Award Abstract # 1928771
RAPID: Collaborative Research: Predicting the Spread of Multi-Species Coral Disease Using Species Immune Traits

NSF Org: OCE
Division Of Ocean Sciences
Recipient: UNIVERSITY OF TEXAS AT ARLINGTON
Initial Amendment Date: April 25, 2019
Latest Amendment Date: April 25, 2019
Award Number: 1928771
Award Instrument: Standard Grant
Program Manager: Daniel J. Thornhill
OCE
 Division Of Ocean Sciences
GEO
 Directorate for Geosciences
Start Date: May 1, 2019
End Date: April 30, 2022 (Estimated)
Total Intended Award Amount: $53,486.00
Total Awarded Amount to Date: $53,486.00
Funds Obligated to Date: FY 2019 = $53,486.00
History of Investigator:
  • Laura Mydlarz (Principal Investigator)
    mydlarz@uta.edu
Recipient Sponsored Research Office: University of Texas at Arlington
701 S NEDDERMAN DR
ARLINGTON
TX  US  76019-9800
(817)272-2105
Sponsor Congressional District: 25
Primary Place of Performance: University of Texas at Arlington
Dept of Biology, 337 Life Scienc
Arlington
TX  US  76019-0498
Primary Place of Performance
Congressional District:
25
Unique Entity Identifier (UEI): LMLUKUPJJ9N3
Parent UEI:
NSF Program(s): BIOLOGICAL OCEANOGRAPHY
Primary Program Source: 01001920DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1097, 7242, 7914, 8556, 8811, 9117, 9150
Program Element Code(s): 165000
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.050

ABSTRACT

Title: Predicting the Spread of Multi-Species Coral Disease Using Species Immune Traits

Coral reef ecosystems provide substantial economic resources to the societies of the United States Virgin Islands (USVI) and other US locations in the forms of tourism, fishing and coastal protection. However, reefs are among the most threatened marine environments, and coral disease is having a devastating impact on these valued systems. In early 2019, a multi-species rapid tissue loss disease matching the description of stony coral tissue loss disease (SCTLD) was found severely affecting a reef off the southwest coast of St. Thomas in the US Virgin Islands (USVI). SCTLD has been devastating coral reef communities in southeast Florida for the last four years, and was very recently reported from disparate areas around the Caribbean, including Mexico, Jamaica, and St. Martin. Rapid surveys by the investigators at the University of the Virgin Islands believe that a 50 km2 area southwest of St. Thomas is the initial incidence area of the disease, but will likely spread across the USVI, British Virgin Islands, and Puerto Rico. This study performs experiments to understand how this disease affects coral species immune traits and compares the microbiology and physiology of disease samples in the USVI to samples from Florida. It also examines how changing the species composition of a coral community affects the spread and impact of the disease. The overall aim is to produce a model to predict the impact of multi-species disease spread on reefs based on coral species assemblages. The project contributes to the research training of at least 2 undergraduates, 2 M.S. students, and 3 Ph.D. students, who benefit from cross-investigator mentoring. The research team includes representatives to the Coral Disease Advisory Committees for the USVI and Florida, which ensures rapid communication of findings to management bodies in both regions.

Coral disease is a significant and increasing threat to Caribbean coral reef systems. Recent results demonstrate that coral species immune traits can predict disease resistance, and thus, forecast impacts to coral community structure, under multi-species coral disease. The onset of this epizootic in the USVI offers an unprecedented opportunity to test hypotheses about the impact of coral resistance, tolerance and immune traits on disease spread during the early stages of an outbreak that could profoundly change the diversity of Caribbean reefs. It is hypothesized that the abundance of highly susceptible species dictates 1) the onset of disease at reef sites downstream of the initial incidence area, and 2) the spread of disease within reef sites. Furthermore, 3) downstream reef sites where highly susceptible species are removed or treated show lower immune responses in all susceptible corals, later onset of disease, and slower within-site disease spread. To test these hypotheses, two experiments directly compare species responses to disease exposure and test the effect of species assemblage on coral immune function and disease spread. Results from these experiments aim to inform a generalizable model to predict the impact of multi-species disease spread on reefs based on coral species assemblages. Results of this project include direct comparison of the USVI disease to Florida SCTLD and a better understanding of how the abundance of highly susceptible host species impacts the spread of disease during the early onset of a multi-species panzootic.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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Beavers, Kelsey M. and Van Buren, Emily W. and Rossin, Ashley M. and Emery, Madison A. and Veglia, Alex J. and Karrick, Carly E. and MacKnight, Nicholas J. and Dimos, Bradford A. and Meiling, Sonora S. and Smith, Tyler B. and Apprill, Amy and Muller, Erin "Stony coral tissue loss disease induces transcriptional signatures of in situ degradation of dysfunctional Symbiodiniaceae" Nature Communications , v.14 , 2023 https://doi.org/10.1038/s41467-023-38612-4 Citation Details
Huntley, Naomi and Brandt, Marilyn E. and Becker, Cynthia C. and Miller, Carolyn A. and Meiling, Sonora S. and Correa, Adrienne M. S. and Holstein, Daniel M. and Muller, Erinn M. and Mydlarz, Laura D. and Smith, Tyler B. and Apprill, Amy "Experimental transmission of Stony Coral Tissue Loss Disease results in differential microbial responses within coral mucus and tissue" ISME Communications , v.2 , 2022 https://doi.org/10.1038/s43705-022-00126-3 Citation Details
Meiling, Sonora S. and Muller, Erinn M. and Lasseigne, Danielle and Rossin, Ashley and Veglia, Alex J. and MacKnight, Nicholas and Dimos, Bradford and Huntley, Naomi and Correa, Adrienne M. and Smith, Tyler Burton and Holstein, Daniel M. and Mydlarz, Laur "Variable Species Responses to Experimental Stony Coral Tissue Loss Disease (SCTLD) Exposure" Frontiers in Marine Science , v.8 , 2021 https://doi.org/10.3389/fmars.2021.670829 Citation Details
Vega Thurber, Rebecca and Mydlarz, Laura D. and Brandt, Marilyn and Harvell, Drew and Weil, Ernesto and Raymundo, Laurie and Willis, Bette L. and Langevin, Stan and Tracy, Allison M. and Littman, Raechel and Kemp, Keri M. and Dawkins, Phoebe and Prager, K "Deciphering Coral Disease Dynamics: Integrating Host, Microbiome, and the Changing Environment" Frontiers in Ecology and Evolution , v.8 , 2020 https://doi.org/10.3389/fevo.2020.575927 Citation Details
Veglia, A. J. and Beavers, K. and Van Buren, E. W. and Meiling, S. S. and Muller, E. M. and Smith, T. B. and Holstein, D. M. and Apprill, A. and Brandt, M. E. and Mydlarz, L. D. and Correa, A. M. "Alphaflexivirus Genomes in Stony Coral Tissue Loss Disease-Affected, Disease-Exposed, and Disease-Unexposed Coral Colonies in the U.S. Virgin Islands" Microbiology Resource Announcements , v.11 , 2022 https://doi.org/10.1128/mra.01199-21 Citation Details

