Award Abstract # 1942647
CAREER: Holobionts Unfiltered: integrated comparative and experimental examination of the role of cnidarian innate immunity on microbiome structure and stability

NSF Org: IOS
Division Of Integrative Organismal Systems
Recipient: UNIVERSITY OF WASHINGTON
Initial Amendment Date: January 24, 2020
Latest Amendment Date: June 14, 2024
Award Number: 1942647
Award Instrument: Continuing Grant
Program Manager: Joanna Shisler
jshisler@nsf.gov
 (703)292-5368
IOS
 Division Of Integrative Organismal Systems
BIO
 Directorate for Biological Sciences
Start Date: March 1, 2020
End Date: February 28, 2026 (Estimated)
Total Intended Award Amount: $940,496.00
Total Awarded Amount to Date: $940,496.00
Funds Obligated to Date: FY 2020 = $174,950.00
FY 2021 = $301,133.00

FY 2022 = $188,608.00

FY 2023 = $180,238.00

FY 2024 = $95,567.00
History of Investigator:
  • Jesse Zaneveld (Principal Investigator)
    zaneveld@gmail.com
Recipient Sponsored Research Office: University of Washington
4333 BROOKLYN AVE NE
SEATTLE
WA  US  98195-1016
(206)543-4043
Sponsor Congressional District: 07
Primary Place of Performance: University of Washington Bothell
18115 Campus Way NE
Bothell
WA  US  98011-8246
Primary Place of Performance
Congressional District:
01
Unique Entity Identifier (UEI): HD1WMN6945W6
Parent UEI:
NSF Program(s): Symbiosis Infection & Immunity
Primary Program Source: 01002021DB NSF RESEARCH & RELATED ACTIVIT
01002122DB NSF RESEARCH & RELATED ACTIVIT

01002223DB NSF RESEARCH & RELATED ACTIVIT

01002324DB NSF RESEARCH & RELATED ACTIVIT

01002425DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1045, 9178, 9179
Program Element Code(s): 765600
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

Tropical coral reefs are biodiversity hotspots. For many coastal communities, they are a source of income, a shield against storm damage, and a cultural icon. For more than 240 million years, the growth of stony corals engineered these ecosystems. Over that time, stony corals split into two main groups with more than 1500 species. But corals are not alone; the use of molecular tools identified symbiosis on microscopic scale. Inside each coral polyp are communities of dinoflagellates, bacteria, and archaea that are together called the coral microbiome. Coral microbiomes can help or harm stressed corals. This can affect reef decline due to coral disease and mass coral bleaching. It is thought that coral species with more innate immunity genes have less diverse microbiomes. However, this has not yet been tested. This project will test this idea using a cost-effective ?genome skimming? approach to compare coral microbes and immunity genes across 128 coral species. This comparison will suggest how different innate immunity genes shape coral microbiomes. The project will use Karenina, a new statistical method, to test ideas about how immunity changes microbiome dynamics during stress. Finally, the project will test those predictions in laboratory experiments. These research aims are paired with an education plan that will use project data in undergraduate classes, develop a new online interactive bioinformatics textbook, and produce Reef Scenarios, a learning product that will let high school and undergraduate students simulate reef ecology in engaging classroom exercises.

The ability of scleractinian (?stony?) corals to survive many ecological stressors ? from macroalgal competition to bleaching ? is thought to depend on the outcome of coral x microbe x environment interactions. Therefore, understanding how corals regulate their microbiome is important for understanding coral?s response to environmental stress. Coral innate immunity is thought to play a critical role in regulating the microbiome. Yet the relationship between coral innate immunity and microbiome richness, composition, and stability is not yet well understood. This project implements an integrated research and education plan to study how the evolution of cnidarian innate immunity has influenced microbiome structure, and how changes in the bacterial and archaeal portion of the microbiome may influence survival of thermal stress. This approach will combine a global cross-species survey relating innate immune gene repertoires in diverse coral genomes with their microbiome richness and composition and laboratory experiments in a model cnidarian that can confirm or falsify proposed immunity-microbiome interactions from the survey. A new modeling approach will be used to carefully distinguish competing time-series models of the effects of innate immunity and thermal stress on microbiome dynamics. By uniting sequencing approaches with a tractable cnidarian model system, this project will test key hypotheses in cnidarian host-microbe symbiosis, ecology and evolution. These research objectives are integrated with an education and outreach plan that includes use of project data in undergraduate classes, development of a new interactive online bioinformatics text, and production of Reef Scenarios, a classroom product for simulating reef ecology.

