Reef Sediments Can Act As a Stony Coral Tissue Loss Disease Vector

Stony coral tissue loss disease (SCTLD) was first observed in 2014 near Virginia Key in Miami-Dade County, Florida. Field sampling, lab experiments, and modeling approaches have suggested that reef sediments may play a role in SCTLD transmission, though a positive link has not been tested experimentally. We conducted an ex situ transmission assay using a statistically-independent disease apparatus to test whether reef sediments can transmit SCTLD in the absence of direct contact between diseased and healthy coral tissue. We evaluated two methods of sediment inoculation: batch inoculation of sediments collected from southeast Florida using whole colonies of diseased Montastraea cavernosa, and individual inoculations of sediments following independent, secondary infections of ∼5 cm2 coral fragments. Healthy fragments of the coral species Orbicella faveolata and M. cavernosa were exposed to these diseased sediment treatments, as well as direct disease contact and healthy sediment controls. SCTLD transmission was observed for both batch and individual diseased sediment inoculation treatments, albeit with lower proportions of infected individuals as compared to disease contact controls. The time to onset of lesions was significantly different between species and among disease treatments, with the most striking infections occurring in the individual diseased sediment treatment in under 24 h. Following infection, tissue samples were confirmed for the presence of SCTLD signs via histological examination, and sediment subsamples were analyzed for microbial community variation between treatments, identifying 16 SCTLD indicator taxa in sediments associated with corals experiencing tissue loss. This study demonstrated that reef sediments can indeed transmit SCTLD through indirect exposure between diseased and healthy corals, and adds credence to the assertion that SCTLD transmission occurs via an infectious agent or agents. This study emphasizes the critical need to understand the roles that sediment microbial communities and coastal development activities may have on the persistence of SCTLD throughout the endemic zone, especially in the context of management and conservation strategies in Florida and the wider Caribbean.

Bacterial Metabolic Potential and Micro-Eukaryotes Enriched in Stony Coral Tissue Loss Disease Lesions

The epizootic disease outbreak known as stony coral tissue loss disease (SCTLD) is arguably the most devastating coral disease in recorded history. SCTLD emerged off the coast of South Florida in 2014 and has since moved into the Caribbean, resulting in coral mortality rates that have changed reef structure and function. Currently, the cause of SCTLD is unknown, but there is evidence from 16S rRNA gene sequencing and bacterial culture studies that the microbial community plays a role in the progression of SCTLD lesions. In this study, we applied shotgun metagenomics to characterize the potential function of bacteria, as well as the composition of the micro-eukaryotic community, associated with SCTLD lesions. We re-examined samples that were previously analyzed using 16S rRNA gene high-throughput sequencing from four coral species: Stephanocoenia intersepta, Diploria labyrinthiformis, Dichocoenia stokesii, and Meandrina meandrites. For each species, tissue from apparently healthy (AH) corals, and unaffected tissue (DU) and lesion tissue (DL) on diseased corals, were collected from sites within the epidemic zone of SCTLD in the Florida Keys. Within the micro-eukaryotic community, the taxa most prominently enriched in DL compared to AH and DU tissue were members of Ciliophora. We also found that DL samples were relatively more abundant in less energy-efficient pathways like the pentose phosphate pathways. While less energy-efficient processes were identified, there were also relatively higher abundances of nucleotide biosynthesis and peptidoglycan maturation pathways in diseased corals compared to AH, which suggests there was more bacteria growth in diseased colonies. In addition, we generated 16 metagenome-assembled genomes (MAGs) belonging to the orders Pseudomonadales, Beggiatoales, Rhodobacterales, Rhizobiales, Rs-D84, Flavobacteriales, and Campylobacterales, and all MAGs were enriched in DL samples compared to AH samples. Across all MAGs there were antibiotic resistance genes that may have implications for the treatment of SCTLD with antibiotics. We also identified genes and pathways linked to virulence, such as nucleotide biosynthesis, succinate dehydrogenase, ureases, nickel/iron transporters, Type-1 secretion system, and metalloproteases. Some of these enzymes/pathways have been previously targeted in the treatment of other bacterial diseases and they may be of interest to mitigate SCTLD lesion progression.

