The global significance of Scleractinian corals without photoendosymbiosis.

Globally tropical Scleractinian corals have been a focal point for discussions on the impact of a changing climate on marine ecosystems and biodiversity. Research into tropical Scleractinian corals, particularly the role and breakdown of photoendosymbiosis in response to warming, has been prolific in recent decades. However, research into their subtropical, temperate, cold- and deep-water counterparts, whose number is dominated by corals without photoendosymbiosis, has not been as prolific. Approximately 50% of Scleractinian corals (> 700 species) do not maintain photoendosymbiosis and as such, do not rely upon the products of photosynthesis for homeostasis. Some species also have variable partnerships with photendosymbionts depending on life history and ecological niche. Here we undertake a systematic map of literature on Scleractinian corals without, or with variable, photoendosymbiosis. In doing so we identify 482 publications spanning 5 decades. In mapping research effort, we find publications have been sporadic over time, predominately focusing on a limited number of species, with greater research effort directed towards deep-water species. We find only 141 species have been studied, with approximately 30% of the total identified research effort directed toward a single species, Desmophyllum pertusum, highlighting significant knowledge gaps into Scleractinian diversity. We find similar limitations to studied locations, with 78 identified from the global data, of which only few represent most research outputs. We also identified inconsistencies with terminology used to describe Scleractinia without photoendosymbiosis, likely contributing to difficulties in accounting for their role and contribution to marine ecosystems. We propose that the terminology requires re-evaluation to allow further systematic assessment of literature, and to ensure it's consistent with changes implemented for photoendosymbiotic corals. Finally, we find that knowledge gaps identified over 20 years ago are still present for most aphotoendosymbiotic Scleractinian species, and we show data deficiencies remain regarding their function, biodiversity and the impacts of anthropogenic stressors.

Localising terrestrially derived pollution inputs to threatened near-shore coral reefs through stable isotope, water quality and oceanographic analysis.

Near-shore coral reefs are at high-risk of exposure to pollution from terrestrial activities. Pollution impacts can vary with site-specific factors that span sources, rainfall and oceanographic characteristics. To effectively manage pollution, we need to understand how these factors interact. In this study, we detect terrestrially derived nutrient inputs on near-shore reefs at Norfolk Island, South Pacific by analysis of dissolved inorganic nitrogen (DIN) and stable isotopes. When compared to a reef site with predominantly oceanic inputs, we found that both the lagoon and a small reef adjacent to a catchment have signatures of human-derived DIN shown through depleted δ15N signatures in macroalgae. We find pollution exposure of reef sites is associated with known and unknown sources, rainfall and mixing of water with the open ocean. In characterising exposure of reef sites we highlight the role of site-specific context in influencing pollution exposure for benthic communities even in remote island systems.

Characteristics of The Bleached Microbiome of The Generalist Coral Pocillopora damicornis from Two Distinct Reef Habitats.

Generalist coral species may play an important role in predicting, managing, and responding to the growing coral reef crisis as sea surface temperatures are rising and reef wide bleaching events are becoming more common. Pocilloporids are amongst the most widely distributed and studied of generalist corals, characterized by a broad geographic distribution, phenotypic plasticity, and tolerance of sub-optimal conditions for coral recruitment and survival. Emerging research indicates that microbial communities associated with Pocilloporid corals may be contributing to their persistence on coral reefs impacted by thermal stress; however, we lack detailed information on shifts in the coral-bacterial symbiosis during bleaching events across many of the reef habitats these corals are found. Here, we characterized the bacterial communities of healthy and bleached Pocillopora damicornis corals during the bleaching events that occurred during the austral summer of 2020 on Heron Island, on the southern Great Barrier Reef, and the austral summer of 2019 on Lord Howe Island, the most southerly coral reef in Australia. Regardless of reef location, significant differences in α and ß diversities, core bacterial community, and inferred functional profile of the bleached microbiome of P. damicornis were not detected. Consistent with previous reports, patterns in the Pocilloporid coral microbiome, including no increase in pathogenic taxa or evidence of dysbiosis, are conserved during bleaching responses. We hypothesize that the resilience of holobiont interactions may aid the Pocilloporids to survive Symbiodiniaceae loss and contribute to the success of Pocilloporids.

