In-situ Effects of Eutrophication and Overfishing on Physiology and Bacterial Diversity of the Red Sea Coral Acropora hemprichii

Coral reefs of the Central Red Sea display a high degree of endemism, and are increasingly threatened by anthropogenic effects due to intense local coastal development measures. Overfishing and eutrophication are among the most significant local pressures on these reefs, but there is no information available about their potential effects on the associated microbial community. Therefore, we compared holobiont physiology and 16S-based bacterial communities of tissue and mucus of the hard coral Acropora hemprichii after 1 and 16 weeks of in-situ inorganic nutrient enrichment (via fertilizer diffusion) and/or herbivore exclusion (via caging) in an offshore reef of the Central Red Sea. Simulated eutrophication and/or overfishing treatments did not affect coral physiology with respect to coral respiration rates, chlorophyll a content, zooxanthellae abundance, or δ ¹⁵N isotopic signatures. The bacterial community of A. hemprichii was rich and uneven, and diversity increased over time in all treatments. While distinct bacterial species were identified as a consequence of eutrophication, overfishing, or both, two bacterial species that could be classified to the genus Endozoicomonas were consistently abundant and constituted two thirds of bacteria in the coral. Several nitrogen-fixing and denitrifying bacteria were found in the coral specimens that were exposed to experimentally increased nutrients. However, no particular bacterial species was consistently associated with the coral under a given treatment and the single effects of manipulated eutrophication and overfishing could not predict the combined effect. Our data underlines the importance of conducting field studies in a holobiont framework, taking both, physiological and molecular measures into account.     

Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome

The importance of Symbiodinium algal endosymbionts and a diverse suite of bacteria for coral holobiont health and functioning are widely acknowledged. Yet, we know surprisingly little about microbial community dynamics and the stability of host‐microbe associations under adverse environmental conditions. To gain insight into the stability of coral host‐microbe associations and holobiont structure, we assessed changes in the community structure of Symbiodinium and bacteria associated with the coral Pocillopora verrucosa under excess organic nutrient conditions. Pocillopora‐associated microbial communities were monitored over 14 days in two independent experiments. We assessed the effect of excess dissolved organic nitrogen (DON) and excess dissolved organic carbon (DOC). Exposure to excess nutrients rapidly affected coral health, resulting in two distinct stress phenotypes: coral bleaching under excess DOC and severe tissue sloughing (>90% tissue loss resulting in host mortality) under excess DON. These phenotypes were accompanied by structural changes in the Symbiodinium community. In contrast, the associated bacterial community remained remarkably stable and was dominated by two Endozoicomonas phylotypes, comprising on average 90% of 16S rRNA gene sequences. This dominance of Endozoicomonas even under conditions of coral bleaching and mortality suggests the bacterial community of P. verrucosa may be rather inflexible and thereby unable to respond or acclimatize to rapid changes in the environment, contrary to what was previously observed in other corals. In this light, our results suggest that coral holobionts might occupy structural landscapes ranging from a highly flexible to a rather inflexible composition with consequences for their ability to respond to environmental change.     

Microbiome structure of the fungid coral Ctenactis echinata aligns with environmental differences

The significance of bacteria for eukaryotic functioning is increasingly recognized. Coral reef ecosystems critically rely on the relationship between coral hosts and their intracellular photosynthetic dinoflagellates, but the role of the associated bacteria remains largely theoretical. Here, we set out to relate coral‐associated bacterial communities of the fungid host species Ctenactis echinata to environmental settings (geographic location, substrate cover, summer/winter, nutrient and suspended matter concentrations) and coral host abundance. We show that bacterial diversity of C. echinata aligns with ecological differences between sites and that coral colonies sampled at the species’ preferred habitats are primarily structured by one bacterial taxon (genus Endozoicomonas) representing more than 60% of all bacteria. In contrast, host microbiomes from lower populated coral habitats are less structured and more diverse. Our study demonstrates that the content and structure of the coral microbiome aligns with environmental differences and denotes habitat adequacy. Availability of a range of coral host habitats might be important for the conservation of distinct microbiome structures and diversity.     

