The coral probiotic hypothesis

Emerging diseases have been responsible for the death of about 30% of corals worldwide during the last 30 years. Coral biologists have predicted that by 2050 most of the world's coral reefs will be destroyed. This prediction is based on the assumption that corals can not adapt rapidly enough to environmental stress-related conditions and emerging diseases. Our recent studies of the Vibrio shiloi/Oculina patagonica model system of the coral bleaching disease indicate that corals can indeed adapt rapidly to changing environmental conditions by altering their population of symbiotic bacteria. These studies have led us to propose the Coral Probiotic Hypothesis. This hypothesis posits that a dynamic relationship exists between symbiotic microorganisms and environmental conditions which brings about the selection of the most advantageous coral holobiont. Changing their microbial partners would allow the corals to adapt to changing environmental conditions more rapidly (days to weeks) than via mutation and selection (many years). An important outcome of the Probiotic Hypothesis would be development of resistance of the coral holobiont to diseases. The following evidence supports this hypothesis: (i) Corals contain a large and diverse bacterial population associated with their mucus and tissues; (ii) the coral-associated bacterial population undergoes a rapid change when environmental conditions are altered; and (iii) although lacking an adaptive immune system (no antibodies), corals can develop resistance to pathogens. The Coral Probiotic Hypothesis may help explain the evolutionary success of corals and moderate the predictions of their demise.     

Phage therapy of the white plague-like disease of Favia favus in the Red Sea

Coral disease is a major factor in the global decline of coral reefs. At present, there are no known procedures for preventing or treating infectious diseases of corals. Immunization is not possible because corals have a restricted adaptive immune system and antibiotics are neither ecologically safe nor practical in an open system. Thus, we tested phage therapy as an alternative therapeutic method for treating diseased corals. Phage BA3, specific to the coral pathogen Thalassomonas loyana, inhibited the progression of the white plague-like disease and transmission to healthy corals in the Gulf of Aqaba, Red Sea. Only one out of 19 (5?%) of the healthy corals became infected when placed near phage-treated diseased corals, whereas 11 out of 18 (61?%) healthy corals were infected in the no-phage control. This is the first successful treatment for a coral disease in the sea. We posit that phage therapy of certain coral diseases is achievable in situ.     

Bacterial profiling of White Plague Disease in a comparative coral species framework

Coral reefs are threatened throughout the world. A major factor contributing to their decline is outbreaks and propagation of coral diseases. Due to the complexity of coral-associated microbe communities, little is understood in terms of disease agents, hosts and vectors. It is known that compromised health in corals is correlated with shifts in bacterial assemblages colonizing coral mucus and tissue. However, general disease patterns remain, to a large extent, ambiguous as comparative studies over species, regions, or diseases are scarce. Here, we compare bacterial assemblages of samples from healthy (HH) colonies and such displaying signs of White Plague Disease (WPD) of two different coral species (Pavona duerdeni and Porites lutea) from the same reef in Koh Tao, Thailand, using 16S rRNA gene microarrays. In line with other studies, we found an increase of bacterial diversity in diseased (DD) corals, and a higher abundance of taxa from the families that include known coral pathogens (Alteromonadaceae, Rhodobacteraceae, Vibrionaceae). In our comparative framework analysis, we found differences in microbial assemblages between coral species and coral health states. Notably, patterns of bacterial community structures from HH and DD corals were maintained over species boundaries. Moreover, microbes that differentiated the two coral species did not overlap with microbes that were indicative of HH and DD corals. This suggests that while corals harbor distinct species-specific microbial assemblages, disease-specific bacterial abundance patterns exist that are maintained over coral species boundaries.     