High flow conditions mediate damaging impacts of sub-lethal thermal stress on corals' endosymbiotic algae.

The effects of thermal anomalies on tropical coral endosymbiosis can be mediated by a range of environmental factors, which in turn ultimately influence coral health and survival. One such factor is the water flow conditions over coral reefs and corals. Although the physiological benefits of living under high water flow are well known, there remains a lack of conclusive experimental evidence characterizing how flow mitigates thermal stress responses in corals. Here we use in situ measurements of flow in a variety of reef habitats to constrain the importance of flow speeds on the endosymbiosis of an important reef building species under different thermal regimes. Under high flow speeds (0.15 m s-1) and thermal stress, coral endosymbionts retained photosynthetic function and recovery capacity for longer compared to low flow conditions (0.03 m s-1). We hypothesize that this may be due to increased rates of mass transfer of key metabolites under higher flow, putatively allowing corals to maintain photosynthetic efficiency for longer. We also identified a positive interactive effect between high flow and a pre-stress, sub-lethal pulse in temperature. While higher flow may delay the onset of photosynthetic stress, it does not appear to confer long-term protection; sustained exposure to thermal stress (eDHW accumulation equivalent to 4.9°C weeks) eventually overwhelmed the coral meta-organism as evidenced by eventual declines in photo-physiological function and endosymbiont densities. Investigating flow patterns at the scale of metres within the context of these physiological impacts can reveal interesting avenues for coral reef management. This study increases our understanding of the effects of water flow on coral reef health in an era of climate change and highlights the potential to learn from existing beneficial bio-physical interactions for the effective preservation of coral reefs into the future.

Light Capture, Skeletal Morphology, and the Biomass of Corals' Boring Endoliths.

There is a growing interest in the endolithic microbial biofilms inhabiting skeletons of living corals because of their contribution to coral reef bioerosion and the reputed benefits they provide to live coral hosts. Here, we sought to identify possible correlations between coral interspecific patterns in skeletal morphology and variability in the biomass of, and chlorophyll concentrations within, the endolithic biofilm. We measured five morphological characteristics of five coral species and the biomasses/chlorophyll concentrations of their endolithic microbiome, and we compare interspecific patterns in these variables. We propose that the specific density of a coral's skeleton and its capacity for capturing and scattering incident light are the main correlates of endolithic microbial biomass. Our data suggest that the correlation between light capture and endolithic biomass is likely influenced by how the green microalgae (obligatory microborers) respond to skeletal variability. These results demonstrate that coral species differ significantly in their endolithic microbial biomass and that their skeletal structure could be used to predict these interspecific differences. Further exploring how and why the endolithic microbiome varies between coral species is vital in defining the role of these microbes on coral reefs, both now and in the future.IMPORTANCE Microbial communities living inside the skeletons of living corals play a variety of important roles within the coral meta-organism, both symbiotic and parasitic. Properly contextualizing the contribution of these enigmatic microbes to the life history of coral reefs requires knowledge of how these endolithic biofilms vary between coral species. To this effect, we measured differences in the morphology of five coral species and correlate these with variability in the biomass of the skeletal biofilms. We found that the density of the skeleton and its capacity to trap incoming light, as opposed to scattering it back into the surrounding water, both significantly correlated with skeletal microbial biomass. These patterns are likely driven by how dominant green microalgae in the endolithic niche, such as Ostreobium spp., are responding to the skeletal morphology. This study highlights that the structure of a coral's skeleton could be used to predict the biomass of its resident endolithic biofilm.

Coral Disease Causes, Consequences, and Risk within Coral Restoration.

As a result of increased reef degradation, restoration efforts are now being widely applied on coral reefs. However, outplanted coral survival in restoration zones varies substantially, and coral mortality can be a significant limitation to the success of restoration efforts. With reef restoration now occurring within, and adjacent to, nationally preserved and managed marine parks, the potential risks of mortality events and disease spread to adjacent marine populations need to be considered, particularly as these ecosystems continue to decline. We review the causes and consequences of coral mortality and disease outbreaks within the context of coral restoration, highlighting knowledge gaps in our understanding of the restored coral microbiome and discussing management practices for assessing coral disease. We identify the need for research efforts into monitoring and diagnostics of disease within coral restoration, as well as practices to mitigate and manage coral disease risks in restoration.

