FWRI Scientist Publications on Stony Coral Tissue Loss Disease

*Authors in bold are FWC researchers

Authors: Erinn Muller, Constance Sartor, Nicholas Alcaraz, and Robert van Woesik

How was Stony Coral Tissue Loss Disease spread on large scales? How contagious is it? What may have influenced the spread of the outbreak? A team of researchers including one from the FWRI Information Science and Management Group wanted to answer these questions. By looking at data collected from a number of sources, including the FWC’s Coral Reef Evaluation and Monitoring Project (CREMP), researchers were able to pick out patterns from the dataset. They found that the spread of the disease was linear and moved fast – up to 300 feet a day. Because the disease spread slightly faster to the north than it did south, scientists propose that the Gulf Stream drove the spread north, and back eddies coming off the Gulf Stream helped spread the disease south. Based on the patterns of spread and how the disease clustered on nearby reefs, the disease is highly contagious. Higher diversity, deeper reefs were at greater risk of this disease than shallower, lower diversity reefs. Although the disease started during a major global bleaching event, its linear mode of movement suggests there is little seasonal influence. It also doesn’t seem to be affected by water temperature, as scientists noticed no relationship between rate of spread and temperature. This study shed light on the movement patterns of this disease, which will be important for Caribbean countries as they start responding to it.

Citation: Muller EM, Sartor C, Alcaraz NI and van Woesik R (2020) Spatial Epidemiology of the Stony-Coral-Tissue-Loss Disease in Florida. Front. Mar. Sci. 7:163. doi: 10.3389/fmars.2020.00163

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Authors: Stephanie Rosales, Abigail Clark, Lindsay Huebner, Rob Ruzicka, and Erinn Muller

In this study, scientists from the University of Miami, Mote Marine Laboratory, and the FWRI Coral Research Program wanted to learn if bacteria are playing a role in the stony coral tissue loss disease outbreak. They identified bacteria taken from samples of healthy and diseased corals, water, and sand from three different zones. These zones included where the outbreak was active, where the outbreak was past its peak, and areas where the disease had yet to arrive. They found different types of bacteria depending on the zone and coral species sampled. They also found that bacteria from the orders Rhodobacterales and Rhizobiales were always higher in abundance in diseased coral tissue in all coral species studied. These bacteria were also present in higher numbers in water and sand samples from diseased reefs. These bacteria may not be the main cause of the disease, but it is likely they are still playing a role in the disease. For example, they may be taking advantage of an already sick coral and making it worse. How exactly are the bacteria impacting the diseased corals? How are they spreading through the environment? Further research is needed to fully tease out their findings and better understand the role these bacteria have in the outbreak.

Citation: Rosales SM, Clark AS, Huebner LK, Ruzicka RR and Muller EM (2020) Rhodobacterales and Rhizobiales Are Associated With Stony Coral Tissue Loss Disease and Its Suspected Sources of Transmission. Front. Microbiol. 11:681. doi: 10.3389/fmicb.2020.00681

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Authors: Bill Sharp, Colin Shea, Kerry Maxwell, Erinn Muller, and John Hunt

How does stony coral tissue loss disease move across a reef? The FWRI Restoration Ecology team based out of Marathon’s South Florida Regional Lab set out to answer this question by watching how the disease moved across four reef sites in the Middle Florida Keys. SCTLD first hit the study reefs in February 2018 and moved from east to west. The disease appears to be spread mainly by water movement – how close corals were to each other had no impact on the spread. However, the size of the coral did, as larger corals were more likely to become infected. Corals in the Families Meandrinidae (including maze and flower corals) and Faviidae (including brain corals) fared the worst, with half of the colonies of these species dying. Inshore sites fared better than offshore sites, with a smaller loss of living coral tissue and slower rate of disease spread. These findings indicate that corals at inshore reefs may have some natural resilience to the disease – of great interest to those working to combat the effects of this disease.

Citation: Sharp WC, CP Shea, KE Maxwell, EM Muller, and JH Hunt. 2020. Evaluating the small-scale epidemiology of the stony-coral -tissue-loss disease in the middle Florida Keys. PLoS ONE 15(11): e0241871.