Effect of species, size, and chimerism on the susceptibility of Caribbean brain coral recruits to stony coral tissue loss disease (SCTLD)

Stony coral tissue loss disease (SCTLD) has devastated coral populations along Florida′s Coral Reef and beyond. Although widespread infection and mortality of adult colonies have been documented, no studies have yet investigated the susceptibility of recruits to this disease. Here, we exposed eight-month-old Diploria labyrinthiformis recruits and four-month-old Colpophyllia natans recruits to two sequential doses of SCTLD in the laboratory to track infection and assess potential resilience. Both species began to develop lesions as early as 48 h after exposure began. During the first dose, 59.0% of C. natans recruits lost all tissue (died) within two to eight days of developing lesions, whereas D. labyrinthiformis recruits experienced significantly slower rates of tissue loss and minimal eventual mortality. In C. natans, larger recruits and those fused into groups of multiple genets (chimeras) exhibited the highest survivorship. In contrast, smaller and/or single (ungrouped) recruits had the lowest survivorship (9.9 - 26.5%). After 20 days, a second SCTLD dose was delivered to further test resistance in remaining recruits, and all recruits of both species succumbed within 6 days. Although no recruits showed absolute resistance to SCTLD following repeated exposures, our results provide evidence that interactions between species, size, and chimerism can impact relative resistance. This study represents the first report of SCTLD in Caribbean coral recruits and carries implications for natural species recovery and reef restoration efforts. Additional research on the susceptibility of coral juveniles to SCTLD is urgently needed, to include different species, locations, parents, and algal symbionts, with the goal of assessing relative susceptibility and identifying potential sources of resilience for this critical life history stage.

Viral-Like Particles Are Associated With Endosymbiont Pathology in Florida Corals Affected by Stony Coral Tissue Loss Disease

Stony coral tissue loss disease (SCTLD) was first documented in 2014 near the Port of Miami, Florida, and has since spread north and south along Florida’s Coral Reef, killing large numbers of more than 20 species of coral and leading to the functional extinction of at least one species, Dendrogyra cylindrus. SCTLD is assumed to be caused by bacteria based on presence of different molecular assemblages of bacteria in lesioned compared to apparently healthy tissues, its apparent spread among colonies, and cessation of spread of lesions in individual colonies treated with antibiotics. However, light microscopic examination of tissues of corals affected with SCTLD has not shown bacteria associated with tissue death. Rather, microscopy shows dead and dying coral cells and symbiotic dinoflagellates (endosymbionts) indicating a breakdown of host cell and endosymbiont symbiosis. It is unclear whether host cells die first leading to death of endosymbionts or vice versa. Based on microscopy, hypotheses as to possible causes of SCTLD include infectious agents not visible at the light microscopy level or toxicosis, perhaps originating from endosymbionts. To clarify this, we examined corals affected with SCTLD and apparently healthy corals using transmission electron microscopy. Endosymbionts in SCTLD-affected and apparently healthy corals consistently had varying degrees of pathology associated with elongated particles compatible in morphology with filamentous positive single-stranded RNA viruses of plants termed anisometric viral-like particles (AVLP). There was apparent progression from early to late replication of AVLP in the cytoplasm of endosymbionts adjacent to or at times within chloroplasts, with morphologic changes in chloroplasts consistent with those seen in plant cells infected by viruses. Coral host cell pathology appeared limited to massive proliferation and lysis of mucus cells. Based on these findings, we hypothesize that SCTLD is a viral disease of endosymbionts leading to coral host death. Efforts to confirm the presence of a virus associated with SCTLD through other means would be appropriate. These include showing the presence of a virus through molecular assays such as deep sequencing, attempts to grow this virus in the laboratory through culture of endosymbionts, localization of virus in tissue sections using immunohistochemistry or in situ hybridization, and experimental infection of known-virus-negative corals to replicate disease at the gross and microscopic level.

Similarities and Differences Between Two Deadly Caribbean Coral Diseases: White Plague and Stony Coral Tissue Loss Disease

For several decades, white plagues (WPDs: WPD-I, II and III) and more recently, stony coral tissue loss disease (SCTLD) have significantly impacted Caribbean corals. These diseases are often difficult to separate in the field as they produce similar gross signs. Here we aimed to compare what we know about WPD and SCTLD in terms of: (1) pathology, (2) etiology, and (3) epizootiology. We reviewed over 114 peer-reviewed publications from 1973 to 2021. Overall, WPD and SCTLD resemble each other macroscopically, mainly due to the rapid tissue loss they produce in their hosts, however, SCTLD has a more concise case definition. Multiple-coalescent lesions are often observed in colonies with SCTLD and rarely in WPD. A unique diagnostic sign of SCTLD is the presence of bleached circular areas when SCTLD lesions are first appearing in the colony. The paucity of histopathologic archives for WPDs for multiple species across geographies makes it impossible to tell if WPD is the same as SCTLD. Both diseases alter the coral microbiome. WPD is controversially regarded as a bacterial infection and more recently a viral infection, whereas for SCTLD the etiology has not been identified, but the putative pathogen, likely to be a virus, has not been confirmed yet. Most striking differences between WPD and SCTLD have been related to duration and phases of epizootic events and mortality rates. While both diseases may become highly prevalent on reefs, SCTLD seems to be more persistent even throughout years. Both transmit directly (contact) and horizontally (waterborne), but organism-mediated transmission is only proven for WPD-II. Given the differences and similarities between these diseases, more detailed information is needed for a better comparison. Specifically, it is important to focus on: (1) tagging colonies to look at disease progression and tissue mortality rates, (2) tracking the fate of the epizootic event by looking at initial coral species affected, the features of lesions and how they spread over colonies and to a wider range of hosts, (3) persistence across years, and (4) repetitive sampling to look at changes in the microbiome as the disease progresses. Our review shows that WPDs and SCTLD are the major causes of coral tissue loss recorded in the Caribbean.

