionts (Acropora millepora/Symbiodinium C21a, Pocillopora damicornis/Symbiodinium C1c-d-t, Montipora monasteriata/Symbiodinium C15, and Turbinaria reniformis/Symbiodinium trenchii). Multivariate analyses indicated that elevated temperature played a greater role in altering physiological response, with the greatest degree of change occurring within M. monasteriata and T. reniformis. Algal cellular volume, protein, and lipid content all increased for M. monasteriata. Likewise, S. trenchii volume and protein content in T. reniformis also increased with temperature. Despite decreases in maximal photochemical efficiency, few changes in biochemical composition (i.e. lipids, proteins, and carbohydrates) or cellular volume occurred at high temperature in the two thermally sensitive symbionts C21a and C1c-d-t. Intracellular carbonic anhydrase transcript abundance increased with temperature in A. millepora but not in P. damicornis, possibly reflecting differences in host mitigated carbon supply during thermal stress. Importantly, our results show that the host and symbiont response to climate change differs considerably across species and that greater physiological plasticity in response to elevated temperature may be an important strategy distinguishing thermally tolerant vs. thermally sensitive species.
Project description:Coral reefs are threatened by climate change as coral-algal symbioses are currently living close to their upper thermal limits. The resilience of the algal partner plays a key role in determining the thermal tolerance of the coral holobiont and therefore, understanding the acclimatory limits of present day coral-algal symbioses is fundamental to forecasting corals' responses to climate change. This study characterised the symbiont community in a highly variable and thermally extreme (Max?=?37.5?°C, Min?=?16.8?°C) lagoon located in the southern Persian/Arabian Gulf using next generation sequencing of ITS2 amplicons. Despite experiencing extreme temperatures, severe bleaching and many factors that would be expected to promote the presence of, or transition to clade D dominance, the symbiont communities of the lagoon remain dominated by the C3 variant, Symbiodinium thermophilum. The stability of this symbiosis across multiple genera with different means of symbiont transmission highlights the importance of Symbiodinium thermophilum for corals living at the acclimatory limits of modern day corals. Corals in this extreme environment did not undergo adaptive bleaching, suggesting they are living at the edge of their acclimatory potential and that this valuable source of thermally tolerant genotypes may be lost in the near future under climate change.
Project description:Coral reefs are in rapid decline on a global scale due to human activities and a changing climate. Shallow water reefs depend on the obligatory symbiosis between the habitat forming coral host and its algal symbiont from the genus Symbiodinium (zooxanthellae). This association is highly sensitive to thermal perturbations and temperatures as little as 1°C above the average summer maxima can cause the breakdown of this symbiosis, termed coral bleaching. Predicting the capacity of corals to survive the expected increase in seawater temperatures depends strongly on our understanding of the thermal tolerance of the symbiotic algae. Here we use molecular phylogenetic analysis of four genetic markers to describe Symbiodinium thermophilum, sp. nov. from the Persian/Arabian Gulf, a thermally tolerant coral symbiont. Phylogenetic inference using the non-coding region of the chloroplast psbA gene resolves S. thermophilum as a monophyletic lineage with large genetic distances from any other ITS2 C3 type found outside the Gulf. Through the characterisation of Symbiodinium associations of 6 species (5 genera) of Gulf corals, we demonstrate that S. thermophilum is the prevalent symbiont all year round in the world's hottest sea, the southern Persian/Arabian Gulf.
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.