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Corals have complex symbiotic associations that can be influenced by the environment. We compare symbiotic dinoflagellate (family: Symbiodiniaceae) associations and the microbiome of five scleractinian coral species from three different reef habitats in Palau, Micronesia. Although pH and temperature corresponded with specific host-Symbiodiniaceae associations common to the nearshore and offshore habitats, bacterial community dissimilarity analyses indicated minimal influence of these factors on microbial community membership for the corals Coelastrea aspera, Psammocora digitata, and Pachyseris rugosa. However, coral colonies sampled close to human development exhibited greater differences in microbial community diversity compared to the nearshore habitat for the coral species Coelastrea aspera, Montipora foliosa, and Pocillopora acuta, and the offshore habitat for Coelastrea aspera, while also showing less consistency in Symbiodiniaceae associations. These findings indicate the influence that habitat location has on the bacterial and Symbiodiniaceae communities comprising the coral holobiont and provide important considerations for the conservation of coral reef communities, especially for island nations with increasing human populations and development., (© 2024 The Author(s). Environmental Microbiology Reports published by John Wiley & Sons Ltd.)

Symbiotic mutualisms are essential to ecosystems and numerous species across the tree of life. For reef-building corals, the benefits of their association with endosymbiotic dinoflagellates differ within and across taxa, and nutrient exchange between these partners is influenced by environmental conditions. Furthermore, it is widely assumed that corals associated with symbionts in the genus Durusdinium tolerate high thermal stress at the expense of lower nutrient exchange to support coral growth. We traced both inorganic carbon (H 13 CO 3 - ) and nitrate ( 15 NO 3 - ) uptake by divergent symbiont species and quantified nutrient transfer to the host coral under normal temperatures as well as in colonies exposed to high thermal stress. Colonies representative of diverse coral taxa associated with Durusdinium trenchii or Cladocopium spp. exhibited similar nutrient exchange under ambient conditions. By contrast, heat-exposed colonies with D. trenchii experienced less physiological stress than conspecifics with Cladocopium spp. while high carbon assimilation and nutrient transfer to the host was maintained. This discovery differs from the prevailing notion that these mutualisms inevitably suffer trade-offs in physiological performance. These findings emphasize that many host-symbiont combinations adapted to high-temperature equatorial environments are high-functioning mutualisms; and why their increased prevalence is likely to be important to the future productivity and stability of coral reef ecosystems.

The existence of widespread species with the capacity to endure diverse, or variable, environments are of importance to ecological and genetic research, and conservation. Such "ecological generalists" are more likely to have key adaptations that allow them to better tolerate the physiological challenges of rapid climate change. Reef-building corals are dependent on endosymbiotic dinoflagellates (Family: Symbiodiniaceae) for their survival and growth. While these symbionts are biologically diverse, certain genetic types appear to have broad geographic distributions and are mutualistic with various host species from multiple genera and families in the order Scleractinia that must acquire their symbionts through horizontal transmission. Despite the considerable ecological importance of putative host-generalist symbionts, they lack formal species descriptions. In this study, we used molecular, ecological, and morphological evidence to verify the existence of five new host-generalist species in the symbiodiniacean genus Cladocopium. Their geographic distribution and prevalence among host communities corresponds to prevailing environmental conditions at both regional and local scales. The influence that each species has on host physiology may partially explain regional differences in thermal sensitivities among coral communities. The potential increased prevalence of a generalist species that endures environmental instability is a consequential ecological response to warming oceans. Large-scale shifts in symbiont dominance could ensure reef coral persistence and productivity in the near term. Ultimately, these formal designations should advance scientific communication and generate informed research questions on the physiology and ecology of coral-dinoflagellate mutualisms., (© 2023 The Authors. Journal of Phycology published by Wiley Periodicals LLC on behalf of Phycological Society of America.)

The flexibility to associate with more than one symbiont may considerably expand a host's niche breadth. Coral animals and dinoflagellate micro-algae represent one of the most functionally integrated and widespread mutualisms between two eukaryotic partners. Symbiont identity greatly affects a coral's ability to cope with extremes in temperature and light. Over its broad distribution across the Eastern Pacific, the ecologically dominant branching coral, Pocillopora grandis , depends on mutualisms with the dinoflagellates Durusdinium glynnii and Cladocopium latusorum . Measurements of skeletal growth, calcification rates, total mass increase, calyx dimensions, reproductive output and response to thermal stress were used to assess the functional performance of these partner combinations. The results show both host-symbiont combinations displayed similar phenotypes; however, significant functional differences emerged when exposed to increased temperatures. Negligible physiological differences in colonies hosting the more thermally tolerant D. glynnii refute the prevailing view that these mutualisms have considerable growth tradeoffs. Well beyond the Eastern Pacific, pocilloporid colonies with D. glynnii are found across the Pacific in warm, environmentally variable, near shore lagoonal habitats. While rising ocean temperatures threaten the persistence of contemporary coral reefs, lessons from the Eastern Pacific indicate that co-evolved thermally tolerant host-symbiont combinations are likely to expand ecologically and spread geographically to dominate reef ecosystems in the future.

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., Competing Interests: Anastazia T. Banaszak and James Davis Reimer are Academic Editors for PeerJ., (© 2023 Davies et al.)

Coral reefs are declining worldwide, yet some coral populations are better adapted to withstand reductions in pH and the rising frequency of marine heatwaves. The nearshore reef habitats of Palau, Micronesia are a proxy for a future of warmer, more acidic oceans. Coral populations in these habitats can resist, and recover from, episodes of thermal stress better than offshore conspecifics. To explore the physiological basis of this tolerance, we compared tissue biomass (ash-free dry weight cm -2 ), energy reserves (i.e., protein, total lipid, carbohydrate content), and several important lipid classes in six coral species living in both offshore and nearshore environments. In contrast to expectations, a trend emerged of many nearshore colonies exhibiting lower biomass and energy reserves than colonies from offshore sites, which may be explained by the increased metabolic demand of living in a warmer, acidic, environment. Despite hosting different dinoflagellate symbiont species and having access to contrasting prey abundances, total lipid and lipid class compositions were similar in colonies from each habitat. Ultimately, while the regulation of colony biomass and energy reserves may be influenced by factors, including the identity of the resident symbiont, kind of food consumed, and host genetic attributes, these independent processes converged to a similar homeostatic set point under different environmental conditions., (© 2023. The Author(s).)