Larval connectivity across temperature gradients and its potential effect on heat tolerance in coral populations

Coral reefs are increasingly exposed to elevated temperatures that can cause coral bleaching and high levels of mortality of corals and associated organisms. The temperature threshold for coral bleaching depends on the acclimation and adaptation of corals to the local maximum temperature regime. However, because of larval dispersal, coral populations can receive larvae from corals that are adapted to very different temperature regimes. We combine an offline particle tracking routine with output from a high‐resolution physical oceanographic model to investigate whether connectivity of coral larvae between reefs of different thermal regimes could alter the thermal stress threshold of corals. Our results suggest that larval transport between reefs of widely varying temperatures is likely in the Coral Triangle and that accounting for this connectivity may be important in bleaching predictions. This has important implications in conservation planning, because connectivity may allow some reefs to have an inherited heat tolerance that is higher or lower than predicted based on local conditions alone.     

Microbial diseases of corals and global warming

Coral bleaching and other diseases of corals have increased dramatically during the last few decades. As outbreaks of these diseases are highly correlated with increased sea-water temperature, one of the consequences of global warming will probably be mass destruction of coral reefs. The causative agent(s) of a few of these diseases have been reported: bleaching of Oculina patagonica by Vibrio shiloi; black band disease by a microbial consortium; sea-fan disease (aspergillosis) by Aspergillus sydowii; and coral white plague possibly by Sphingomonas sp. In addition, we have recently discovered that Vibrio coralyticus is the aetiological agent for bleaching the coral Pocillopora damicornis in the Red Sea. In the case of coral bleaching by V. shiloi, the major effect of increasing temperature is the expression of virulence genes by the pathogen. At high summer sea-water temperatures, V. shiloi produces an adhesin that allows it to adhere to a beta-galactoside-containing receptor in the coral mucus, penetrate into the coral epidermis, multiply intracellularly, differentiate into a viable-but-not-culturable (VBNC) state and produce toxins that inhibit photosynthesis and lyse the symbiotic zooxanthellae. In black band disease, sulphide is produced at the coral-microbial biofilm interface, which is probably responsible for tissue death. Reports of newly emerging coral diseases and the lack of epidemiological and biochemical information on the known diseases indicate that this will become a fertile area of research in the interface between microbial ecology and infectious disease.     

Interactions between coral restoration and fish assemblages: implications for reef management

Corals create complex reef structures that provide both habitat and food for many fish species. Because of numerous natural and anthropogenic threats, many coral reefs are currently being degraded, endangering the fish assemblages they support. Coral reef restoration, an active ecological management tool, may help reverse some of the current trends in reef degradation through the transplantation of stony corals. Although restoration techniques have been extensively reviewed in relation to coral survival, our understanding of the effects of adding live coral cover and complexity on fishes is in its infancy with a lack of scientifically validated research. This study reviews the limited data on reef restoration and fish assemblages, and complements this with the more extensive understanding of complex interactions between natural reefs and fishes and how this might inform restoration efforts. It also discusses which key fish species or functional groups may promote, facilitate or inhibit restoration efforts and, in turn, how restoration efforts can be optimised to enhance coral fish assemblages. By highlighting critical knowledge gaps in relation to fishes and restoration interactions, the study aims to stimulate research into the role of reef fishes in restoration projects. A greater understanding of the functional roles of reef fishes would also help inform whether restoration projects can return fish assemblages to their natural compositions or whether alternative species compositions develop, and over what timeframe. Although alleviation of local and global reef stressors remains a priority, reef restoration is an important tool; an increased understanding of the interactions between replanted corals and the fishes they support is critical for ensuring its success for people and nature.     

Shifts in bacterial communities of two caribbean reef-building coral species affected by white plague disease

Coral reefs are deteriorating at an alarming rate mainly as a consequence of the emergence of coral diseases. The white plague disease (WPD) is the most prevalent coral disease in the southwestern Caribbean, affecting dozens of coral species. However, the identification of a single causal agent has proved problematic. This suggests more complex etiological scenarios involving alterations in the dynamic interaction between environmental factors, the coral immune system and the symbiotic microbial communities. Here we compare the microbiome of healthy and WPD-affected corals from the two reef-building species Diploria strigosa and Siderastrea siderea collected at the Tayrona National Park in the Caribbean of Colombia. Microbiomes were analyzed by combining culture-dependent methods and pyrosequencing of 16S ribosomal DNA (rDNA) V5-V6 hypervariable regions. A total of 20 410 classifiable 16S rDNA sequences reads were obtained including all samples. No significant differences in operational taxonomic unit diversity were found between healthy and affected tissues; however, a significant increase of Alphaproteobacteria and a concomitant decrease in the Beta- and Gammaproteobacteria was observed in WPD-affected corals of both species. Significant shifts were also observed in the orders Rhizobiales, Caulobacteriales, Burkholderiales, Rhodobacterales, Aleteromonadales and Xanthomonadales, although they were not consistent between the two coral species. These shifts in the microbiome structure of WPD-affected corals suggest a loss of community-mediated growth control mechanisms on bacterial populations specific for each holobiont system.     