Spatial and Species Variations in Bacterial Communities Associated with Corals from the Red Sea as Revealed by Pyrosequencing

Microbial associations with corals are common and are most likely symbiotic, although their diversity and relationships with environmental factors and host species remain unclear. In this study, we adopted a 16S rRNA gene tag-pyrosequencing technique to investigate the bacterial communities associated with three stony Scleractinea and two soft Octocorallia corals from three locations in the Red Sea. Our results revealed highly diverse bacterial communities in the Red Sea corals, with more than 600 ribotypes detected and up to 1,000 species estimated from a single coral species. Altogether, 21 bacterial phyla were recovered from the corals, of which Gammaproteobacteria was the most dominant group, and Chloroflexi, Chlamydiae, and the candidate phylum WS3 were reported in corals for the first time. The associated bacterial communities varied greatly with location, where environmental conditions differed significantly. Corals from disturbed areas appeared to share more similar bacterial communities, but larger variations in community structures were observed between different coral species from pristine waters. Ordination methods identified salinity and depth as the most influential parameters affecting the abundance of Vibrio, Pseudoalteromonas, Serratia, Stenotrophomonas, Pseudomonas, and Achromobacter in the corals. On the other hand, bacteria such as Chloracidobacterium and Endozoicomonas were more sensitive to the coral species, suggesting that the host species type may be influential in the associated bacterial community, as well. The combined influences of the coral host and environmental factors on the associated microbial communities are discussed. This study represents the first comparative study using tag-pyrosequencing technology to investigate the bacterial communities in Red Sea corals.     

Inhibition of Calvin–Benson cycle suppresses the repair of photosystem II in Symbiodinium: implications for coral bleaching

Inhibition of Calvin–Benson cycle (CBC) activity by thermal stress has been hypothesized to cause photoinhibition of photosystem II (PSII) in zooxanthellae of reef-building corals and consequently lead to bleaching. This study tests whether the interruption of CBC by glycolaldehyde (GA) leads to photoinhibition and subsequent coral bleaching in Stylophora pistillata. When S. pistillata was incubated with GA, the O₂ evolution rate declined in a dose-dependent manner and the extent of photoinhibition, reflected by a decreased maximum quantum yield of PSII (F _v/F _m), was enhanced. The effect of GA on photoinhibition was similar to that of chloramphenicol (CAP), an inhibitor of protein synthesis in chloroplasts. When S. pistillata was incubated in weak light following a high-light-induced photoinhibitory treatment, the recovery of PSII from photoinhibition was suppressed in a similar manner to both GA- and CAP-treated samples. After incubation in moderate light at 26°C, S. pistillata showed a bleaching response only in presence of GA. These results suggest that coral bleaching-like responses are caused by interruption of the CBC activity in S. pistillata and are associated with accelerated photoinhibition through suppression of the protein synthesis-dependent repair of PSII but not to an increase in photodamage to PSII.     

16SrDNA Pyrosequencing of the Mediterranean Gorgonian Paramuricea clavata Reveals a Link among Alterations in Bacterial Holobiont Members,Anthropogenic Influence and Disease Outbreaks

Mass mortality events of benthic invertebrates in the Mediterranean Sea are becoming an increasing concern with catastrophic effects on the coastal marine environment. Sea surface temperature anomalies leading to physiological stress, starvation and microbial infections were identified as major factors triggering animal mortality. However the highest occurrence of mortality episodes in particular geographic areas and occasionally in low temperature deep environments suggest that other factors play a role as well. We conducted a comparative analysis of bacterial communities associated with the purple gorgonian Paramuricea clavata, one of the most affected species, collected at different geographic locations and depth, showing contrasting levels of anthropogenic disturbance and health status. Using massive parallel 16SrDNA gene pyrosequencing we showed that the bacterial community associated with healthy P. clavata in pristine locations was dominated by a single genus Endozoicomonas within the order Oceanospirillales which represented ∼90% of the overall bacterial community. P. clavata samples collected in human impacted areas and during disease events had higher bacterial diversity and abundance of disease-related bacteria, such as vibrios, than samples collected in pristine locations whilst showed a reduced dominance of Endozoicomonas spp. In contrast, bacterial symbionts exhibited remarkable stability in P. clavata collected both at euphotic and mesophotic depths in pristine locations suggesting that fluctuations in environmental parameters such as temperature have limited effect in structuring the bacterial holobiont. Interestingly the coral pathogen Vibrio coralliilyticus was not found on diseased corals collected during a deep mortality episode suggesting that neither temperature anomalies nor recognized microbial pathogens are solely sufficient to explain for the events. Overall our data suggest that anthropogenic influence may play a significant role in determining the coral health status by affecting the composition of the associated microbial community. Environmental stressful events and microbial infections may thus be superimposed to compromise immunity and trigger mortality outbreaks.     

Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: The host does matter in determining the tolerance of corals to bleaching

The role of both host and dinoflagellate symbionts was investigated in the response of reef-building corals to thermal stress in the light. Replicate coral nubbins of Stylophora pistillata and Porites cylindrica from the GBR were exposed to either 28 °C (control) or 32 °C for 5 days before being returned to an ambient reef temperature (28 °C). S. pistillata was found to contain either Symbiodinium genotype C1 or C8a, while P. cylindrica had type C15 based on ITS genotyping. Analysis of the quantum yield of photosystem (PS) II fluorescence of the symbionts in P. cylindrica showed that light-induced excitation pressure on the C15 Symbiodinium was significantly less, and the steady state quantum yield of PSII fluorescence at noon (ΔF/Fm′) greater, than that measured in C1/C8a Symbiodinium sp. from S. pistillata. Immunoblots of the PS II D1 protein were significantly lower in Symbiodinium from S. pistillata compared to those in P. cylindrica after exposure to thermal stress. The biochemical markers, heat-stress protein (HSP) 70 and superoxide dismutase (SOD), were significantly greater in P. cylindrica before the experiment, and both species of coral increased their biosynthesis of HSP 70 and SOD when exposed to thermal stress. Concentrations of MAAs, glycerol, and lipids were not significantly affected by thermal stress in these experiments, but DNA damage was greater in heat-stressed S. pistillata compared to P. cylindrica. There was minimal coral mucus, which accounts for up to half of the total energy budget of a coral and provides the first layer of defense for invading microbes, produced by S. pistillata after heat stress compared to P. cylindrica. It is concluded that P. cylindrica contains a heat resistant C15 Symbiodinium and critical host proteins are present at higher concentrations than observed for S. pistillata, the combination of which provides greater protection from bleaching conditions of high temperature in the light.     

Influence of Species Specificity and Other Factors on Bacteria Associated with the Coral Stylophora pistillata in Taiwan