The global impacts of climate change are evident in every marine ecosystem. On coral reefs, mass coral bleaching and mortality have emerged as ubiquitous responses to ocean warming, yet one of the greatest challenges of this epiphenomenon is linking information across scientific disciplines and spatial and temporal scales. Here we review some of the seminal and recent coral-bleaching discoveries from an ecological, physiological, and molecular perspective. We also evaluate which data and processes can improve predictive models and provide a conceptual framework that integrates measurements across biological scales. Taking an integrative approach across biological and spatial scales, using for example hierarchical models to estimate major coral-reef processes, will not only rapidly advance coral-reef science but will also provide necessary information to guide decision-making and conservation efforts. To conserve reefs, we encourage implementing mesoscale sanctuaries (thousands of km 2 ) that transcend national boundaries. Such networks of protected reefs will provide reef connectivity, through larval dispersal that transverse thermal environments, and genotypic repositories that may become essential units of selection for environmentally diverse locations. Together, multinational networks may be the best chance corals have to persist through climate change, while humanity struggles to reduce emissions of greenhouse gases to net zero., (© 2022 The Authors. Global Change Biology published by John Wiley & Sons Ltd.)

There is little information on the impacts of climate change on resource partitioning for mixotrophic phytoplankton. Here, we investigated the hypothesis that light interacts with temperature and CO2 to affect changes in growth and cellular carbon and nitrogen content of the mixotrophic dinoflagellate, Karlodinium veneficum, with increasing cellular carbon and nitrogen content under low light conditions and increased growth under high light conditions. Using a multifactorial design, the interactive effects of light, temperature and CO2 were investigated on K. veneficum at ambient temperature and CO2 levels (25°C, 375 ppm), high temperature (30°C, 375 ppm CO2), high CO2 (30°C, 750 ppm CO2), or a combination of both high temperature and CO2 (30°C, 750 ppm CO2) at low light intensities (LL: 70 μmol photons m-2 s-2) and light-saturated conditions (HL: 140 μmol photons m-2 s-2). Results revealed significant interactions between light and temperature for all parameters. Growth rates were not significantly different among LL treatments, but increased significantly with temperature or a combination of elevated temperature and CO2 under HL compared to ambient conditions. Particulate carbon and nitrogen content increased in response to temperature or a combination of elevated temperature and CO2 under LL conditions, but significantly decreased in HL cultures exposed to elevated temperature and/or CO2 compared to ambient conditions at HL. Significant increases in C:N ratios were observed only in the combined treatment under LL, suggesting a synergistic effect of temperature and CO2 on carbon assimilation, while increases in C:N under HL were driven only by an increase in CO2. Results indicate light-driven variations in growth and nutrient acquisition strategies for K. veneficum that may benefit this species under anticipated climate change conditions (elevated light, temperature and pCO2) while also affecting trophic transfer efficiency during blooms of this species., Competing Interests: The authors have declared that no competing interests exist.

Reef-building corals in the genus Porites are one of the most important constituents of Indo-Pacific reefs. Many species within this genus tolerate abnormally warm water and exhibit high specificity for particular kinds of endosymbiotic dinoflagellates that cope with thermal stress better than those living in other corals. Still, during extreme ocean heating, some Porites exhibit differences in their stress tolerance. While corals have different physiological qualities, it remains unknown whether the stability and performance of these mutualisms is influenced by the physiology and genetic relatedness of their symbionts. We investigated two ubiquitous Pacific reef corals, Porites rus and Porites cylindrica, from warmer inshore and cooler offshore reef systems in Palau. While these corals harbored a similar kind of symbiont in the genus Cladocopium (within the ITS2 C15 subclade), rapidly evolving genetic markers revealed evolutionarily diverged lineages corresponding to each Porites species living in each reef habitat. Furthermore, these closely related Cladocopium lineages were differentiated by their densities in host tissues, cell volume, chlorophyll concentration, gross photosynthesis, and photoprotective pathways. When assessed using several physiological proxies, these previously undifferentiated symbionts contrasted in their tolerance to thermal stress. Symbionts within P. cylindrica were relatively unaffected by exposure to 32℃ for 14 days, whereas P. rus colonies lost substantial numbers of photochemically compromised symbionts. Heating reduced the ability of the offshore symbiont associated with P. rus to translocate carbon to the coral. By contrast, high temperatures enhanced symbiont carbon assimilation and delivery to the coral skeleton of inshore P. cylindrica. This study indicates that large physiological differences exist even among closely related symbionts, with significant implications for thermal susceptibility among reef-building Porites., (© 2021 The Authors. Global Change Biology published by John Wiley & Sons Ltd.)

Harmful algal blooms (HABs) affect both freshwater and marine systems. Laboratory experiments suggest an exudate produced by the bacterium Shewanella sp. IRI-160 could be used to prevent or mitigate dinoflagellate blooms; however, effects on non-target organisms are unknown. The algicide (IRI-160AA) was tested on various ontogenetic stages of the copepod Acartia tonsa (nauplii and adult copepodites), the blue crab Callinectes sapidus (zoea larvae and megalopa postlarvae), and the eastern oyster Crassostrea virginica (pediveliger larvae and adults). Mortality experiments with A. tonsa revealed that the 24-h LC50 was 13.4% v/v algicide for adult females and 5.96% for early-stage nauplii. For C. sapidus, the 24-h LC50 for first-stage zoeae was 16.8%; results were not significant for megalopae or oysters. Respiration rates for copepod nauplii increased in the 11% concentration, and in the 11% and 17% concentrations for crab zoeae; rates of later stages and oysters were unaffected. Activity level was affected for crab zoeae in the 1%, 11%, and 17% treatments, and for oyster pediveliger larvae at the 17% level. Activity of later stages and of adult copepods was unaffected. Smaller, non-target biota with higher surface to volume could be negatively impacted from IRI-160AA dosing, but overall the taxa and stages assayed were tolerant to the algicide at concentrations required for dinoflagellate mortality (EC50 =  ~ 1%).

Characterizing the thermal niche of harmful algae is crucial for understanding and projecting the effects of future climate change on harmful algal blooms. The effects of 6 different temperatures (18-32 °C) on the growth, photophysiology, and toxicity were examined in the dinoflagellate Karlodinium veneficum, and the raphidophytes, Heterosigma akashiwo and Chattonella subsalsa from the Delaware Inland Bays (DIB). K. veneficum and H. akashiwo had skewed unimodal growth patterns, with temperature optima (Topt) at 28.6 and 27.3 °C respectively and an upper thermal niche limit of 32 °C. In contrast, C. subsalsa growth increased linearly with temperature, suggesting Topt and upper thermal boundaries >32 °C. K. veneficum photosystem II (PSII) photochemical efficiency remained stable across all temperatures, while H. akashiwo PSII efficiency declined at higher temperature and C. subsalsa was susceptible to low temperature (~18 °C) photoinactivation. Cell toxicity thermal response was species-specific such that K. veneficum toxicity increased with temperature above Topt. Raphidophyte toxicity peaked at 25-28 °C and was in close agreement with Topt for growth in H. akashiwo but below C. subsalsa maximal growth. The mode of toxicity was markedly different between the dinoflagellate and the raphidophytes such that K. veneficum had greater hemolytic activity while the raphidophytes had pronounced fish gill cell toxicity. These results and patterns of natural abundance for these algae in the DIB suggest that continued ocean warming may contribute to C. subsalsa bloom formation while possibly promoting highly toxic blooms of K. veneficum., Competing Interests: Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2020 The Authors. Published by Elsevier B.V. All rights reserved.)

