Characterization of the Microbiome of Corals with Stony Coral Tissue Loss Disease along Florida’s Coral Reef

Clark, Abigail S.; Sd, Williams; Maxwell, Kerry; Rosales, Stephanie M.; Huebner, Lindsay K.; Landsberg, Jan H.; Hunt, John; Muller, Erinn M.

doi:10.3390/microorganisms9112181

Cited by 25 publications

(42 citation statements)

References 69 publications

(97 reference statements)

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“…However, in the past, it has been difficult to identify pathogenic agents of coral diseases (Vega Thurber et al, 2020); of the ∼18 coral diseases described, Koch's Postulates have been fulfilled for only six (Bourne et al, 2009). Researchers have mainly focused on identifying bacteria associated with SCTLD using 16S rRNA high-throughput sequencing (Meyer et al, 2019;Iwanowicz et al, 2020;Rosales et al, 2020;Becker et al, 2021;Clark et al, 2021;Thome et al, 2021) and culturing techniques (Ushijima et al, 2020). However, these methodologies have not provided definitive evidence that SCTLD is indeed caused by bacteria.…”

Section: Introductionmentioning

confidence: 99%

“…Bacterial taxa such as Rhodobacterales, Rhizobiales, Clostridiales, Alteromonadales, and Vibrionales are described in multiple SCTLD studies, but these taxa are not consistently found throughout all samples (Meyer et al, 2019;Iwanowicz et al, 2020;Rosales et al, 2020;Becker et al, 2021;Clark et al, 2021;Thome et al, 2021). In addition, these bacterial taxa are not unique to SCTLD, as many have been identified in other coral diseases, such as black band disease (BBD; Miller and Richardson, 2011), white-plague (Sunagawa et al, 2009), and rapid tissue loss (Rosales et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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

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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.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2022

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“…There was no clear transition from AH to DU to DL in alpha diversity, and AH and DL alpha diversity values were similar. It may be difficult to capture a general microbial alpha diversity response to SCTLD across coral species, as alpha diversity values are highly species-specific [28]. However, there were differences in microbial composition between AH and DL.…”

Section: Discussionmentioning

confidence: 99%

“…The most well-studied SCTLD microbial group is the bacterial community, examined using small subunit (SSU)16S rRNA gene analysis [11,12,15,16,23,[25][26][27][28][29]. It is likely that the bacterial community is important for SCTLD progression, since there is a shift in bacterial composition from healthy corals to diseased corals, and SCTLD lesion progression can be mitigated using antibiotics [22,30,31].…”

Section: Introductionmentioning

confidence: 99%

A meta-analysis of the stony coral tissue loss disease microbiome finds key bacteria in lesions and unaffected tissue of diseased colonies

Rosales

Huebner

Evans

et al. 2022

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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 limited concurrence of SCTLD-associated bacteria among studies. We conducted a meta-analysis of SSU 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 disease 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. While Rhodobacterales and Peptostreptococcales-Tissierellales were prominent in structuring microbial interactions in DL. Peptostreptococcales-Tissierellales specifically may contribute to lesion progression through an alpha-toxin. We provide a consensus of SCTLD-associated bacteria both prior to and during lesion progression and identify how these taxa vary across studies, coral species, coral compartments, seawater, and sediment.

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“…It is an AZA-accredited (Association of Zoos and Aquariums) institution and is home to one of the world's most comprehensive, science-based coral reef restoration programs. This program has the ability to carry out every aspect of coral restoration, in-house, and integrates coral reef scientists and experts from a diversity of disciplines to conduct research on -or apply interventions related to-asexual coral propagation (Schopmeyer et al, 2012;Forsman et al, 2015;Page, 2015;Schopmeyer et al, 2017;Page et al, 2018;Koch et al, 2021b;Merck et al, 2022), sexual coral propagation (Koch, 2021a), disease (Klinges et al, 2020;Clark et al, 2021;Williams et al, 2021), ocean acidification (Hall et al, 2015;Page et al, 2021), thermotolerance, symbiosis (e.g., (Klepac et al, 2015)), resilience screening (Muller et al, 2018), outplanting, coral reef monitoring, gene banking, land and field nursery management (Merck et al, 2022), and the culture/distribution of benthic invertebrate grazers across the reef tract (e.g., (Spadaro and Butler, 2021)).…”

Section: Introductionmentioning

confidence: 99%

No apparent cost of disease resistance on reproductive output in Acropora cervicornis genets used for active coral reef restoration in Florida

et al. 2022

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As assisted sexual reproduction interventions continue to become embedded within coral reef restoration initiatives, it is important to understand the potential for trade-offs between key traits like reproductive output and disease resistance. Oocyte size and fecundity, quantitative measures of reproductive output and important life-history traits, can be used as proxies for coral reproductive success and health. Sexual reproduction, particularly gametogenesis, is an energetically costly process and at the physiological level, trade-offs are caused by competitive allocation of limited resources to various functions. However, resource allocation trade-offs may also have a genetic basis, and thus, different genets may differ in these aspects. Therefore, the purpose of this study was to assess the reproductive output of A. cervicornis genets with known white-band disease resistance or susceptibility by quantifying the number and size of oocytes within colonies maintained within Mote Marine Laboratory’s offshore coral spawning nursery in the Lower Florida Keys, USA. We also quantified the number of eggs and sperm packaged within gamete bundles that were collected during the August 2020 spawning event. Consistent with previous studies, we found a positive correlation between colony size and fecundity. Interestingly though, we found no evidence for a trade-off between disease resistance and reproductive output and instead found a negative correlation between disease susceptibility and oocyte size. These data are relevant for population management interventions and for managing broodstock used for active restoration where a suite of corals with different genotypes and phenotypes are continuously propagated and outplanted. Having a more comprehensive understanding of the fitness differences among candidates can help guide such efforts and ensure that a diversity of fit genets is used for restoration, which should ultimately support greater adaptive potential and population resilience.

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Characterization of the Microbiome of Corals with Stony Coral Tissue Loss Disease along Florida’s Coral Reef

Cited by 25 publications

References 69 publications

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

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

A meta-analysis of the stony coral tissue loss disease microbiome finds key bacteria in lesions and unaffected tissue of diseased colonies

No apparent cost of disease resistance on reproductive output in Acropora cervicornis genets used for active coral reef restoration in Florida

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