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Authors: Jan Landsberg, Yasunari Kiryu, Esther Peters, Patrick Wilson, Noretta Perry, Yvonne Waters, Kerry Maxwell, Lindsay Huebner, and Thierry Work

What does stony coral tissue loss disease look like on a cellular level? What can this tell us about the cause of the disease? The FWRI Fish and Wildlife Health team teamed up with scientists from the Coral Research Program and Restoration Ecology Team to answer these questions. By looking at coral tissue through microscopes, researchers found that the disease appears to affect the coral’s relationship with its zooxanthellae – the tiny beneficial algae that lives inside coral. The coral provides zooxanthellae with a safe place to live, and the zooxanthellae shares the “food” it creates from photosynthesis. The disease first appears deep inside the coral, close to the skeleton. This is where most of the corals’ zooxanthellae are found. The zooxanthellae start to die, along with coral cells. These changes make their way through the coral tissue, until it can be seen as living tissue sloughing off the coral skeleton. Even in some corals showing no outward signs of the disease at reefs having an outbreak, the scientists found microscopic evidence of the disease. The cause of the disease remains a mystery for now - no obvious causes, such as bacteria, were found within the diseased tissue. Regardless of cause, reducing sources of stress, like pollution, will help corals resist disease.

Citation: Landsberg JH, Kiryu Y, Peters EC, Wilson PW, Perry N, Waters Y, Maxwell KE, Huebner LK and Work TM (2020) Stony Coral Tissue Loss Disease in Florida Is Associated With Disruption of Host–Zooxanthellae Physiology. Front. Mar. Sci. 7:576013. doi: 10.3389/fmars.2020.576013

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Authors: Abigail S. Clark, Sara D. Williams, Kerry Maxwell, Stephanie M. Rosales, Lindsay K. Huebner, Jan H. Landsberg, John H. Hunt, and Erinn M. Muller

Stony coral tissue loss disease (SCTLD) is an emergent and often lethal coral disease that was first reported near Miami, FL (USA) in 2014. Our objective was to determine if coral colonies showing signs of SCTLD possess a specific microbial signature across five susceptible species sampled in Florida’s Coral Reef. Three sample types were collected: lesion tissue and apparently unaffected tissue of diseased colonies, and tissue of apparently healthy colonies. Using 16S rRNA high-throughput gene sequencing, our results show that, for every species, the microbial community composition of lesion tissue was significantly different from healthy colony tissue and from the unaffected tissue of diseased colonies. The lesion tissue of all but one species (Siderastrea siderea) had higher relative abundances of the order Rhodobacterales compared with other types of tissue samples, which may partly explain why S. siderea lesions often differed in appearance compared to other species. The order Clostridiales was also present at relatively high abundances in the lesion tissue of three species compared to healthy and unaffected tissues. Stress often leads to the dysbiosis of coral microbiomes and increases the abundance of opportunistic pathogens. The present study suggests that Rhodobacterales and Clostridiales likely play an important role in SCTLD.

Citation: Clark AS, Williams SD, Maxwell K, Rosales SM, Huebner LK, Landsberg JH, Hunt JH, Muller EM. Characterization of the Microbiome of Corals with Stony Coral Tissue Loss Disease along Florida’s Coral Reef. Microorganisms. 2021; 9(11):2181. https://doi.org/10.3390/microorganisms9112181

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Authors: Stephanie M. Rosales, Lindsay K. Huebner, Abigail S. Clark, Ryan McMinds, Rob R. Ruzicka, and Erinn M. Muller.

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.

Citation: Rosales SM, Huebner LK, Clark AS, McMinds R, Ruzicka RR, Muller EM. Bacterial metabolic potential and micro-eukaryotes enriched in stony coral tissue loss disease lesions. Front Mar Sci. 2022;8:776859. https://doi.org​/10.3389/fmars.​2021.776859.