Background: The capacity of reef-building corals to tolerate (or adapt to) heat stress is a key factor determining their resilience to future climate change. Changes in coral microbiome composition (particularly for microalgal endosymbionts and bacteria) is a potential mechanism that may assist corals to thrive in warm waters. The northern Red Sea experiences extreme temperatures anomalies, yet corals in this area rarely bleach suggesting possible refugia to climate change. However, the coral microbiome composition, and how it relates to the capacity to thrive in warm waters in this region, is entirely unknown., Results: We investigated microbiomes for six coral species (Porites nodifera, Favia favus, Pocillopora damicornis, Seriatopora hystrix, Xenia umbellata, and Sarcophyton trocheliophorum) from five sites in the northern Red Sea spanning 4° of latitude and summer mean temperature ranges from 26.6 °C to 29.3 °C. A total of 19 distinct dinoflagellate endosymbionts were identified as belonging to three genera in the family Symbiodiniaceae (Symbiodinium, Cladocopium, and Durusdinium). Of these, 86% belonged to the genus Cladocopium, with notably five novel types (19%). The endosymbiont community showed a high degree of host-specificity despite the latitudinal gradient. In contrast, the diversity and composition of bacterial communities of the surface mucus layer (SML)-a compartment particularly sensitive to environmental change-varied significantly between sites, however for any given coral was species-specific., Conclusion: The conserved endosymbiotic community suggests high physiological plasticity to support holobiont productivity across the different latitudinal regimes. Further, the presence of five novel algal endosymbionts suggests selection of certain genotypes (or genetic adaptation) within the semi-isolated Red Sea. In contrast, the dynamic composition of bacteria associated with the SML across sites may contribute to holobiont function and broaden the ecological niche. In doing so, SML bacterial communities may aid holobiont local acclimatization (or adaptation) by readily responding to changes in the host environment. Our study provides novel insight about the selective and endemic nature of coral microbiomes along the northern Red Sea refugia.

High sea surface temperatures often lead to coral bleaching wherein reef-building corals lose significant numbers of their endosymbiotic dinoflagellates (Symbiodiniaceae). These increasingly frequent bleaching events often result in large scale coral mortality, thereby devasting reef systems throughout the world. The reef habitats surrounding Palau are ideal for investigating coral responses to climate perturbation, where many inshore bays are subject to higher water temperature as compared with offshore barrier reefs. We examined fourteen physiological traits in response to high temperature across various symbiotic dinoflagellates in four common Pacific coral species, Acropora muricata, Coelastrea aspera, Cyphastrea chalcidicum and Pachyseris rugosa found in both offshore and inshore habitats. Inshore corals were dominated by a single homogenous population of the stress tolerant symbiont Durusdinium trenchii, yet symbiont thermal response and physiology differed significantly across coral species. In contrast, offshore corals harbored specific species of Cladocopium spp. (ITS2 rDNA type-C) yet all experienced similar patterns of photoinactivation and symbiont loss when heated. Additionally, cell volume and light absorption properties increased in heated Cladocopium spp., leading to a greater loss in photo-regulation. While inshore coral temperature response was consistently muted relative to their offshore counterparts, high physiological variability in D. trenchii across inshore corals suggests that bleaching resilience among even the most stress tolerant symbionts is still heavily influenced by their host environment.

Rising seawater temperature and ocean acidification threaten the survival of coral reefs. The relationship between coral physiology and its microbiome may reveal why some corals are more resilient to these global change conditions. Here, we conducted the first experiment to simultaneously investigate changes in the coral microbiome and coral physiology in response to the dual stress of elevated seawater temperature and ocean acidification expected by the end of this century. Two species of corals, Acropora millepora containing the thermally sensitive endosymbiont C21a and Turbinaria reniformis containing the thermally tolerant endosymbiont Symbiodinium trenchi, were exposed to control (26.5°C and pCO2 of 364 μatm) and treatment (29.0°C and pCO2 of 750 μatm) conditions for 24 days, after which we measured the microbial community composition. These microbial findings were interpreted within the context of previously published physiological measurements from the exact same corals in this study (calcification, organic carbon flux, ratio of photosynthesis to respiration, photosystem II maximal efficiency, total lipids, soluble animal protein, soluble animal carbohydrates, soluble algal protein, soluble algal carbohydrate, biomass, endosymbiotic algal density, and chlorophyll a). Overall, dually stressed A. millepora had reduced microbial diversity, experienced large changes in microbial community composition, and experienced dramatic physiological declines in calcification, photosystem II maximal efficiency, and algal carbohydrates. In contrast, the dually stressed coral T. reniformis experienced a stable and more diverse microbiome community with minimal physiological decline, coupled with very high total energy reserves and particulate organic carbon release rates. Thus, the microbiome changed and microbial diversity decreased in the physiologically sensitive coral with the thermally sensitive endosymbiotic algae but not in the physiologically tolerant coral with the thermally tolerant endosymbiont. Our results confirm recent findings that temperature-stress tolerant corals have a more stable microbiome, and demonstrate for the first time that this is also the case under the dual stresses of ocean warming and acidification. We propose that coral with a stable microbiome are also more physiologically resilient and thus more likely to persist in the future, and shape the coral species diversity of future reef ecosystems.

Coral reefs have entered an era of 'ecological crisis' as climate change drives catastrophic reef loss worldwide. Coral growth and stress susceptibility are regulated by their endosymbiotic dinoflagellates (genus Symbiodinium). The phylogenetic diversity of Symbiodinium frequently corresponds to patterns of coral health and survival, but knowledge of functional diversity is ultimately necessary to reconcile broader ecological success over space and time. We explore here functional traits underpinning the complex biology of Symbiodinium that spans free-living algae to coral endosymbionts. In doing so we propose a mechanistic framework integrating the primary traits of resource acquisition and utilisation as a means to explain Symbiodinium functional diversity and to resolve the role of Symbiodinium in driving the stability of coral reefs under an uncertain future., (Copyright © 2017 Elsevier Ltd. All rights reserved.)

Bacteria may play a role in regulating harmful algal blooms, but little is known about the biochemical and physiological changes associated with cell death induced by algicidal bacteria. Previous work characterized an algicidal exudate (IRI-160AA) produced by Shewanella sp. IRI-160 that is effective against dinoflagellates, while having little to no effect on other phytoplankton species in laboratory culture experiments. The objective of this study was to evaluate biochemical changes associated with cell death and impacts on the cell cycle in three dinoflagellate species (Prorocentrum minimum, Karlodinium veneficum and Gyrodinium instriatum) after exposure to IRI-160AA. In this study, IRI-160AA induced cell cycle arrest in all dinoflagellates examined. Several indicators for programmed cell death (PCD) that are often observed in phytoplankton in response to a variety of stressors were also evaluated. Cell death was accompanied by significant increases in DNA degradation, intra- and extracellular ROS concentrations and DEVDase (caspase-3 like) protease activity, which have been associated with PCD in other phytoplankton species. Overall, results of this investigation provide strong evidence that treatment with the bacterial algicide, IRI-160AA results in cell cycle arrest and induces biochemical changes consistent with stress-related cell death responses observed in other phytoplankton.