Microalgae, a Boring Bivalve and a Coral-A Newly Described Association Between Two Coral Reef Bioeroders Within Their Coral Host.

Bioeroding organisms play an important part in shaping structural complexity and carbonate budgets on coral reefs. Species interactions between various bioeroders are an important area of study, as these interactions can affect net rates of bioerosion within a community and mediate how bioeroders respond to environmental change. Here we test the hypothesis that the biomass of endolithic bioeroding microalgae is positively associated with the presence of a macroboring bivalve. We compared the biomass and chlorophyll concentrations of microendolithic biofilms in branches of the coral Isopora palifera (Lamarck, 1816) that were or were not inhabited by a macroboring bivalve. Those branches with a macroborer present hosted ∼80% higher microbial biomass compared to adjacent branches from the same coral with no macroborer. Increased concentrations of chlorophyll b indicated that this was partly due to a greater abundance of green microalgae. This newly described association has important implications for the coral host as both the bivalve and the microalgae have been hypothesized as symbiotic.

The Other Microeukaryotes of the Coral Reef Microbiome.

In marine ecosystems microbial communities are critical to ocean function, global primary productivity, and biogeochemical cycles. Both prokaryotic and eukaryotic microbes are essential symbionts and mutualists, nonpathogenic invaders, primary pathogens, have been linked to disease emergence, and can underpin broader ecosystem changes. However, in the effort to determine coral-microbial interactions, the structure and function of the eukaryotic microbes of the microbiome have been studied less. Eukaryotic microbes are important members of the microbiome, constitute entire kingdoms of life, and make important contributions to ecosystem function. Here, we outline the roles of eukaryotic microbes in marine systems and their contribution to ecosystem change, and discuss the microeukaryotic microbiome of corals and coral reefs.

In situ hybridisation detects pro-apoptotic gene expression of a Bcl-2 family member in white syndrome-affected coral.

White syndrome has been described as one of the most prolific diseases on the Great Barrier Reef. Previously, apoptotic cell death has been described as the mechanism driving the characteristic rapid tissue loss associated with this disease, but the molecular mechanisms controlling apoptotic cell death in coral disease have yet to be investigated. In situ methods were used to study the expression patterns of 2 distinct regulators of apoptosis in Acropora hyacinthus tissues undergoing white syndrome and apoptotic cell death. Apoptotic genes within the Bcl-2 family were not localized in apparently healthy coral tissues. However, a Bcl-2 family member (bax-like) was found to localize to cells and tissues affected by white syndrome and those with morphological evidence for apoptosis. A potential up-regulation of pro-apoptotic or bax-like gene expression in tissues with apoptotic cell death adjacent to disease lesions is consistent with apoptosis being the primary cause of rapid tissue loss in coral affected by white syndrome. Pro-apoptotic (bax-like) expression in desmocytes and the basal tissue layer, the calicodermis, distant from the disease lesion suggests that apoptosis may also underlie the sloughing of healthy tissues associated with the characteristic, rapid spread of tissue loss, evident of this disease. This study also shows that in situ hybridisation is an effective tool for studying gene expression in adult corals, and wider application of these methods should allow a better understanding of many aspects of coral biology and disease pathology.

Defining the tipping point: a complex cellular life/death balance in corals in response to stress.

Apoptotic cell death has been implicated in coral bleaching but the molecules involved and the mechanisms by which apoptosis is regulated are only now being identified. In contrast the mechanisms underlying apoptosis in higher animals are relatively well understood. To better understand the response of corals to thermal stress, the expression of coral homologs of six key regulators of apoptosis was studied in Acropora aspera under conditions simulating those of a mass bleaching event. Significant changes in expression were detected between the daily minimum and maximum temperatures. Maximum daily temperatures from as low as 3°C below the bleaching threshold resulted in significant changes in both pro- and anti-apoptotic gene expression. The results suggest that the control of apoptosis is highly complex in this eukaryote-eukaryote endosymbiosis and that apoptotic cell death cascades potentially play key roles tipping the cellular life/death balance during environmental stress prior to the onset of coral bleaching.

