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Coral bleaching—the stress-induced collapse of the coral– Symbiodinium symbiosis—is a significant driver of worldwide coral reef degradation. Yet, not all corals are equally susceptible to bleaching, and we lack a clear understanding of the mechanisms underpinning their differential susceptibilities. Here, we focus on cellular redox regulation as a potential determinant of bleaching susceptibility in the reef coral Stylophora pistillata . Using slow heating (1 °C d −1 ) and altered irradiance, we induced bleaching in S. pistillata colonies sampled from two depths [5–8 m (shallow) and 15–18 m (deep)]. There was significant depth-dependent variability in the timing and extent of bleaching (loss of symbiont cells), as well as in host enzymatic antioxidant activity [specifically, superoxide dismutase and catalase (CAT)]. However, among the coral fragments that bleached, most did so without displaying any evidence of a host enzymatic antioxidant response. For example, both deep and shallow corals suffered significant symbiont loss at elevated temperature, but only deep colonies exposed to high temperature and high light displayed any up-regulation of host antioxidant enzyme activity (CAT). Surprisingly, this preceded the equivalent antioxidant responses of the symbiont, which raises questions about the source(s) of hydrogen peroxide in the symbiosis. Overall, changes in enzymatic antioxidant activity in the symbionts were driven primarily by irradiance rather than temperature, and responses were similar across depth groups. Taken together, our results suggest that in the absence of light stress, heating of 1 °C d −1 to 4 °C above ambient is not sufficient to induce a substantial oxidative challenge in S. pistillata . We provide some of the first evidence that regulation of coral enzymatic antioxidants can vary significantly depending on habitat, and, in terms of determining bleaching susceptibility, our results suggest a significant role for the host’s differential regulation of cellular redox status.

The relationship between cnidarians and their micro-algal symbionts is crucial for normal animal function and the formation of coral reefs. We used the sea anemone Exaiptasia pallida (Aiptasia) as a model cnidarian–dinoflagellate system to determine the effects of white, blue and red light on photo-movement. In white light, phototropism and phototaxis of Aiptasia were dependent on the presence of symbionts; anemones with symbionts bent and moved toward the light, whereas aposymbiotic anemones (lacking algal symbionts) moved, but without strong directionality. Phototaxis and phototropism also occurred in blue light, but to a lesser extent than in white light, with no apparent response to red light. Phototactic behavior was also sensitive to the specific anemone–symbiont pairing. The ability to sense and move in response to light would presumably allow for selection of favorable habitats. Overall, this study demonstrates that the algal symbiont is required for photo-movement of the host and that the extent of movement is influenced by the different anemone–symbiont associations.

The endosymbiosis between cnidarians and photosynthetic dinoflagellates of the Symbiodiniaceae family forms the foundation of coral reef ecosystems. Prolonged environmental shifts can disrupt the cnidarian–Symbiodiniaceae partnership, triggering dysbiosis and coral bleaching and ultimately resulting in coral starvation, mortality, and the collapse of reef ecosystems. Despite its significance, critical gaps remain in our understanding of the cellular mechanisms governing symbiosis and dysbiosis. Innate immune genes and pathways are highly conserved across the Metazoa, including in cnidarians. Among these is NADPH oxidase (NOX), a key enzyme responsible for generating reactive oxygen species (ROS), primarily for microbial degradation within phagolysosomes. In this study, we hypothesize that NOX plays a role in the regulation of cnidarian–Symbiodiniaceae symbiosis and the host phagosomal maturation process. We investigated NOX function in relation to symbiotic state and heat stress in the sea anemone Exaiptasia diaphana (commonly called aiptasia), a model for cnidarian–Symbiodiniaceae symbiosis and dysbiosis. Our findings show that NOX gene and protein expression is suppressed in the symbiotic state, supporting the hypothesis that symbionts modulate host innate immunity. However, upon heat treatment, we observed increased NOX expression and activity along with NOX localization around algal symbionts, suggesting that host phagosomal maturation processes are engaged during bleaching. We propose a model where the phagocytic NOX complex becomes activated during symbiosis breakdown and bleaching. Our findings support the hypothesis that in situ degradation, facilitated by ROS generated by NOX, plays a key role in the process of dysbiosis. This work contributes to our understanding of cnidarian innate immunity, highlighting critical steps in dysbiosis and phagosomal maturation processes within cnidarian–Symbiodiniaceae symbiosis.