Preconditioning to non-stressful warming can protect some symbiotic cnidarians against the high temperature-induced collapse of their mutualistic endosymbiosis with photosynthetic dinoflagellates ( Symbiodinium spp.), a process known as bleaching. Here, we sought to determine whether such preconditioning is underpinned by differential regulation of aerobic respiration. We quantified in vivo metabolism and mitochondrial respiratory enzyme activity in the naturally symbiotic sea anemone Exaiptasia pallida preconditioned to 30°C for >7 weeks as well as anemones kept at 26°C. Preconditioning resulted in increased Symbiodinium photosynthetic activity and holobiont (host+symbiont) respiration rates. Biomass-normalised activities of host respiratory enzymes [citrate synthase and the mitochondrial electron transport chain (mETC) complexes I and IV] were higher in preconditioned animals, suggesting that increased holobiont respiration may have been due to host mitochondrial biogenesis and/or enlargement. Subsequent acute heating of preconditioned and 'thermally naive' animals to 33°C induced dramatic increases in host mETC complex I and Symbiodinium mETC complex II activities only in thermally naive E. pallida These changes were not reflected in the activities of other respiratory enzymes. Furthermore, bleaching in preconditioned E. pallida (defined as the significant loss of symbionts) was delayed by several days relative to the thermally naive group. These findings suggest that changes to mitochondrial biogenesis and/or function in symbiotic cnidarians during warm preconditioning might play a protective role during periods of exposure to stressful heating., (© 2017. Published by The Company of Biologists Ltd.)

The algicide, IRI-160AA, induces mortality in dinoflagellates but not other species of algae, suggesting that a shared characteristic or feature renders this class of phytoplankton vulnerable to the algicide. In contrast to other eukaryotic species, the genome of dinoflagellates is stabilized by high concentrations of divalent cations and transition metals and contains large amounts of DNA with unusual base modifications. These distinctions set dinoflagellates apart from other phytoplankton and suggest that the nucleus may be a dinoflagellate-specific target for IRI-160AA. In this study, morphological and ultrastructural changes in three dinoflagellate species, Prorocentrum minimum, Karlodinium veneficum and Gyrodinium instriatum, were evaluated after short-term exposure to IRI-160AA using super resolution structured illumination microscopy (SR-SIM) and transmission electron microscopy (TEM). Exposure to the algicide resulted in cytoplasmic membrane blebbing, differing chloroplast morphologies, nuclear expansion, and chromosome expulsion and/or destabilization. TEM analysis showed that chromosomes of algicide-treated K. veneficum appeared electron dense with fibrous protrusions. In algicide-treated P. minimum and G. instriatum, chromosome decompaction occurred, while for P. minimum, nuclear expulsion was also observed for several cells. Results of this investigation demonstrate that exposure to the algicide destabilizes dinoflagellate chromosomes, although it was not clear if the nucleus was the primary target of the algicide or if the observed effects on chromosomal structure were due to downstream impacts. In all cases, changes in cellular morphology and ultrastructure were observed within two hours, suggesting that the algicide may be an effective and rapid approach to mitigate dinoflagellate blooms., (Copyright © 2017 Elsevier B.V. All rights reserved.)

Symbioses between cnidarians and symbiotic dinoflagellates (Symbiodinium) are ecologically important and physiologically diverse. This diversity contributes to the spatial distribution of specific cnidarian-Symbiodinium associations. Physiological variability also exists within Symbiodinium species, yet we know little regarding its relevance for the establishment of symbiosis under different environmental conditions. Two putatively conspecific Symbiodinium strains (both ITS2-type A4) were isolated from the sea anemone Exaiptasia pallida and placed into unialgal culture. Thermal tolerance of these cultures was compared following heating from 26°C to 33.5°C over 18 days. Photosystem II function was negatively impacted by heating in one strain while PSII function in the other showed little response to elevated temperature. Additionally, infection of Symbiodinium cells into aposymbiotic anemones was assessed for both strains at 26°C and 30.5°C. The heat-sensitive strain had greater infection success at 26°C, while there was no difference in infection between the two strains at the higher temperature. Results from this work suggest that variability in thermal optima or -tolerance within Symbiodinium spp. has relevance for early stages of host-Symbiodinium interactions. Thus, varying infectiousness among differentially heat-sensitive Symbiodinium strains could provide a mechanism for the emergence of novel and potentially resilient cnidarian-Symbiodinium associations in a rapidly warming environment., (© 2016 Society for Applied Microbiology and John Wiley & Sons Ltd.)

Cnidarian-dinoflagellate symbioses are ecologically important and the subject of much investigation. However, our understanding of critical aspects of symbiosis physiology, such as the partitioning of total respiration between the host and symbiont, remains incomplete. Specifically, we know little about how the relationship between host and symbiont respiration varies between different holobionts (host-symbiont combinations). We applied molecular and biochemical techniques to investigate aerobic respiratory capacity in naturally symbiotic Exaiptasia pallida sea anemones, alongside animals infected with either homologous ITS2-type A4 Symbiodinium or a heterologous isolate of Symbiodinium minutum (ITS2-type B1). In naturally symbiotic anemones, host, symbiont, and total holobiont mitochondrial citrate synthase (CS) enzyme activity, but not host mitochondrial copy number, were reliable predictors of holobiont respiration. There was a positive association between symbiont density and host CS specific activity (mg protein(-1)), and a negative correlation between host- and symbiont CS specific activities. Notably, partitioning of total CS activity between host and symbiont in this natural E. pallida population was significantly different to the host/symbiont biomass ratio. In re-infected anemones, we found significant between-holobiont differences in the CS specific activity of the algal symbionts. Furthermore, the relationship between the partitioning of total CS activity and the host/symbiont biomass ratio differed between holobionts. These data have broad implications for our understanding of cnidarian-algal symbiosis. Specifically, the long-held assumption of equivalency between symbiont/host biomass and respiration ratios can result in significant overestimation of symbiont respiration and potentially erroneous conclusions regarding the percentage of carbon translocated to the host. The interspecific variability in symbiont aerobic capacity provides further evidence for distinct physiological differences that should be accounted for when studying diverse host-symbiont combinations.