Metabolomics of Healthy and Stony Coral Tissue Loss Disease Affected Montastraea cavernosa Corals

Stony coral tissue loss disease, first observed in Florida in 2014, has now spread along the entire Florida Reef Tract and on reefs in many Caribbean countries. The disease affects a variety of coral species with differential outcomes, and in many instances results in whole-colony mortality. We employed untargeted metabolomic profiling of Montastraea cavernosa corals affected by stony coral tissue loss disease to identify metabolic markers of disease. Herein, extracts from apparently healthy, diseased, and recovered Montastraea cavernosa collected at a reef site near Ft. Lauderdale, Florida were subjected to liquid-chromatography mass spectrometry-based metabolomics. Unsupervised principal component analysis reveals wide variation in metabolomic profiles of healthy corals of the same species, which differ from diseased corals. Using a combination of supervised and unsupervised data analyses tools, we describe metabolite features that explain variation between the apparently healthy corals, between diseased corals, and between the healthy and the diseased corals. By employing a culture-based approach, we assign sources of a subset of these molecules to the endosymbiotic dinoflagellates, Symbiodiniaceae. Specifically, we identify various endosymbiont- specific lipid classes, such as betaine lipids, glycolipids, and tocopherols, which differentiate samples taken from apparently healthy corals and diseased corals. Given the variation observed in metabolite fingerprints of corals, our data suggests that metabolomics is a viable approach to link metabolite profiles of different coral species with their susceptibility and resilience to numerous coral diseases spreading through reefs worldwide.

Considering Commercial Vessels as Potential Vectors of Stony Coral Tissue Loss Disease

Stony coral tissue loss disease (SCTLD) is a troubling new disease that is spreading rapidly across the greater Caribbean region, but the etiological agent(s) and the mechanisms(s) of spread are both unknown. First detected off the coast of Miami, Florida, major ocean currents alone do not explain the pattern of spread, with outbreaks occurring across geographically disjunct and distant locations. This has raised concerns by researchers and resource managers that commercial vessels may contribute as vectors to spread of the disease. Despite existing regulatory and management strategies intended to limit coastal marine invasion risks, the efficacy of these measures is still unresolved for ship-borne microorganisms, and disease transport via ballast water and hull biofouling are under examination given the high ship traffic in the region. Here, to help inform the discussion of ships as possible vectors of SCTLD, we provide an overview of the current state of knowledge about ships and their potential to transfer organisms in the greater Caribbean, focusing in particular on ballast water, and outline a set of recommendations for future research.