Implications of coral harvest and transplantation on reefs in northwestern Dominica

In June, 2002, the government of Dominica requested assistance in evaluating the coral culture and transplantation activities being undertaken by Oceanographic Institute of Dominica (OID), a coral farm culturing both western Atlantic and Indo-Pacific corals for restoration and commercial sales. We assessed the culture facilities of OID, the condition of reefs, potential impacts of coral collection and benefits of coral transplantation. Coral reefs (9 reefs, 3-20 m depth) were characterized by 35 species of scleractinian corals and a live coral cover of 8-35%. Early colonizing, brooders such as Porites astreoides (14.8% of all corals), P. porites (14.8%), Meandrina meandrites (14.7%) and Agaricia agaricites (9.1%) were the most abundant corals, but colonies were mostly small (mean = 25 cm diameter). Montastraea annularis (complex) was the other dominant taxa (20.8% of all corals) and colonies were larger (mean = 70 cm). Corals (pooled species) were missing an average of 20% of their tissue, with a mean of 1.4% recent mortality. Coral diseases affected 6.4% of all colonies, with the highest prevalence at Cabrits West (11.0%), Douglas Bay (12.2%) and Coconut Outer reef (20.7%). White plague and yellow band disease were causing the greatest loss of tissue, especially among M. annularis (complex), with localized impacts from corallivores, overgrowth by macroalgae, storm damage and sedimentation. While the reefs appeared to be undergoing substantial decline, restoration efforts by OlD were unlikely to promote recovery. No Pacific species were identified at OID restoration sites, yet species chosen for transplantation with highest survival included short-lived brooders (Agaricia and Porites) that were abundant in restoration sites, as well as non-reef builders (Palythoa and Erythropodium) that monopolize substrates and overgrow corals. The species of highest value for restoration (massive broadcast spawners) showed low survivorship and unrestored populations of these species were most affected by biotic stressors and human impacts, all of which need to be addressed to enhance survival of outplants. Problems with culture practices at OID, such as high water temperature, adequate light levels and persistent overgrowth by macroalgae could be addressed through simple modifications. Nevertheless, coral disease and other stressors are of major concern to the most important reef builders, as these species are less amenable to restoration, collection could threaten their survival and losses require decades to centuries to replace.     

Latent virus‐like infections are present in a diverse range of Symbiodinium spp. (Dinophyta)

Coral reefs are increasingly threatened by disease outbreaks, which affect the coral animal and/or its algal symbionts (Symbiodinium spp.) and can cause mass mortalities. Currently around half of the recognized coral diseases have unknown causative agents. While many of the diseases are thought to be bacterial in origin, there is growing evidence that viruses may play a role. In particular, it appears that viruses may infect the algal symbionts, causing breakdown of the coral‐algal mutualism. In this study, we screened a wide range of Symbiodinium cultures in vitro for the presence of latent viral infections. Using flow cytometry and electron microscopy, we found that many types of Symbiodinium apparently harbor such infections, and that the type of putative virus varied within and among host types. Furthermore, the putative viral infections could be induced via abiotic stress and cause host cell lysis and population decline. If similar processes occur in Symbiodinium cells in hospite, they may provide an explanation for some of the diseases affecting corals and other organisms forming symbioses with these algae.     