Reliably predicting how coral calcification may respond to ocean acidification and warming depends on our understanding of coral calcification mechanisms. However, the concentration and speciation of dissolved inorganic carbon (DIC) inside corals remain unclear, as only pH has been measured while a necessary second parameter to constrain carbonate chemistry has been missing. Here we report the first carbonate ion concentration ([CO3(2-)]) measurements together with pH inside corals during the light period. We observe sharp increases in [CO3(2-)] and pH from the gastric cavity to the calcifying fluid, confirming the existence of a proton (H(+)) pumping mechanism. We also show that corals can achieve a high aragonite saturation state (Ωarag) in the calcifying fluid by elevating pH while at the same time keeping [DIC] low. Such a mechanism may require less H(+)-pumping and energy for upregulating pH compared with the high [DIC] scenario and thus may allow corals to be more resistant to climate change related stressors.

Coral reefs are under assault from stressors including global warming, ocean acidification, and urbanization. Knowing how these factors impact the future fate of reefs requires delineating stress responses across ecological, organismal and cellular scales. Recent advances in coral reef biology have integrated molecular processes with ecological fitness and have identified putative suites of temperature acclimation genes in a Scleractinian coral Acropora hyacinthus. We wondered what unique characteristics of these genes determined their coordinate expression in response to temperature acclimation, and whether or not other corals and cnidarians would likewise possess these features. Here, we focus on cytosine methylation as an epigenetic DNA modification that is responsive to environmental stressors. We identify common conserved patterns of cytosine-guanosine dinucleotide (CpG) motif frequencies in upstream promoter domains of different functional gene groups in two cnidarian genomes: a coral (Acropora digitifera) and an anemone (Nematostella vectensis). Our analyses show that CpG motif frequencies are prominent in the promoter domains of functional genes associated with environmental adaptation, particularly those identified in A. hyacinthus. Densities of CpG sites in upstream promoter domains near the transcriptional start site (TSS) are 1.38x higher than genomic background levels upstream of -2000 bp from the TSS. The increase in CpG usage suggests selection to allow for DNA methylation events to occur more frequently within 1 kb of the TSS. In addition, observed shifts in CpG densities among functional groups of genes suggests a potential role for epigenetic DNA methylation within promoter domains to impact functional gene expression responses in A. digitifera and N. vectensis. Identifying promoter epigenetic sequence motifs among genes within specific functional groups establishes an approach to describe integrated cellular responses to environmental stress in reef corals and potential roles of epigenetics on survival and fitness in the face of global climate change.

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.

Mass bleaching events are predicted to occur annually later this century. Nevertheless, it remains unknown whether corals will be able to recover between annual bleaching events. Using a combined tank and field experiment, we simulated annual bleaching by exposing three Caribbean coral species (Porites divaricata, Porites astreoides and Orbicella faveolata) to elevated temperatures for 2.5 weeks in 2 consecutive years. The impact of annual bleaching stress on chlorophyll a, energy reserves, calcification, and tissue C and N isotopes was assessed immediately after the second bleaching and after both short- and long-term recovery on the reef (1.5 and 11 months, respectively). While P. divaricata and O. faveolata were able to recover from repeat bleaching within 1 year, P. astreoides experienced cumulative damage that prevented full recovery within this time frame, suggesting that repeat bleaching had diminished its recovery capacity. Specifically, P. astreoides was not able to recover protein and carbohydrate concentrations. As energy reserves promote bleaching resistance, failure to recover from annual bleaching within 1 year will likely result in the future demise of heat-sensitive coral species., (© 2015 The Author(s).)

Dinoflagellates of the genus Symbiodinium express broad diversity in both genetic identity (phylogeny) and photosynthetic function to presumably optimize ecological success across extreme light environments; however, whether differences in the primary photobiological characteristics that govern photosynthetic optimization are ultimately a function of phylogeny is entirely unresolved. We applied a novel fast repetition rate fluorometry approach to screen genetically distinct Symbiodinium types (n = 18) spanning five clades (A-D, F) for potential phylogenetic trends in factors modulating light absorption (effective cross-section, reaction center content) and utilization (photochemical vs dynamic nonphotochemical quenching; [1 - C] vs [1 - Q]) by photosystem II (PSII). The variability of PSII light absorption was independent of phylogenetic designation, but closely correlated with cell size across types, whereas PSII light utilization intriguingly followed one of three characteristic patterns: (1) similar reliance on [1 - C] and [1 - Q] or (2) preferential reliance on [1 - C] (mostly A, B types) vs (3) preferential reliance on [1 - Q] (mostly C, D, F types), and thus generally consistent with cladal designation. Our functional trait-based approach shows, for the first time, how Symbiodinium photosynthetic function is governed by the interplay between phylogenetically dependent and independent traits, and is potentially a means to reconcile complex biogeographic patterns of Symbiodinium phylogenetic diversity in nature., (© 2015 The Authors. New Phytologist © 2015 New Phytologist Trust.)

The association between cnidarians and photosynthetic dinoflagellates within the genus Symbiodinium is a prevalent relationship in tropical and subtropical marine environments. Although the diversity of Symbiodinium provides a possible axis for niche diversification, increased functional range and resilience to physical stressors such as elevated temperature, how such diversity relates to the physiological balance between autotrophy and heterotrophy of the host animal remains unknown. Here, we experimentally show interspecific and intraspecific variability of photosynthetic carbon fixation and subsequent translocation by Symbiodinium to the model cnidarian host Aiptasia pallida. By using a clonal anemone line harboring different species of Symbiodinium, we determined that symbiont identity influences trophic plasticity through its density, capacity to fix carbon, quantity of translocated carbon and ultimately the host's capacity to ingest and digest prey. Symbiont carbon translocation and host prey ingestion were positively correlated across symbiont combinations that consisted of different isoclonal lines of Symbiodinium minutum, while a combination with type D4-5 Symbiodinium displayed lower carbon translocation, and prey capture and digestion more similar to Aiptasia lacking symbionts. The absence of a shift toward greater heterotrophy when carbon translocation is low suggests that the metabolic demand of feeding and digestion may overwhelm nutritional stores when photosynthesis is reduced, and amends the possible role of animal feeding in resistance to or recovery from the effects of climate change in more obligate symbioses such as reef-building corals., (© 2015. Published by The Company of Biologists Ltd.)