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

Intellectual Merit

Coral diseases have increased significantly throughout the past 30 years. Unhealthy coral reefs cannot support fish and other life that make the reef a vibrant and diverse ecosystem. Coral reefs in the Caribbean have experienced population collapses due to outbreaks of disease. One disease in particular, Stoney Coral Tissue Loss Disease is a new fast spreading and lethal disease first reported in Florida in 2014. SCTLD affects over 30 species of corals including the iconic brain and pillar corals. Since its discovery in Florida, the disease has spread to Caribbean and was first detected in US Virgin Islands in 2019.

In this study we conducted experiments to understand how this disease affects immune traits and immune responses of five coral species. It also examines how changing the species composition of a coral community affects the spread and impact of the disease. We therefore quantified coral susceptibility to disease and examined coral immune mechanisms that may drive disease outcomes.  In response to exposure to Stoney Coral Tissue Loss Disease the five species of corals had one of two treatment outcomes, exposed to disease and not infected or infected with a visible lesion, leading to a gradient of susceptible, moderately susceptible, and tolerant. We leveraged this range of coral responses to SCTLD exposure to determine the patterns of gene expression associated with SCTLD resistance or susceptibility. The gene expression profiles of coral hosts and their endosymbionts were examined independently by bioinformatically separating the RNA-seq reads prior to analyses.

We show that SCTLD exposure induces significant transcriptional changes in both the coral animal and their algal symbionts, altering normal host-symbiont interactions. We identify orthologous coral genes exhibiting lineage-specific differences in constitutive expression that correlate to disease susceptibility, as well as those that are significantly differentially expressed in all coral species in response to SCTLD infection. We have several significant findings:  First, we find that SCTLD infection induces genes involved in antiviral immunity, symbiont maintenance, starvation, and apoptosis in all five coral species. Second, species-specific differences in SCTLD susceptibility involve increased vesicular trafficking and decreased signal transduction. Third, the intracellular algal symbiont, rather than the coral animal, are the first to exhibit gene expression shifts in response to SCTLD exposure.

Taken together our data show that SCTLD disrupts normal host-symbiont interactions, leading to starvation of the coral host and subsequent in situ degradation of intracellular Symbiodiniaceae.  We find that SCTLD-exposure induces initial shifts in endosymbiont gene expression, followed by expression of coral genes involved in immunity, starvation, and apoptosis. Overall, our results indicate that SCTLD infection induces in situ degradation of dysfunctional endosymbionts across species and that the severity of disease is strongly influenced by the identity of the symbiont genera within the coral. 

Broader Impacts

This project supported students at University of Texas, Arlington (Hispanic-serving Institution). Over the funding period, 2 graduate students were directly funded and trained on the award, another 2 benefited indirectly from assisting with field work, and spin-off projects resulting from the large amount of data collected from this award. This award also supported the training in marketable skills such as RNA and DNA extractions, bioinformatic tools and statistical modelling, of 2 undergraduate students who were mentored by graduate students in the lab.

Public outreach was limited due to COVID shutdowns, but we were able to host one booth in April 2022 at the large EarthX expo in Dallas. All Mydlarz lab students all took part in developing activities and interacting with the public at these events, where we estimate engagement with about 1800 people. PI Mydlarz also led several workshops targeting women in science and the concept of sponsorship vs mentorship.  

To date this award has led to the publication of 5 papers, with one manuscript currently in review and multiple others in a stage of writing and/or development. There were approximately fifteen presentations by graduate and undergraduate students at various conferences. PI Mydlarz co-led a special issue of Frontiers of Immunology, a session at the 14th International Coral Reef Symposium all related to the topic and data from this award.

 


Last Modified: 09/12/2022
Modified by: Laura D Mydlarz

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