Diets of coral-dwelling fishes of the genus Gobiodon with evidence of corallivory.

Evidence of facultative corallivory is documented in three species of obligate coral-dwelling gobies (genus Gobiodon) based on the presence of spirocysts in gut contents. Coral-dwelling gobies also consumed a broad range of other items with gut contents dominated by algae, invertebrates and amorphous material. Dietary similarities between species suggest corallivory may be widespread in this genus.

Imaging the fluorescence of marine invertebrates and their associated flora.

The cells and tissues of many marine invertebrates and their associated flora contain fluorescent pigments and proteins, many of which have been utilized commercially and provide marker molecules in other systems for fluorescence imaging technology. However, in the study of marine invertebrates and their symbioses these naturally occurring molecules have been seen to limit or confound fluorescence microscopy analyses. Here we demonstrate the endogenous fluorescence associated with two marine invertebrates (coral and foraminifera) and describe how these qualities can be utilized in fluorescence microanalyses. Understanding and imaging the diversity of fluorescent molecules provide insight into how fluorescence microscopy techniques can now be applied to these complex systems.

Bacteria are not the primary cause of bleaching in the Mediterranean coral Oculina patagonica.

Coral bleaching occurs when the endosymbiosis between corals and their symbionts disintegrates during stress. Mass coral bleaching events have increased over the past 20 years and are directly correlated with periods of warm sea temperatures. However, some hypotheses have suggested that reef-building corals bleach due to infection by bacterial pathogens. The 'Bacterial Bleaching' hypothesis is based on laboratory studies of the Mediterranean invading coral, Oculina patagonica, and has further generated conclusions such as the coral probiotic hypothesis and coral hologenome theory of evolution. We aimed to investigate the natural microbial ecology of O. patagonica during the annual bleaching using fluorescence in situ hybridization to map bacterial populations within the coral tissue layers, and found that the coral bleaches on the temperate rocky reefs of the Israeli coastline without the presence of Vibrio shiloi or bacterial penetration of its tissue layers. Bacterial communities were found associated with the endolithic layer of bleached coral regions, and a community dominance shift from an apparent cyanobacterial-dominated endolithic layer to an algal-dominated layer was found in bleached coral samples. While bacterial communities certainly play important roles in coral stasis and health, we suggest environmental stressors, such as those documented with reef-building corals, are the primary triggers leading to bleaching of O. patagonica and suggest that bacterial involvement in patterns of bleaching is that of opportunistic colonization.

Coral disease diagnostics: what's between a plague and a band?

Recently, reports of coral disease have increased significantly across the world's tropical oceans. Despite increasing efforts to understand the changing incidence of coral disease, very few primary pathogens have been identified, and most studies remain dependent on the external appearance of corals for diagnosis. Given this situation, our current understanding of coral disease and the progression and underlying causes thereof is very limited. In the present study, we use structural and microbial studies to differentiate different forms of black band disease: atypical black band disease and typical black band disease. Atypical black band diseased corals were infected with the black band disease microbial consortium yet did not show any of the typical external signs of black band disease based on macroscopic observations. In previous studies, these examples, here referred to as atypical black band disease, would have not been correctly diagnosed. We also differentiate white syndrome from white diseases on the basis of tissue structure and the presence/absence of microbial associates. White diseases are those with dense bacterial communities associated with lesions of symbiont loss and/or extensive necrosis of tissues, while white syndromes are characteristically bacterium free, with evidence for extensive programmed cell death/apoptosis associated with the lesion and the adjacent tissues. The pathology of coral disease as a whole requires further investigation. This study emphasizes the importance of going beyond the external macroscopic signs of coral disease for accurate disease diagnosis.

Fluorescence in situ hybridization and spectral imaging of coral-associated bacterial communities.

Microbial communities play important roles in the functioning of coral reef communities. However, extensive autofluorescence of coral tissues and endosymbionts limits the application of standard fluorescence in situ hybridization (FISH) techniques for the identification of the coral-associated bacterial communities. This study overcomes these limitations by combining FISH and spectral imaging.