Diel vertical migration (DVM) is thought to provide an adaptive advantage to some phytoplankton, and may help determine the ecological niche of certain harmful algae. Here we separately compared DVM patterns between two species of harmful algae isolated from the Delaware Inland Bays, Karlodinium veneficum and Chattonella subsalsa, in laboratory columns. We interpreted the DVM patterns of each species with Photosystem II (PSII) photochemistry, rates of carbon assimilation, and specific growth rates. Each species migrated differently, wherein K. veneficum migrated closer to the surface each day with high population synchrony, while C. subsalsa migrated near to the surface from the first day of measurements with low population synchrony. Both species appeared to downregulate PSII in high light at the surface, but by different mechanisms. C. subsalsa grew slower than K. veneficum in low light intensities (≈bottom of columns), and exhibited maximal rates of C-assimilation (Pmax) at surface light intensities, suggesting this species may prefer high light, potentially explaining this species' rapid surface migration. Contrastingly, K. veneficum showed declines in carbon assimilation at surface light intensities, and exhibited a smaller reduction in growth at low (bottom) light intensities (compared to C. subsalsa), suggesting that this species' step-wise migration was photoacclimative and determined daily migration depth. DVM was found to be under circadian control in C. subsalsa, but not in K. veneficum. However, there was little evidence for circadian regulation of PSII photochemistry in either species. Migration conformed to each species' physiology, and the results contribute to our understanding each alga's realized environmental niche., (Copyright © 2014 Elsevier B.V. All rights reserved.)

Mass coral bleaching events caused by elevated seawater temperatures result in extensive coral loss throughout the tropics, and are projected to increase in frequency and severity. If bleaching becomes an annual event later in this century, more than 90% of coral reefs worldwide may be at risk of long-term degradation. While corals can recover from single isolated bleaching and can acclimate to recurring bleaching events that are separated by multiple years, it is currently unknown if and how they will survive and possibly acclimatize to annual coral bleaching. Here, we demonstrate for the first time that annual coral bleaching can dramatically alter thermal tolerance in Caribbean corals. We found that high coral energy reserves and changes in the dominant algal endosymbiont type (Symbiodinium spp.) facilitated rapid acclimation in Porites divaricata, whereas low energy reserves and a lack of algal phenotypic plasticity significantly increased susceptibility in Porites astreoides to bleaching the following year. Phenotypic plasticity in the dominant endosymbiont type of Orbicella faveolata did not prevent repeat bleaching, but may have facilitated rapid recovery. Thus, coral holobiont response to an isolated single bleaching event is not an accurate predictor of its response to bleaching the following year. Rather, the cumulative impact of annual coral bleaching can turn some coral species 'winners' into 'losers', and can also facilitate acclimation and turn some coral species 'losers' into 'winners'. Overall, these findings indicate that cumulative impact of annual coral bleaching could result in some species becoming increasingly susceptible to bleaching and face a long-term decline, while phenotypically plastic coral species will acclimatize and persist. Thus, annual coral bleaching and recovery could contribute to the selective loss of coral diversity as well as the overall decline of coral reefs in the Caribbean., (© 2014 John Wiley & Sons Ltd.)

Coral skeletal boron isotopes have been established as a proxy for seawater pH, yet it remains unclear if and how this proxy is affected by seawater temperature. Specifically, it has never been directly tested whether coral bleaching caused by high water temperatures influences coral boron isotopes. Here we report the results from a controlled bleaching experiment conducted on the Caribbean corals Porites divaricata, Porites astreoides, and Orbicella faveolata. Stable boron (δ11B), carbon (δ13C), oxygen (δ18O) isotopes, Sr/Ca, Mg/Ca, U/Ca, and Ba/Ca ratios, as well as chlorophyll a concentrations and calcification rates were measured on coral skeletal material corresponding to the period during and immediately after the elevated temperature treatment and again after 6 weeks of recovery on the reef. We show that under these conditions, coral bleaching did not affect the boron isotopic signature in any coral species tested, despite significant changes in coral physiology. This contradicts published findings from coral cores, where significant decreases in boron isotopes were interpreted as corresponding to times of known mass bleaching events. In contrast, δ13C and δ18O exhibited major enrichment corresponding to decreases in calcification rates associated with bleaching. Sr/Ca of bleached corals did not consistently record the 1.2°C difference in seawater temperature during the bleaching treatment, or alternatively show a consistent increase due to impaired photosynthesis and calcification. Mg/Ca, U/Ca, and Ba/Ca were affected by coral bleaching in some of the coral species, but the observed patterns could not be satisfactorily explained by temperature dependence or changes in coral physiology. This demonstrates that coral boron isotopes do not record short-term bleaching events, and therefore cannot be used as a proxy for past bleaching events. The robustness of coral boron isotopes to changes in coral physiology, however, suggests that reconstruction of seawater pH using boron isotopes should be uncompromised by short-term bleaching events.

Rising atmospheric CO2 concentrations threaten coral reefs globally by causing ocean acidification (OA) and warming. Yet, the combined effects of elevated pCO2 and temperature on coral physiology and resilience remain poorly understood. While coral calcification and energy reserves are important health indicators, no studies to date have measured energy reserve pools (i.e., lipid, protein, and carbohydrate) together with calcification under OA conditions under different temperature scenarios. Four coral species, Acropora millepora, Montipora monasteriata, Pocillopora damicornis, Turbinaria reniformis, were reared under a total of six conditions for 3.5 weeks, representing three pCO2 levels (382, 607, 741 µatm), and two temperature regimes (26.5, 29.0 °C) within each pCO2 level. After one month under experimental conditions, only A. millepora decreased calcification (-53%) in response to seawater pCO2 expected by the end of this century, whereas the other three species maintained calcification rates even when both pCO2 and temperature were elevated. Coral energy reserves showed mixed responses to elevated pCO2 and temperature, and were either unaffected or displayed nonlinear responses with both the lowest and highest concentrations often observed at the mid-pCO2 level of 607 µatm. Biweekly feeding may have helped corals maintain calcification rates and energy reserves under these conditions. Temperature often modulated the response of many aspects of coral physiology to OA, and both mitigated and worsened pCO2 effects. This demonstrates for the first time that coral energy reserves are generally not metabolized to sustain calcification under OA, which has important implications for coral health and bleaching resilience in a high-CO2 world. Overall, these findings suggest that some corals could be more resistant to simultaneously warming and acidifying oceans than previously expected.

Growing concerns over ocean acidification have highlighted the need to critically understand inorganic carbon acquisition and utilization in marine microalgae. Here, we contrast these characteristics for the first time between two genetically distinct dinoflagellate species of the genus Symbiodinium (phylotypes A13 and A20) that live in symbiosis with reef-forming corals. Both phylotypes were grown in continuous cultures under identical environmental conditions. Rubisco was measured using quantitative Western blots, and radioisotopic (14) C uptake was used to characterize light- and total carbon dioxide (TCO2 )-dependent carbon fixation, as well as inorganic carbon species preference and external carbonic anhydrase activity. A13 and A20 exhibited similar rates of carbon fixation despite cellular concentrations of Rubisco being approximately four-fold greater in A13. The uptake of CO2 over HCO3 - was found to support the majority of carbon fixation in both phylotypes. However, A20 was also able to indirectly utilize HCO3 - by first converting it to CO2 via external carbonic anhydrase. These results show that adaptive differences in inorganic carbon acquisition have evolved within the Symbiodinium genus, which thus carries fundamental implications as to how this functionally key genus will respond to ocean acidification, but could also represent a key trait factor that influences their productivity when in hospite of their coral hosts., (© 2013 The Authors. New Phytologist © 2013 New Phytologist Trust.)