The role of microorganisms in coral health, disease and evolution

Coral microbiology is an emerging field, driven largely by a desire to understand, and ultimately prevent, the worldwide destruction of coral reefs. The mucus layer, skeleton and tissues of healthy corals all contain large populations of eukaryotic algae, bacteria and archaea. These microorganisms confer benefits to their host by various mechanisms, including photosynthesis, nitrogen fixation, the provision of nutrients and infection prevention. Conversely, in conditions of environmental stress, certain microorganisms cause coral bleaching and other diseases. Recent research indicates that corals can develop resistance to specific pathogens and adapt to higher environmental temperatures. To explain these findings the coral probiotic hypothesis proposes the occurrence of a dynamic relationship between symbiotic microorganisms and corals that selects for the coral holobiont that is best suited for the prevailing environmental conditions. Generalization of the coral probiotic hypothesis has led us to propose the hologenome theory of evolution.     

Carbonic anhydrases in anthozoan corals—A review

Coral reefs are among the most biologically diverse and economically important ecosystems on the planet. The deposition of massive calcium carbonate skeletons (biomineralization or calcification) by scleractinian corals forms the coral reef framework/architecture that serves as habitat for a large diversity of organisms. This process would not be possible without the intimate symbiosis between corals and photosynthetic dinoflagellates, commonly called zooxanthellae. Carbonic anhydrases play major roles in those two essential processes of coral’s physiology: they are involved in the carbon supply for calcium carbonate precipitation as well as in carbon-concentrating mechanisms for symbiont photosynthesis. Here, we review the current understanding of diversity and function of carbonic anhydrases in corals and discuss the perspective of theses enzymes as a key to understanding impacts of environmental changes on coral reefs.     

Density‐dependent effects on initial growth of a branching coral under restoration

Coral reef restoration aims to help threatened coral ecosystems recover from recent severe declines. Here we address whether coral fragments should be out‐planted individually or in larger aggregations. Theory suggests alternative possible outcomes: whereas out‐plants within aggregations might suffer from heightened negative interactions with neighbors (e.g. competition for space), they may alternatively benefit from positive interactions with neighbors (e.g. buffering wave disturbances). On a degraded reef in the Caribbean (St. Croix, USVI), using out‐plants of the critically endangered staghorn coral Acropora cervicornis, we experimentally tested how aggregation density (1–20 out‐planted coral fragments spaced at approximately 5 cm) influenced initial coral growth (over 3 months). Coral growth declined as a function of aggregation size, and out‐plants within larger aggregations had fewer and shorter secondary branches on average, indicative of horizontal competition for space. Our results therefore suggest that wide spacing of individuals will maximize the initial growth of out‐planted branching corals.     

A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals

Diseases are an emerging threat to ocean ecosystems. Coral reefs, in particular, are experiencing a worldwide decline because of disease and bleaching, which have been exacerbated by rising seawater temperatures. Yet, the ecological mechanisms behind most coral diseases remain unidentified. Here, we demonstrate that a coral pathogen, Vibrio coralliilyticus, uses chemotaxis and chemokinesis to target the mucus of its coral host, Pocillopora damicornis. A primary driver of this response is the host metabolite dimethylsulfoniopropionate (DMSP), a key element in the global sulfur cycle and a potent foraging cue throughout the marine food web. Coral mucus is rich in DMSP, and we found that DMSP alone elicits chemotactic responses of comparable intensity to whole mucus. Furthermore, in heat-stressed coral fragments, DMSP concentrations increased fivefold and the pathogen''s chemotactic response was correspondingly enhanced. Intriguingly, despite being a rich source of carbon and sulfur, DMSP is not metabolized by the pathogen, suggesting that it is used purely as an infochemical for host location. These results reveal a new role for DMSP in coral disease, demonstrate the importance of chemical signaling and swimming behavior in the recruitment of pathogens to corals and highlight the impact of increased seawater temperatures on disease pathways.     