Species of bacteria associated with Stylophora pistillata were determined by analyses of 16S ribosomal genes. Coral samples were taken from two distinct sites at Kenting, in the far south of Taiwan; three coral colonies at each site were tagged and sampled in the winter and summer of 2007. Six hundred 16S rRNA gene clones were selected and sequenced for diversity analysis and community comparison. LIBSHUFF and nonparametric multiple dimensional scaling analyses showed variations in the composition of the coral-associated bacteria in the different samples, suggesting that seasonal and geographic factors and variations in individual coral colonies were all vital drivers of the structure of the S. pistillata-associated bacterial community. To examine the association between species specificity and environmental impacts on the structure of the coral-associated bacterial community, we conducted an integrated, comparative analysis of 44 coral-associated bacterial data sets, including the present study''s data. The clustering analysis suggests that the influence of spatial and temporal factors on the coral-associated bacteria population structure is considerable; nonetheless, the effect of species specificity is still detectable in some coral species, especially those from the Caribbean Sea.Microbes are abundant in the ocean and thrive around corals. In earlier investigations over the past decades, microbes have been detected in coral mucus (8), in coral tissues (5), and in the surrounding reef waters (25). Although we understand little about the real interactions between these coral-associated microbes and the coral itself, or their mutual roles, much indirect evidence suggests that these microbes may play an important role in the coral holobiont, with respect to coral nutrition, health, and disease (14, 18, 30).It is now known that most microbes are uncultivable by present laboratory methods (1, 28, 10). To understand more about coral-associated microbial communities, to identify the diversity of microbes associated with particular corals, and to assess whether these microbes are indeed species specific or represent only opportunistic interactions with the coral animal, some relatively comprehensive studies have been carried out in recent years based on culture-independent molecular techniques, e.g., construction of 16S rRNA gene clone libraries or denaturing gradient gel electrophoresis (3, 6, 9, 11, 13, 16, 17, 19, 20, 21, 23, 30, 31, 33). Consequently, coral-associated microbes are now known to be not only highly diverse and dynamic but also substantially coral specific.Recently, the specificity of association between coral and bacterial species has been a topic of much discussion. Earlier reports suggested that similar microbial communities were specifically associated with identical coral species, regardless of whether they were isolated from distinct geographic regions or at different times (3, 9, 20, 21); however, environmental factors have also recently been found to significantly influence the specificity of bacteria-coral associations (2, 17). Such inconsistency might reasonably be expected in light of the complexity of interaction in the coral holobiont, which includes coral, algae, fungi, bacteria, archaea, and other biotic and environmental factors (30). Nonetheless, more-detailed studies are needed for a better comprehension of species-specific bacterial associations.In this study, we selected Stylophora pistillata, a widely distributed coral in western Pacific reefs (26), to study the diversity and composition of the coral-associated bacteria and the effects of spatial and temporal differences on such population structures. We also examined the species specificity of such coral-bacteria associations by comparing our data with another 44 coral-associated bacterial data sets. This biodiversity analysis shows the presence of a large variation in the composition of S. pistillata-associated bacterial communities, suggesting that specificity between S. pistillata and associated bacteria is significantly influenced by geographic and seasonal factors. Furthermore, a comparison with 10 previous studies of coral-associated microbes showed that spatial and temporal factors play a role in affecting the population structure of coral-associated bacteria, though distinct species-specific bacterial profiles are detectable in some corals of the Caribbean Sea.     

Assessment of bacterial community composition within and among Acropora loripes colonies in the wild and in captivity

A growing number of studies have provided insights into the diversity of coral-associated bacteria and their function in the coral holobiont. Yet, information about spatial heterogeneity of bacteria within coral colonies is limited. Using 16S rRNA gene metabarcoding, we analyzed the bacterial community composition across four distinct locations in each of five wild Acropora loripes colonies. Considerable variation within and among colonies was present, which has implications for sampling strategies and data interpretation in coral microbiome research. Bacterial assemblages significantly differed in alpha and beta diversity among colonies, with all corals possessing a high relative abundance of Endozoicomonas. When the same A. loripes colonies were subsequently reared in aquaria over 4 weeks, the relative abundance of Marinobacter initially increased in all colonies. However, no significant alteration in bacterial community composition was observed over time and the colonies maintained distinct bacterial microbiomes.

     

Carbonic anhydrase inhibitors. Inhibition studies with anions and sulfonamides of a new cytosolic enzyme from the scleractinian coral Stylophora pistillata

The catalytic activity and the inhibition of a new coral carbonic anhydrase (CA, EC 4.2.1.1), from the scleractinian coral Stylophora pistillata, STPCA-2, has been investigated. STPCA-2 has high catalytic activity for the physiological reaction being less sensitive to anion and sulfonamide inhibitors compared to STPCA, a coral enzyme previously described. The best STPCA-2 anion inhibitors were sulfamide, sulfamic acid, phenylboronic acid, and phenylarsonic acid (K_Is of 5.7-67.2 μM) whereas the best sulfonamide inhibitors were acetazolamide and dichlorophenamide (K_Is of 74-79 nM). Because this discriminatory effect between these two coral CAs, sulfonamides may be useful to better understand the physiological role of STPCA and STPCA-2 in corals and biomineralization processes.     