Microalgae possess numerous cellular mechanisms specifically employed for acclimating the photosynthetic pathways to changes in the physical environment. Despite the importance of coral-dinoflagellate symbioses, little focus has been given as to how the symbiotic algae (Symbiodinium spp.) regulate the expression of their photosynthetic genes. This study used real-time PCR to investigate the transcript abundance of the plastid-encoded genes, psbA (encoding the D1 protein of photosystem II) and psaA (encoding the P700 protein in photosystem I), within the cultured Symbiodinium ITS-2 (internal transcribed spacer region) types A20 and A13. Transcript abundance was monitored during a low to high-light shift, as well as over a full diel light cycle. In addition, psaA was characterized in three isolates (A20, A13, and D4-5) and noted as another example of a dinoflagellate plastid gene encoded on a minicircle. In general, the overall incongruence of transcript patterns for both psbA and psaA between the Symbiodinium isolates and other models of transcriptionally controlled chloroplast gene expression (e.g., Pisum sativum [pea], Sinapis alba [mustard seedling], and Synechocystis sp. PCC 6803 [cyanobacteria]) suggests that Symbiodinium is reliant on posttranscriptional mechanisms for homeostatic regulation of its photosynthetic proteins., (© 2013 Phycological Society of America.)

Periodic and seasonal exposure to high light is a common occurrence for many near-shore and estuarine phytoplankton. Rapid acclimatization to shifts in light may provide an axis by which some species of phytoplankton can outcompete other microalgae. Patterns of photoacclimation and photosynthetic capacity in the raphidophyte Heterosigma akashiwo (Hada) Hada ex Hara et Chihara isolated from the mid-Atlantic of the United States were followed in continuous cultures at low- and high-light intensities, followed by reciprocal shifts to the opposite light level. The maximum quantum yield (Fv /Fm ) as well as the photosynthetic cross-section (σPSII ) of photosystem II was higher in high-light cultures compared to low-light cultures. Significant diurnal variability in photochemistry and photoprotection was noted at both light levels, and high-light-acclimated cultures displayed greater variability in photoprotective pathways. When shifted from low to high light, there was only a slight and temporary decline in maximum quantum yield, while cell specific growth more than doubled within 24 h. Rapid acclimation to high light was facilitated by short-term photoprotection (nonphotochemical quenching), reduced PSII reaction center connectivity, and electron transport. Short-term increases in de-epoxidated xanthophyll pigments contributed to nonphotochemical protection, but lagged behind initial increases in nonphotochemical quenching and were not the primary pathway of photoprotection in this alga. By 48 h, photochemistry of cultures shifted from low to high light resembled long-term high-light-acclimated cultures. This isolate of H. akashiwo appears well poised to exploit rapid shifts in light by using unique cellular adjustments in light harvesting and photochemistry., (© 2013 Phycological Society of America.)

Increased seawater pCO 2 , and in turn 'ocean acidification' (OA), is predicted to profoundly impact marine ecosystem diversity and function this century. Much research has already focussed on calcifying reef-forming corals (Class: Anthozoa) that appear particularly susceptible to OA via reduced net calcification. However, here we show that OA-like conditions can simultaneously enhance the ecological success of non-calcifying anthozoans, which not only play key ecological and biogeochemical roles in present day benthic ecosystems but also represent a model organism should calcifying anthozoans exist as less calcified (soft-bodied) forms in future oceans. Increased growth (abundance and size) of the sea anemone (Anemonia viridis) population was observed along a natural CO 2 gradient at Vulcano, Italy. Both gross photosynthesis (P G ) and respiration (R) increased with pCO 2 indicating that the increased growth was, at least in part, fuelled by bottom up (CO 2 stimulation) of metabolism. The increase of P G outweighed that of R and the genetic identity of the symbiotic microalgae (Symbiodinium spp.) remained unchanged (type A19) suggesting proximity to the vent site relieved CO 2 limitation of the anemones' symbiotic microalgal population. Our observations of enhanced productivity with pCO 2 , which are consistent with previous reports for some calcifying corals, convey an increase in fitness that may enable non-calcifying anthozoans to thrive in future environments, i.e. higher seawater pCO 2 . Understanding how CO 2 -enhanced productivity of non- (and less-) calcifying anthozoans applies more widely to tropical ecosystems is a priority where such organisms can dominate benthic ecosystems, in particular following localized anthropogenic stress., (© 2012 Blackwell Publishing Ltd.)

Mutualistic symbioses between scleractinian corals and endosymbiotic dinoflagellates (Symbiodinium spp.) are the foundation of coral reef ecosystems. For many coral-algal symbioses, prolonged episodes of thermal stress damage the symbiont's photosynthetic capability, resulting in its expulsion from the host. Despite the link between photosynthetic competency and symbiont expulsion, little is known about the effect of thermal stress on the expression of photosystem genes in Symbiodinium. This study used real-time PCR to monitor the transcript abundance of two important photosynthetic reaction center genes, psbA (encoding the D1 protein of photosystem II) and psaA (encoding the P(700) protein of photosystem I), in four cultured isolates (representing ITS2-types A13, A20, B1, and F2) and two in hospite Symbiodinium spp. within the coral Pocillopora spp. (ITS2-types C1b-c and D1). Both cultured and in hospite Symbiodinium samples were exposed to elevated temperatures (32°C) over a 7-day period and examined for changes in photochemistry and transcript abundance. Symbiodinium A13 and C1b-c (both thermally sensitive) demonstrated significant declines in both psbA and psaA during the thermal stress treatment, whereas the transcript levels of the other Symbiodinium types remained stable. The downregulation of both core photosystem genes could be the result of several different physiological mechanisms, but may ultimately limit repair rates of photosynthetic proteins, rendering some Symbiodinium spp. especially susceptible to thermal stress.

Dimethyl sulfide (DMS) and dimethylsulfoniopropionate (DMSP) are sulfur compounds that may function as antioxidants in algae. Symbiotic dinoflagellates of the genus Symbiodinium show strain-specific differences in their susceptibility to temperature-induced oxidative stress and have been shown to contain high concentrations of DMSP. We investigated continuous cultures of four strains from distinct phylotypes (A1, A13, A2, and B1) that can be characterized by differential thermal tolerances. We hypothesized that strains with high thermal tolerance have higher concentrations of DMSP and DMS in comparison to strains with low thermal tolerance. DMSP concentrations were strain-specific with highest concentrations occurring in A1 (225 ± 3.5 mmol · L(-1 ) cell volume [CV]) and lowest in A2 (158 ± 3.8 mmol · L(-1 ) CV). Both strains have high thermal tolerance. Strains with low thermal tolerance (A13 and B1) showed DMSP concentrations in between these extremes (194 ± 19.0 and 160 ± 6.1 mmol · L(-1 ) CV, respectively). DMS data further confirmed this general pattern with high DMS concentrations in A1 and A13 (4.1 ± 1.22 and 2.1 ± 0.37 mmol · L(-1 ) CV, respectively) and low DMS concentrations in A2 and B1 (0.3 ± 0.06 and 0.5 ± 0.22 mmol · L(-1) CV, respectively). Hence, the strain-specific differences in DMSP and DMS concentrations did not match the different abilities of the four phylotypes to withstand thermal stress. Future work should quantify the possible dynamics in DMSP and DMS concentrations during periods of high oxidative stress in Symbiodinium sp. and address the role of these antioxidants in zooxanthellate cnidarians., (© 2011 Phycological Society of America.)