Coral recruitment: patterns and processes determining the dynamics of coral populations

Coral recruitment describes the addition of new individuals to populations, and it is one of the most fundamental demographic processes contributing to population size. As many coral reefs around the world have experienced large declines in coral cover and abundance, there has been great interest in understanding the factors causing coral recruitment to vary and the conditions under which it can support community resilience. While progress in these areas is being facilitated by technological and scientific advances, one of the best tools to quantify recruitment remains the humble settlement tile, variants of which have been in use for over a century. Here I review the biology and ecology of coral recruits and the recruitment process, largely as resolved through the use of settlement tiles, by: (i) defining how the terms ‘recruit’ and ‘recruitment’ have been used, and explaining why loose terminology has impeded scientific advancement; (ii) describing how coral recruitment is measured and why settlement tiles have value for this purpose; (iii) summarizing previous efforts to review quantitative analyses of coral recruitment; (iv) describing advances from hypothesis-driven studies in determining how refuges, seawater flow, and grazers can modulate coral recruitment; (v) reviewing the biology of small corals (i.e. recruits) to understand better how they respond to environmental conditions; and (vi) updating a quantitative compilation of coral recruitment studies extending from 1974 to present, thus revealing long-term global declines in density of recruits, juxtaposed with apparent resilience to coral bleaching. Finally, I review future directions in the study of coral recruitment, and highlight the need to expand studies to deliver taxonomic resolution, and explain why time series of settlement tile deployments are likely to remain pivotal in quantifying coral recruitment.     

Global coral disease prevalence associated with sea temperature anomalies and local factors

Coral diseases are taking an increasing toll on coral reef structure and biodiversity and are important indicators of declining health in the oceans. We implemented standardized coral disease surveys to pinpoint hotspots of coral disease, reveal vulnerable coral families and test hypotheses about climate drivers from 39 locations worldwide. We analyzed a 3 yr study of coral disease prevalence to identify links between disease and a range of covariates, including thermal anomalies (from satellite data), location and coral cover, using a Generalized Linear Mixed Model. Prevalence of unhealthy corals, i.e. those with signs of known diseases or with other signs of compromised health, exceeded 10% on many reefs and ranged to over 50% on some. Disease prevalence exceeded 10% on 20% of Caribbean reefs and 2.7% of Pacific reefs surveyed. Within the same coral families across oceans, prevalence of unhealthy colonies was higher and some diseases were more common at sites in the Caribbean than those in the Pacific. The effects of high disease prevalence are potentially extensive given that the most affected coral families, the acroporids, faviids and siderastreids, are among the major reef-builders at these sites. The poritids and agaricids stood out in the Caribbean as being the most resistant to disease, even though these families were abundant in our surveys. Regional warm temperature anomalies were strongly correlated with high disease prevalence. The levels of disease reported here will provide a much-needed local reference point against which to compare future change.     

Algal contact as a trigger for coral disease

Diseases are causing alarming declines in reef‐building coral species, the foundation blocks of coral reefs. The emergence of these diseases has occurred simultaneously with large increases in the abundance of benthic macroalgae. Here, we show that physical contact with the macroalga Halimeda opuntia can trigger a virulent disease known as white plague type II that has caused widespread mortality in most Caribbean coral species. Colonies of the dominant coral Montastraea faveolata exposed to algal transplants developed the disease whereas unexposed colonies did not. The bacterium Aurantimonas coralicida, causative agent of the disease, was present on H. opuntia sampled close to, and away from diseased corals, indicating that the alga serves as a reservoir for this pathogen. Our results suggest that the spread of macroalgae on coral reefs could account for the elevated incidence of coral diseases over past decades and that reduction of macroalgal abundance could help control coral epizootics.     

