Mass coral bleaching due to thermal stress represents a major threat to the integrity and functioning of coral reefs. Thermal thresholds vary, however, between corals, partly as a result of the specific type of endosymbiotic dinoflagellate (Symbiodinium sp.) they harbour. The production of reactive oxygen species (ROS) in corals under thermal and light stress has been recognised as one mechanism that can lead to cellular damage and the loss of their symbiont population (Oxidative Theory of Coral Bleaching). Here, we compared the response of symbiont and host enzymatic antioxidants in the coral species Acropora millepora and Montipora digitata at 28°C and 33°C. A. millepora at 33°C showed a decrease in photochemical efficiency of photosystem II (PSII) and increase in maximum midday excitation pressure on PSII, with subsequent bleaching (declining photosynthetic pigment and symbiont density). M. digitata exhibited no bleaching response and photochemical changes in its symbionts were minor. The symbiont antioxidant enzymes superoxide dismutase, ascorbate peroxidase, and catalase peroxidase showed no significant upregulation to elevated temperatures in either coral, while only catalase was significantly elevated in both coral hosts at 33°C. Increased host catalase activity in the susceptible coral after 5 days at 33°C was independent of antioxidant responses in the symbiont and preceded significant declines in PSII photochemical efficiencies. This finding suggests a potential decoupling of host redox mechanisms from symbiont photophysiology and raises questions about the importance of symbiont-derived ROS in initiating coral bleaching.
Coral bleaching (involving the loss of symbiotic algae from the cnidarian host) is a major threat to coral reefs and appears to be mediated at the cellular level by nitric oxide (NO). In this study, we examined the specific role of NO in bleaching using the sea anemone Aiptasia pulchella, a model system for the study of corals. Exposure of A. pulchella to high-temperature shock (26-33°C over <1 h) or an NO donor (S-nitrosoglutathione) resulted in significant increases in host caspase-like enzyme activity. These responses were reflected in the intensities of bleaching, which were significantly higher in heat- or NO-treated specimens than in controls maintained in seawater at 26°C. Notably, the inhibition of caspase-like activity prevented bleaching even in the presence of an NO donor or at elevated temperature. The additional use of an NO scavenger controlled for effects mediated by agents other than NO. We also exposed A. pulchella to a more ecologically relevant treatment (an increase from 26 to 33°C over 6-7 d). Again, host NO synthesis correlated with the activation of caspase-like enzyme activity. Therefore, we conclude that NO's involvement in cnidarian bleaching arises through the regulation of host apoptotic pathways.
Nitric oxide (NO) is a ubiquitous molecule and its involvement in metazoan-microbe symbiosis is well known. Evidence suggests that it plays a role in the temperatureinduced breakdown ('bleaching') of the ecologically important cnidarian-dinoflagellate association, and this can often lead to widespread mortality of affected hosts. This study confirms that dinoflagellates of the genus Symbiodinium can produce NO and that production of the compound is differentially regulated in different types when exposed to elevated temperature. Temperature-sensitive type B1 cells under heat stress (8 C above ambient) exhibited significant increases in NO synthesis, which occurred alongside pronounced photoinhibition and cell mortality. Tolerant type A1 cells also displayed increases in NO production, yet maintained photosynthetic yields at levels similar to those of untreated cells and displayed less dramatic increases in cell death. Type C1 cells displayed a down-regulation of NO synthesis at high temperature, and no significant mortality increases were observed in this type. Temperatureinduced mortality in types A1 and B1 was affected by the prevailing level of NO and, furthermore, photosynthetic yields of these temperature-tolerant and -sensitive types appeared differentially susceptible to NO donated by pharmacological agents. Taken together, these differences in NO synthesis and tolerance could potentially influence the varying bleaching responses seen among hosts harboring different Symbiodinium types.
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 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.
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.
Summary The temperature-induced collapse ("bleaching") of the coral-dinoflagellate symbiosis is hypothesised to result from symbiont oxidative stress and a subsequent host innate immune-like response. This includes the production of nitric oxide (NO), which is involved in numerous microbial symbioses. Much of NO's cytotoxicity has been attributed to its conversion, in the presence of superoxide (O2-), to highly reactive peroxynitrite (ONOO-). However, ONOO- generation has yet to be observed in either a lower invertebrate or intracellular mutualism. Using confocal laser scanning microscopy with the fluorescent ONOO- indicator aminophenyl fluorescein (APF), we observed strong evidence that ONOO- is generated in symbiotic Aiptasia pulchella under conditions known to induce thermal bleaching. However, a role for ONOO- in bleaching remains unclear as treatment with a peroxynitrite scavenger had no significant effect on thermal bleaching. Therefore, while ONOO- may have a potential for cytotoxicity, in vivo levels of the compound may be insufficient to affect bleaching.
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.
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