Coral-inspired hierarchical structures for sunlight harvesting

Concentrating solar thermal (CST) is an efficient renewable energy technology with low-cost thermal energy storage. CST relies on wide-spectrum solar thermal absorbers that must withstand high temperatures (> 700°C) for many years, but state-of-the-art coatings have poor optical stability. Here, we show that the largely overlooked macro-scale morphology is key to enhancing both optical resilience and light trapping. Inspired by stony-coral morphology, we developed a hierarchical coating with three tuneable length-scale morphologies: nano- (~ 120 nm), micro- (~ 3 µm) and macro-scales (> 50 µm). Our coating exhibits outstanding, stable solar-weighted absorptance of > 97.75 ± 0.04% after ageing at 850°C for more than 2,000 hours. The scalability of our coating is demonstrated on a commercial solar thermal receiver, paving the way for more reliable high-performance solar thermal systems. Scleractinia, commonly known as stony corals (Fig. 1a), have evolved their morphology over millions of years to improve their chances of survival. A symbiotic relationship with algae, which need sunlight for photosynthesis, was an evolutionary milestone 240 million years ago that enabled corals to secure nutrients in otherwise infertile waters1 and thrive in all Earth’s oceans. Sunlight attenuation in seawater initially restricted coral colonies to shallow waters2,3. To thrive in deeper waters where light is more scarce, coral morphology4 has evolved to improve light trapping5 via multiple internal light reflections (Fig. 1b, c). We can then learn from stony-coral morphology in engineering and science where light trapping is needed, including sunlight harvesting using concentrating solar thermal (CST) systems6,7. Absorber coatings applied to solar receivers in CST plants have the function of converting concentrated sunlight in a wide-spectrum into thermal energy8 for many applications, including electric power generation (Fig. 1d) 9,10. Importantly, CST incorporates thermal energy storage, a more affordable, scalable, and durable alternative than other well-known storage technologies for long duration energy storage11. A key barrier to the wide adoption of CST, contributing to both increasing cost and reducing performance, is the poor durability of its light-absorbing coatings12. These coatings need to withstand high temperatures (> 700°C) and thousands of thermal cycles over many years of operation13. The best-known CST coatings are spinel-based coatings (Supplementary Note 1) such as Pyromark 2500® (henceforth referred to as Pyromark)14, which is widely considered the gold-standard in the CST industry. These coatings implement an organic binder15 that decomposes during a curing process to produce a nano-textured porous coating with spinel pigments, without macro-scale (> 50 µm) features. Solar-weighted absorptance, the key performance metric16, is typically reported after long-term isothermal exposure at high temperature, with the highest reported values being 94.6% after ageing for 2350 h at 850°C14, 97.2% after aging for 2,000 h at 800°C15, and 96.3% after aging for 3800 h at 770°C13. However, unstable optical performance is generally observed in CST coatings because the elevated temperatures re-arrange the material phases, alter the material composition13, and modify the nano-scale morphology via sintering and crystal grain growth17. Advanced light absorbers made of carbon nanotubes18 and graphene19 can absorb more than 99% of incoming light from every angle, but these coatings burn at the surface temperatures commonly found in conventional receivers20. Most coating research so far has focused on texturing the nano-scale morphology and improving the thermal stability of the materials13,15,21−23, while neglecting the micro- (~ 3 µm) and macro-scale (> 50 µm) geometries24 and the tuning of various length-scale morphologies in the coating to maximise light absorptance. Hierarchical structures have been shown to be a powerful tool to improve radiative cooling in clothing25, as well as mechanical rigidity and stability in sea sponges26. Here, we show that a hierarchical design with coral-inspired micro- and macro-scale features can produce high-temperature solar absorbers with enhanced light absorption and outstanding optical resilience, which we define as the capacity to retain stable optical properties despite material degradation.

Multi-Variate Analyses of Coral Mortality From the 2014–2015 Stony Coral Tissue Loss Disease Outbreak Off Miami-Dade County, Florida

Environmental compliance monitoring associated with the Port Miami dredging project (2013–2015), designed to assess the impact of project-generated sediments on the local coral community, fortuitously captured a thermal bleaching event and the first reports of an emergent, highly contagious, white-plague-like coral disease outbreak in the fall of 2014. The disease, now termed stony coral tissue loss disease (SCTLD), has decimated reefs throughout Florida and is now spreading across the Caribbean. The high prevalence of disease, the number of affected species, and the high mortality of corals affected suggests SCTLD may be the most lethal coral disease ever recorded. Previous analyses of the dredge monitoring data have reached mixed conclusions about the relative impact of dredging on coral mortality and has often parsed out disease susceptible individuals to isolate the impacts of dredging only. We use multi-variate analyses, including time-based survival analyses, to examine the timing and impacts of dredging, coral bleaching, and disease on local coral mortality. By examining the status of corals monthly from the October 2013 to July 2015 observational period, we found that coral mortality was not significantly affected by a coral’s proximity to the dredge site or sediment burial. Instead, coral mortality was most strongly impacted by disease and the emergence of SCTLD during the monitoring period. During the 2-year monitoring period, 26.3% of the monitored corals died, but the only conditions significantly affected by the dredge were partial burial and partial mortality. The strongest link to mortality was due to disease, which impacted coral species differently depending on their susceptibility to SCTLD. The focus on disturbances associated with dredging created a circumstance where the greater impacts of this emergent disease were downplayed, leading to a false narrative of the resulting mortality on the local coral communities. The results of this study reveal that while local events such as a dredging project do have quantifiable effects and can be harmful to corals, regional and global threats that result in mass coral mortality such as thermal stress and disease represent an existential threat to coral reefs and must be urgently addressed.