Coral reefs are in decline. The basic functional unit of coral reefs is the coral metaorganism or holobiont consisting of the cnidarian host animal, symbiotic algae of the genus Symbiodinium, and a specific consortium of bacteria (among others), but research is slow due to the difficulty of working with corals. Aiptasia has proven a tractable model system to elucidate the intricacies of cnidarian-dinoflagellate symbioses, but characterization of the associated bacterial microbiome and the underlying genomic features relevant for bacterial selection and control is required to provide a complete and integrated understanding of holobiont function. In this work, we characterize and analyze the microbiome of aposymbiotic and symbiotic Aiptasia and show that bacterial associates are distinct in both conditions. We further show that key microbial associates can be cultured without their cnidarian host. Our results suggest that bacteria play an important role in the symbiosis of Aiptasia with Symbiodinium, a finding that underlines the power of the Aiptasia model system where cnidarian hosts can be analyzed in aposymbiotic and symbiotic states. The characterization of the native microbiome and the ability to retrieve culturable isolates contributes to the resources available for the Aiptasia model system. This provides an opportunity to comparatively analyze cnidarian metaorganisms as collective functional holobionts and as separated member species. We hope that this will accelerate research into understanding the intricacies of coral biology, which is urgently needed to develop strategies to mitigate the effects of environmental change.

Coral bleaching poses a threat to coral reefs worldwide. As a consequence of the temperature-induced breakdown in coral–dinoflagellate symbiosis, bleaching can have extensive effects on reef communities. However, our understanding of bleaching at a cellular level is limited, and this is particularly true regarding differential susceptibility among coral species. Recent work suggests that bleaching may represent a host innate immune-like response to symbiont dysfunction that involves synthesis of the signalling compound nitric oxide (NO) and the induction of host apoptotic-like cell death. In this study, we examined the activity of apoptosis-regulating enzymes alongside oxidised NO accumulation (a proxy for NO synthesis) in the reef corals Acropora millepora , Montipora digitata , and Pocillopora damicornis during experimental thermal stress. P. damicornis was the most sensitive species, suffering mortality (tissue sloughing) after 5 days at 33 °C but non-lethal bleaching after 9 days at 31.5 °C. A. millepora bleached at 33 °C but remained structurally intact, while M. digitata showed little evidence of bleaching. P. damicornis and A. millepora both exhibited evidence of temperature-induced NO synthesis and, after 5 days of heating, levels of oxidised NO in both species were fivefold higher than in controls maintained at 28.5 °C. These responses preceded bleaching by a number of days and may have occurred before symbiont dysfunction (measured as chlorophyll a degradation and oxidised NO accumulation). In A. millepora , apparent NO synthesis correlated with the induction of host apoptotic-like pathways, while in P. damicornis, the upregulation of apoptotic pathways occurred later. No evidence of elevated NO production or apoptosis was observed in M. digitata at 33 °C and baseline activity of apoptosis-regulating enzymes was negligible in this species. These findings provide important physiological data in the context of the responses of corals to global change and suggest that early events in the host may be important in the collapse of the coral–dinoflagellate symbiosis.

Coral cell cultures made from reef-building scleractinian corals have the potential to aid in the pursuit of understanding of the cnidarian–dinoflagellate symbiosis. Various methods have previously been described for the production of cell cultures in vitro with a range of success and longevity. In this study, viable tissue spheroids containing host tissue and symbionts (coral explants) were grown from the tissues of Fungia granulosa . The cultured explants remained viable for over 2 months and showed morphological similarities in tissue structure and internal microenvironment to reef-building scleractinian corals. The photophysiology of the explants (1 week old) closely matched that of the parent coral F. granulosa . This study provides the first empirical basis for supporting the use of coral explants as laboratory models for studying coral symbioses. In particular, it highlights how these small, self-sustaining, skeleton-free models can be useful for a number of molecular, genetic and physiological analyses necessary for investigating host–symbiont interactions at the microscale.

Intracellular pH (pH i ) is likely to play a key role in maintaining the functional success of cnidarian–dinoflagellate symbiosis, yet until now the pH i of the symbiotic dinoflagellates (genus Symbiodinium ) has never been quantified. Flow cytometry was used in conjunction with the ratiometric fluorescent dye BCECF to monitor changes in pH i over a daily light/dark cycle. The pH i of Symbiodinium type B1 freshly isolated from the model sea anemone Aiptasia pulchella was 7.25 ± 0.01 (mean ± SE) in the light and 7.10 ± 0.02 in the dark. A comparable effect of irradiance was seen across a variety of cultured Symbiodinium genotypes (types A1, B1, E1, E2, F1, and F5) which varied between pH i 7.21–7.39 in the light and 7.06–7.14 in the dark. Of note, there was a significant genotypic difference in pH i , irrespective of irradiance.