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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.)

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.

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 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.

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.)

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.)

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.

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.

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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 14C 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 [ABSTRACT FROM AUTHOR]