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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Brown, Tanya and Sonett, Dylan and Zaneveld, Jesse R. and PadillaGamiño, Jacqueline L. "Characterization of the microbiome and immune response in corals with chronic Montipora white syndrome" Molecular Ecology , v.30 , 2021 https://doi.org/10.1111/mec.15899 Citation Details
Brown, Tanya and Sonett, Dylan and Zaneveld, Jesse R. and PadillaGamiño, Jacqueline L. "Characterization of the microbiome and immune response in corals with chronic Montipora white syndrome" Molecular Ecology , v.30 , 2021 https://doi.org/10.1111/mec.15899 Citation Details
Epstein, Hannah_E and Brown, Tanya and Akinrinade, Aymikun_O and McMinds, Ryan and Pollock, F_Joseph and Sonett, Dylan and Smith, Styles and Bourne, David_G and Carpenter, Carolina_S and Knight, Rob and Willis, Bette_L and Medina, Mónica and Lamb, Joleah "Evidence for microbially-mediated tradeoffs between growth and defense throughout coral evolution" Animal Microbiome , v.7 , 2025 https://doi.org/10.1186/s42523-024-00370-z Citation Details
Medina, Mónica and Baker, David M. and Baltrus, David A. and Bennett, Gordon M. and Cardini, Ulisse and Correa, Adrienne M. and Degnan, Sandie M. and Christa, Gregor and Kim, Eunsoo and Li, Jingchun and Nash, David R. and Marzinelli, Ezequiel and Nishiguc "Grand Challenges in Coevolution" Frontiers in ecology and evolution , v.9 , 2022 https://doi.org/10.3389/fevo.2021.618251 Citation Details
Shaffer, Justin P. and Nothias, Louis-Félix and Thompson, Luke R. and Sanders, Jon G. and Salido, Rodolfo A. and Couvillion, Sneha P. and Brejnrod, Asker D. and Lejzerowicz, Franck and Haiminen, Niina and Huang, Shi and Lutz, Holly L. and Zhu, Qiyun and M "Standardized multi-omics of Earths microbiomes reveals microbial and metabolite diversity" Nature Microbiology , v.7 , 2022 https://doi.org/10.1038/s41564-022-01266-x Citation Details
Sonett, D and Brown, T and Bengtsson-Palme, J and Padilla-Gamiño, J and Zaneveld, J "The Organelle in the Room: Under-annotated Mitochondrial Reads Bias Coral Microbiome Analysis" bioRxiv , 2021 https://doi.org/10.1101/2021.02.23.431501 Citation Details
Sonett, Dylan and Brown, Tanya and Bengtsson-Palme, Johan and Padilla-Gamiño, Jacqueline_L and Zaneveld, Jesse_R "Organelles in the ointment: improved detection of cryptic mitochondrial reads resolves many unknown sequences in cross-species microbiome analyses" ISME Communications , v.4 , 2024 https://doi.org/10.1093/ismeco/ycae114 Citation Details
van Woesik, Robert and Shlesinger, Tom and Grottoli, Andréa G. and Toonen, Rob J. and Vega Thurber, Rebecca and Warner, Mark E. and Marie Hulver, Ann and Chapron, Leila and McLachlan, Rowan H. and Albright, Rebecca and Crandall, Eric and DeCarlo, Thomas M "Coralbleaching responses to climate change across biological scales" Global Change Biology , v.28 , 2022 https://doi.org/10.1111/gcb.16192 Citation Details
Vega_Thurber, Rebecca L and Silva, Denise and Speare, Lauren and Croquer, Aldo and Veglia, Alex J and Alvarez-Filip, Lorenzo and Zaneveld, Jesse R and Muller, Erinn M and Correa, Adrienne MS "Coral Disease: Direct and Indirect Agents, Mechanisms of Disease, and Innovations for Increasing Resistance and Resilience" Annual Review of Marine Science , v.17 , 2024 https://doi.org/10.1146/annurev-marine-011123-102337 Citation Details
Zaneveld, Jesse and McMinds, Ryan and Vega Thurber, Rebecca "Stress and stability: applying the Anna Karenina principle to animal microbiomes" Nature microbiology , 2017 https://doi.org/10.1038/nmicrobiol.2017.121 Citation Details

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