Soluble organic matrix of two Scleractinian corals: partial and comparative analysis

This study is a biochemical and molecular analysis of the soluble organic matrix (SOM) of two Scleractinian corals differing in their morphological characteristics: Stylophora pistillata, a branched robust coral and Pavona cactus, a leafy complex coral. Soluble organic matrix of both coral species were shown to contain high amounts of potentially acidic amino acids and glycine. However, proportions of glycosaminoglycans and SDS-PAGE analyses of soluble organic matrix proteins were very different. Three proteins of S. pistillata and at least five proteins of P. cactus were detected by silver staining, some of them being able to bind calcium. Internal peptide sequences of two matrix proteins (one from each species) were obtained. One sequence of S. pistillata is unusual because it contains a long poly-aspartate domain, as described in proteins belonging to the calsequestrin family and in proteins from molluscan species. This domain suggests an essential role for this protein in the control of mineralization.     

Differential susceptibility to oxidative stress of two scleractinian corals: antioxidant functioning of mycosporine-glycine

This study examined the importance of mycosporine-glycine (Myc-Gly) as a functional antioxidant in the thermal-stress susceptibility of two scleractinian corals, Platygyra ryukyuensis and Stylophora pistillata. Photochemical efficiency of PSII (F_v/F_m), activity of antioxidant enzymes, superoxide dismutase (SOD) and catalase (CAT), and composition and abundance of mycosporine-like amino acids (MAAs) in the coral tissue and in symbiotic zooxanthellae were analyzed during 12-h exposure to high temperature (33 °C). After 6- and 12-h exposures at 33 °C, S. pistillata showed a significantly more pronounced decline in F_v/F_m compared to P. ryukyuensis. A 6-h exposure at 33 °C induced a significant increase in the activities of SOD and CAT in both host and zooxanthellae components of S. pistillata while in P. ryukyuensis a significant increase was observed only in the CAT activity of zooxanthellae. After 12-h exposure, the SOD activity of P. ryukyuensis was unaffected in the coral tissue but slightly increased in zooxanthellae, whereas the CAT activity in the coral tissue showed a 2.5-fold increase. The total activity of antioxidant enzymes was significantly higher in S. pistillata than in P. ryukyuensis, suggesting that P. ryukyuensis is less sensitive to oxidative stress than S. pistillata. This differential susceptibility of the corals is consistent with a 20-fold higher initial concentration of Myc-Gly in P. ryukyuensis compared to S. pistillata. In the coral tissue and zooxanthellae of both species investigated, the first 6 h of exposure to thermal stress induced a pronounced reduction in the abundance of Myc-Gly but not in other MAAs. When exposure was prolonged to 12 h, the Myc-Gly pool continued to decrease in P. ryukyuensis and was completely depleted in S. pistillata. The delay in the onset of oxidative stress in P. ryukyuensis and the dramatic increase in the activities of the antioxidant enzymes in S. pistillata, which contains low concentrations of Myc-Gly suggest that Myc-Gly provides rapid protection against oxidative stress before the antioxidant enzymes are induced. These findings strongly suggest that Myc-Gly is functioning as a biological antioxidant in the coral tissue and zooxanthellae and demonstrate its importance in the survival of reef-building corals under thermal stress.     

Engineering of coral reef larval supply through transplantation of nursery-farmed gravid colonies

The continuous worldwide degradation of coral reefs raises an urgent need for novel active restoration techniques as traditional conservation practices have failed to impede the incessant reefs' decline. While applying the “gardening coral reefs” methodology in Eilat (Red Sea, Israel), we examined reproductive outputs of naturally-grown and outplanted, nursery-farmed Stylophora pistillata colonies from three coral-transplantation trials (November 2005, May 2007, and September 2008), along three reproductive seasons. Surprisingly, transplanted colonies showed better reproductive capacities than the natal Stylophora colonies during > 4 post-transplantation years. A higher percentage of nursery-farmed colonies released planula larvae as compared to naturally-grown colonies. Gravid transplants also shed more planulae per colony, yielding significantly augmented numbers of total planulae over naturally developed S. pistillata colonies. Our results indicate that nursery-grown corals may be used to enhance reef resilience by contributing to the larval pool, forming an engineered larval dispersal instrument for reef rehabilitation.     