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Authors: Stephanie M Rosales, Lindsay K Huebner, James S Evans, Amy Apprill, Andrew C Baker, Cynthia C Becker, Anthony J Bellantuono, Marilyn E Brandt, Abigail S Clark, Javier del Campo, Caroline E Dennison, Katherine R Eaton, Naomi E Huntley, Christina A Kellogg, Mónica Medina, Julie L Meyer, Erinn M Muller, Mauricio Rodriguez-Lanetty, Jennifer L Salerno, William B Schill, Erin N Shilling, Julia Marie Stewart, Joshua D Voss

Stony coral tissue loss disease (SCTLD) has been causing significant whole colony mortality on reefs in Florida and the Caribbean. The cause of SCTLD remains unknown, with the limited concurrence of SCTLD-associated bacteria among studies. We conducted a meta-analysis of 16S ribosomal RNA gene datasets generated by 16 field and laboratory SCTLD studies to find consistent bacteria associated with SCTLD across disease zones (vulnerable, endemic, and epidemic), coral species, coral compartments (mucus, tissue, and skeleton), and colony health states (apparently healthy colony tissue (AH), and unaffected (DU) and lesion (DL) tissue from diseased colonies). We also evaluated bacteria in seawater and sediment, which may be sources of SCTLD transmission. Although AH colonies in endemic and epidemic zones harbor bacteria associated with SCTLD lesions, and aquaria and field samples had distinct microbial compositions, there were still clear differences in the microbial composition among AH, DU, and DL in the combined dataset. Alpha-diversity between AH and DL was not different; however, DU showed increased alpha-diversity compared to AH, indicating that, prior to lesion formation, corals may undergo a disturbance to the microbiome. This disturbance may be driven by Flavobacteriales, which were especially enriched in DU. In DL, Rhodobacterales and Peptostreptococcales–Tissierellales were prominent in structuring microbial interactions. We also predict an enrichment of an alpha-toxin in DL samples which is typically found in Clostridia. We provide a consensus of SCTLD-associated bacteria prior to and during lesion formation and identify how these taxa vary across studies, coral species, coral compartments, seawater, and sediment.

Citation: Rosales SM, Huebner LK, Evans JS, Apprill A, Baker AC, Becker CC, et al. 2023. A meta-analysis of the stony coral tissue loss disease microbiome finds key bacteria in unaffected and lesion tissue in diseased colonies. ISME Commun. 3(1):19. 

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Authors: Jakob M Heinz, Jennifer Lu, Lindsay K Huebner, Steven L Salzberg, Markus Sommer, Stephanie M Rosales

Stony coral tissue loss disease (SCTLD) has devastated coral reefs off the coast of Florida and continues to spread throughout the Caribbean. Although a number of bacterial taxa have consistently been associated with SCTLD, no pathogen has been definitively implicated in the etiology of SCTLD. Previous studies have predominantly focused on the prokaryotic community through 16S rRNA sequencing of healthy and affected tissues. Here, we provide a different analytical approach by applying a bioinformatics pipeline to publicly available metagenomic sequencing samples of SCTLD lesions and healthy tissues from four stony coral species. To compensate for the lack of coral reference genomes, we used data from apparently healthy coral samples to approximate a host genome and healthy microbiome reference. These reads were then used as a reference to which we matched and removed reads from diseased lesion tissue samples, and the remaining reads associated only with disease lesions were taxonomically classified at the DNA and protein levels. For DNA classifications, we used a pathogen identification protocol originally designed to identify pathogens in human tissue samples, and for protein classifications, we used a fast protein sequence aligner. To assess the utility of our pipeline, a species-level analysis of a candidate genus, Vibrio, was used to demonstrate the pipeline's effectiveness. Our approach revealed both complementary and unique coral microbiome members compared to a prior metagenome analysis of the same dataset.

Citation: Jakob M Heinz, Jennifer Lu, Lindsay K Huebner, Steven L Salzberg, Markus Sommer, Stephanie M Rosales. Novel metagenomics analysis of stony coral tissue loss disease, G3 Genes|Genomes|Genetics, 2024;, jkae137, https://doi.org/10.1093/g3journal/jkae137

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