Increased sea-surface temperatures linked to warming climate threaten coral reef ecosystems globally. To better understand how corals and their endosymbiotic dinoflagellates (Symbiodinium spp.) respond to environmental change, tissue biomass and Symbiodinium density of seven coral species were measured on various reefs approximately every four months for up to thirteen years in the Upper Florida Keys, United States (1994-2007), eleven years in the Exuma Cays, Bahamas (1995-2006), and four years in Puerto Morelos, Mexico (2003-2007). For six out of seven coral species, tissue biomass correlated with Symbiodinium density. Within a particular coral species, tissue biomasses and Symbiodinium densities varied regionally according to the following trends: Mexico≥Florida Keys≥Bahamas. Average tissue biomasses and symbiont cell densities were generally higher in shallow habitats (1-4 m) compared to deeper-dwelling conspecifics (12-15 m). Most colonies that were sampled displayed seasonal fluctuations in biomass and endosymbiont density related to annual temperature variations. During the bleaching episodes of 1998 and 2005, five out of seven species that were exposed to unusually high temperatures exhibited significant decreases in symbiotic algae that, in certain cases, preceded further decreases in tissue biomass. Following bleaching, Montastraea spp. colonies with low relative biomass levels died, whereas colonies with higher biomass levels survived. Bleaching- or disease-associated mortality was also observed in Acropora cervicornis colonies; compared to A. palmata, all A. cervicornis colonies experienced low biomass values. Such patterns suggest that Montastraea spp. and possibly other coral species with relatively low biomass experience increased susceptibility to death following bleaching or other stressors than do conspecifics with higher tissue biomass levels., (© 2011 Thornhill et al.)

Mutualisms between reef-building corals and endosymbiotic dinoflagellates are particularly sensitive to environmental stress, yet the ecosystems they construct have endured major oscillations in global climate. During the winter of 2008, an extreme cold-water event occurred in the Gulf of California that bleached corals in the genus Pocillopora harbouring a thermally 'sensitive' symbiont, designated Symbiodinium C1b-c, while colonies possessing Symbiodinium D1 were mostly unaffected. Certain bleached colonies recovered quickly while others suffered partial or complete mortality. In most colonies, no appreciable change was observed in the identity of the original symbiont, indicating that these partnerships are stable. During the initial phases of recovery, a third species of symbiont B1(Aiptasia), genetically identical to that harboured by the invasive anemone, Aiptasia sp., grew opportunistically and was visible as light-yellow patches on the branch tips of several colonies. However, this symbiont did not persist and was displaced in all cases by C1b-c several months later. Colonies with D1 were abundant at inshore habitats along the continental eastern Pacific, where seasonal turbidity is high relative to offshore islands. Environmental conditions of the central and southern coasts of Mexico were not sufficient to explain the exclusivity of D1 Pocillopora in these regions. It is possible that mass mortalities associated with major thermal disturbances during the 1997-1998 El Niño Southern Oscillation eliminated C1b-c holobionts from these locations. The differential loss of Pocillopora holobionts in response to thermal stress suggests that natural selection on existing variation can cause rapid and significant shifts in the frequency of particular coral-algal partnerships. However, coral populations may take decades to recover following episodes of severe selection, thereby raising considerable uncertainty about the long-term viability of these communities.

Dinoflagellates in the genus Symbiodinium are among the most abundant and important group of eukaryotic microbes found in coral reef ecosystems. Recent analyses conducted on various host cnidarians indicated that Symbiodinium assemblages in the Caribbean Sea are genetically and ecologically diverse. In order to further characterize this diversity and identify processes important to its origins, samples from six orders of Cnidaria comprising 45 genera were collected from reef habitats around Barbados (eastern Caribbean) and from the Mesoamerican barrier reef off the coast of Belize (western Caribbean). Fingerprinting of the ribosomal internal transcribed spacer 2 identified 62 genetically different Symbiodinium. Additional analyses of clade B Symbiodinium using microsatellite flanker sequences unequivocally characterized divergent lineages, or "species," within what was previously thought to be a single entity (B1 or B184). In contrast to the Indo-Pacific where host-generalist symbionts dominate many coral communities, partner specificity in the Caribbean is relatively high and is influenced little by the host's apparent mode of symbiont acquisition. Habitat depth (ambient light) and geographic isolation appeared to influence the bathymetric zonation and regional distribution for most of the Symbiodinium spp. characterized. Approximately 80% of Symbiodinium types were endemic to either the eastern or western Caribbean and 40-50% were distributed to compatible hosts living in shallow, high-irradiance, or deep, low-irradiance environments. These ecologic, geographic, and phylogenetic patterns indicate that most of the present Symbiodinium diversity probably originated from adaptive radiations driven by ecological specialization in separate Caribbean regions during the Pliocene and Pleistocene periods.

Occurrences whereby cnidaria lose their symbiotic dinoflagellate microalgae (Symbiodinium spp.) are increasing in frequency and intensity. These so-called bleaching events are most often related to an increase in water temperature, which is thought to limit certain Symbiodinium phylotypes from effectively dissipating absorbed excitation energy that is otherwise used for photochemistry. Here, we examined photosynthetic characteristics and hydrogen peroxide (H2 O2 ) production, a possible signal involved in bleaching, from two Symbiodinium types (a thermally "tolerant" A1 and "sensitive" B1) representative of cnidaria-Symbiodinium symbioses of reef-building Caribbean corals. Under steady-state growth at 26°C, a higher efficiency of PSII photochemistry, rate of electron turnover, and rate of O2 production were observed for type A1 than for B1. The two types responded very differently to a period of elevated temperature (32°C): type A1 increased light-driven O2 consumption but not the amount of H2 O2 produced; in contrast, type B1 increased the amount of H2 O2 produced without an increase in light-driven O2 consumption. Therefore, our results are consistent with previous suggestions that the thermal tolerance of Symbiodinium is related to adaptive constraints associated with photosynthesis and that sensitive phylotypes are more prone to H2 O2 production. Understanding these adaptive differences in the genus Symbiodinium will be crucial if we are to interpret the response of symbiotic associations, including reef-building corals, to environmental change., (© 2008 Phycological Society of America.)