Oriented translocation of energy in grafted reef corals

Colonies of the Red Sea reef coral Stylophora pistillata were grafted with alien branches (alografts), which had been labelled by NaH¹⁴CO₃ in the light. The “cold” host-colonies translocated the ¹⁴C-containing photosynthetic metabolites in an oriented pathway from the grafted branches into their own tissues. The highest accumulations of ¹⁴C products were detected in specific branch-tips of the host, away from the contact zones. The “recipient” colonies utilize these energy-rich materials for their metabolic requirements. The ¹⁴CO₂ produced through respiration is consequently detected in the skeletal-carbonate of the tips as Ca¹⁴CO₃. The purple morph of S. pistillata is found to be superior to the yellow morph.     

Carbonic anhydrase inhibitors: Inhibition studies of a coral secretory isoform with inorganic anions

The inhibition of a coral carbonic anhydrase (CA, EC 4.2.1.1) has been investigated with a series of inorganic anions such as halogenides, pseudohalogenides, bicarbonate, carbonate, nitrate, nitrite, hydrogen sulfide, bisulfite, perchlorate, sulfate. The full-length scleractinian coral Stylophora pistillata CA, STPCA, has a significant catalytic activity for the physiological reaction of CO₂ hydration to bicarbonate, similarly to the ubiquitous human isoforms hCA I (cytosolic) and hCA VI (secreted). The best STPCA anion inhibitors were bromide, iodide, carbonate, and sulfamate, with inhibition constants of 9.0–10.0 μM.     

Dimethylsulfoniopropionate,superoxide dismutase and glutathione as stress response indicators in three corals under short-term hyposalinity stress

Corals are among the most active producers of dimethylsulfoniopropionate (DMSP), a key molecule in marine sulfur cycling, yet the specific physiological role of DMSP in corals remains elusive. Here, we examine the oxidative stress response of three coral species (Acropora millepora, Stylophora pistillata and Pocillopora damicornis) and explore the antioxidant role of DMSP and its breakdown products under short-term hyposalinity stress. Symbiont photosynthetic activity declined with hyposalinity exposure in all three reef-building corals. This corresponded with the upregulation of superoxide dismutase and glutathione in the animal host of all three species. For the symbiont component, there were differences in antioxidant regulation, demonstrating differential responses to oxidative stress between the Symbiodinium subclades. Of the three coral species investigated, only A. millepora provided any evidence of the role of DMSP in the oxidative stress response. Our study reveals variability in antioxidant regulation in corals and highlights the influence life-history traits, and the subcladal differences can have on coral physiology. Our data expand on the emerging understanding of the role of DMSP in coral stress regulation and emphasizes the importance of exploring both the host and symbiont responses for defining the threshold of the coral holobiont to hyposalinity stress.     

Photosynthetic circadian rhythmicity patterns of Symbiodium,the coral endosymbiotic algae

Biological clocks are self-sustained endogenous timers that enable organisms (from cyanobacteria to humans) to anticipate daily environmental rhythms, and adjust their physiology and behaviour accordingly. Symbiotic corals play a central role in the creation of biologically rich ecosystems based on mutualistic symbioses between the invertebrate coral and dinoflagellate protists from the genus Symbiodinium. In this study, we experimentally establish that Symbiodinium photosynthesis, both as a free-living unicellular algae and as part of the symbiotic association with the coral Stylophora pistillata, is ‘wired’ to the circadian clock mechanism with a ‘free-run’ cycle close to 24 h. Associated photosynthetic pigments also showed rhythmicity under light/dark conditions and under constant light conditions, while the expression of the oxygen-evolving enhancer 1 gene (within photosystem II) coincided with photosynthetically evolved oxygen in Symbiodinium cultures. Thus, circadian regulation of the Symbiodinium photosynthesis is, however, complicated as being linked to the coral/host that have probably profound physiochemical influence on the intracellular environment. The temporal patterns of photosynthesis demonstrated here highlight the physiological complexity and interdependence of the algae circadian clock associated in this symbiosis and the plasticity of algae regulatory mechanisms downstream of the circadian clock.     