Coral reefs studies and threats in Malaysia: a mini review

Coral reefs in Malaysia are about 4,006 km² with over 550 species contributed to nation’s economy. Coral reefs studies and threats in Malaysia have been reviewed briefly. Perspectives are addressed as coral reefs studies, threats, gaps and future studies. Coral reefs in Malaysia are being damaged at an increasing rate where it faces natural and anthropogenic stresses. Excellent summaries are available in terms of coral reefs cover throughout Malaysia however scarce in terms of qualitative, quantitative and biogeographical data. There are also limited studies on heavy metals concentration in corals skeleton studies. Poor to fair conditions of coral reefs in Peninsular Malaysia is due to increases of sedimentation and tourism impacts. Overfishing and fish blasting were main threats of coral reefs damage in Sabah. In Sarawak, coral reefs are threatened by high sedimentation and sand mining. The 1998–1999 bleaching event also affected coral reefs in Malaysia due to climate change. Gaps in coral reefs studies can be completed by continuous collaborations between local and international researchers as well as research by local universities. Economic valuation, policy analysis and community participation are directions in future coral reefs studies in Malaysia. Future studies are to understand effects of management on coral reefs health and impact of pollution on coral reefs growth with a standard coral reefs methodology. Established legal systems to reduce threats received by coral reefs are also need to be introduced. Role of science-driven management with community participation and media mass are also gaps to be highlighted in future studies.     

Algae as Reservoirs for Coral Pathogens

Benthic algae are associated with coral death in the form of stress and disease. It''s been proposed that they release exudates, which facilitate invasion of potentially pathogenic microbes at the coral-algal interface, resulting in coral disease. However, the original source of these pathogens remains unknown. This study examined the ability of benthic algae to act as reservoirs of coral pathogens by characterizing surface associated microbes associated with major Caribbean and Indo-Pacific algal species/types and by comparing them to potential pathogens of two dominant coral diseases: White Syndrome (WS) in the Indo-Pacific and Yellow Band Disease (YBD) in the Caribbean. Coral and algal sampling was conducted simultaneously at the same sites to avoid spatial effects. Potential pathogens were defined as those absent or rare in healthy corals, increasing in abundance in healthy tissues adjacent to a disease lesion, and dominant in disease lesions. Potentially pathogenic bacteria were detected in both WS and YBD and were also present within the majority of algal species/types (54 and 100% for WS and YBD respectively). Pathogenic ciliates were associated only with WS and not YBD lesions and these were also present in 36% of the Indo-Pacific algal species. Although potential pathogens were associated with many algal species, their presence was inconsistent among replicate algal samples and detection rates were relatively low, suggestive of low density and occurrence. At the community level, coral-associated microbes irrespective of the health of their host differed from algal-associated microbes, supporting that algae and corals have distinctive microbial communities associated with their tissue. We conclude that benthic algae are common reservoirs for a variety of different potential coral pathogens. However, algal-associated microbes alone are unlikely to cause coral death. Initial damage or stress to the coral via other competitive mechanisms is most likely a prerequisite to potential transmission of these pathogens.     

Coral reef bleaching: ecological perspectives

Coral reef bleaching, the whitening of diverse invertebrate taxa, results from the loss of symbiotic zooxanthellae and/or a reduction in photosynthetic pigment concentrations in zooxanthellae residing within the gastrodermal tissues of host animals. Of particular concern are the consequences of bleaching of large numbers of reef-building scleractinian corals and hydrocorals. Published records of coral reef bleaching events from 1870 to the present suggest that the frequency (60 major events from 1979 to 1990), scale (co-occurrence in many coral reef regions and often over the bathymetric depth range of corals) and severity (>95% mortality in some areas) of recent bleaching disturbances are unprecedented in the scientific literature. The causes of small scale, isolated bleaching events can often be explained by particular stressors (e.g., temperature, salinity, light, sedimentation, aerial exposure and pollutants), but attempts to explain large scale bleaching events in terms of possible global change (e.g., greenhouse warming, increased UV radiation flux, deteriorating ecosystem health, or some combination of the above) have not been convincing. Attempts to relate the severity and extent of large scale coral reef bleaching events to particular causes have been hampered by a lack of (a) standardized methods to assess bleaching and (b) continuous, long-term data bases of environmental conditions over the periods of interest. An effort must be made to understand the impact of bleaching on the remainder of the reef community and the long-term effects on competition, predation, symbioses, bioerosion and substrate condition, all factors that can influence coral recruitment and reef recovery. If projected rates of sea warming are realized by mid to late AD 2000, i.e. a 2°C increase in high latitude coral seas, the upper thermal tolerance limits of many reef-building corals could be exceeded. Present evidence suggests that many corals would be unable to adapt physiologically or genetically to such marked and rapid temperature increases.