Nutritional resources as positional information for morphogenesis in the stony coral Stylophora pistillata

We are interested in deciphering the mechanisms for morphogenesis in the Red Sea scleractinian coral Stylophora pistillata with the help of mathematical models. Previous mathematical models for coral morphogenesis assume that skeletal growth is proportional to the amount of locally available energetic resources like diffusible nutrients and photosynthetic products. We introduce a new model which includes factors like dissolved nutrients and photosynthates, but these resources do not serve as building blocks for growth but rather provide some kind of positional information for coral morphogenesis. Depending on this positional information side branches are generated, splittings of branches take place and branch growth direction is determined. The model results are supported by quantitative comparisons with experimental data obtained from young coral colonies.     

Seasonal Mesophotic Coral Bleaching of Stylophora pistillata in the Northern Red Sea

Coral bleaching occurs when environmental stress induces breakdown of the coral-algae symbiosis and the host initiates algae expulsion. Two types of coral bleaching had been thoroughly discussed in the scientific literature; the first is primarily associated with mass coral bleaching events; the second is a seasonal loss of algae and/or pigments. Here, we describe a phenomenon that has been witnessed for repeated summers in the mesophotic zone (40–63 m) in the northern Red Sea: seasonal bleaching and recovery of several hermatypic coral species. In this study, we followed the recurring bleaching process of the common coral Stylophora pistillata. Bleaching occurred from April to September with a 66% decline in chlorophyll a concentration, while recovery began in October. Using aquarium and transplantation experiments, we explored environmental factors such as temperature, photon flux density and heterotrophic food availability. Our experiments and observations did not yield one single factor, alone, responsible for the seasonal bleaching. The dinoflagellate symbionts (of the genus Symbiodinium) in shallow (5 m) Stylophora pistillata were found to have a net photosynthetic rate of 56.98–92.19 µmol O₂ cm⁻² day⁻¹. However, those from mesophotic depth (60 m) during months when they are not bleached are net consumers of oxygen having a net photosynthetic rate between −12.86 - (−10.24) µmol O₂ cm⁻² day⁻¹. But during months when these mesophotic corals are partially-bleached, they yielded higher net production, between −2.83–0.76 µmol O₂ cm⁻² day⁻¹. This study opens research questions as to why mesophotic zooxanthellae are more successfully meeting the corals metabolic requirements when Chl a concentration decreases by over 60% during summer and early fall.     

Multiple Symbiont Acquisition Strategies as an Adaptive Mechanism in the Coral Stylophora pistillata

In obligate symbioses, the host’s survival relies on the successful acquisition and maintenance of symbionts. Symbionts can either be transferred from parent to offspring via direct inheritance (vertical transmission) or acquired anew each generation from the environment (horizontal transmission). With vertical symbiont transmission, progeny benefit by not having to search for their obligate symbionts, and, with symbiont inheritance, a mechanism exists for perpetuating advantageous symbionts. But, if the progeny encounter an environment that differs from that of their parent, they may be disadvantaged if the inherited symbionts prove suboptimal. Conversely, while in horizontal symbiont acquisition host survival hinges on an unpredictable symbiont source, an individual host may acquire genetically diverse symbionts well suited to any given environment. In horizontal acquisition, however, a potentially advantageous symbiont will not be transmitted to subsequent generations. Adaptation in obligate symbioses may require mechanisms for both novel symbiont acquisition and symbiont inheritance. Using denaturing-gradient gel electrophoresis and real-time PCR, we identified the dinoflagellate symbionts (genus Symbiodinium) hosted by the Red Sea coral Stylophora pistillata throughout its ontogenesis and over depth. We present evidence that S. pistillata juvenile colonies may utilize both vertical and horizontal symbiont acquisition strategies. By releasing progeny with maternally derived symbionts, that are also capable of subsequent horizontal symbiont acquisition, coral colonies may acquire physiologically advantageous novel symbionts that are then perpetuated via vertical transmission to subsequent generations. With symbiont inheritance, natural selection can act upon the symbiotic variability, providing a mechanism for coral adaptation.