Anatomically-specific coupling between innate immune gene repertoire and microbiome structure during coral evolution

Abstract
Tropical reef-building corals exist in intimate symbiosis with diverse microbes and viruses. Coral microbiomes are generally much less diverse than their environment, but across studied corals, the biodiversity of these microbiomes varies greatly. It has previously been hypothesized that differences in coral innate immunity in general, and the copy number of TIR-domain containing innate immune genes in particular, may drive interspecific differences in microbiome structure. Despite many existing studies of coral microbiomes, this hypothesis has previously been difficult to test due to a lack of consistently collected cross-species data on coral microbiomes. In this manuscript, we reannotate TIR-domain containing genes across diverse coral genomes, and use phylogenetic comparative methods to compare these innate immune gene copy numbers against 16S rRNA marker gene data on coral mucus, tissue, and skeleton microbiomes from the Global Coral Microbiome Project (GCMP). The copy number of Toll-like receptor (TLRs) and Interleukin-1 receptor (IL-1Rs) gene families, as well as the total genomic count of their constituent domains (LRR and TIR domains; and Ig and TIR domains, respectively), explained most interspecific differences in microbiome richness and beta-diversity among corals with sequenced genomes. We find that these correlations are also anatomically specific, with an especially strong correlation between IL-1R gene copy numbers and microbiome richness in the coral’s endolithic skeleton. Together, these results suggest innate immunity may play a key role in sculpting microbiome structure in corals.

Citation
Brown, T., Sonett, D., McMinds, R., Pollock, F. J., Medina, M., & Zaneveld, J. R. (2023). Anatomically-specific coupling between innate immune gene repertoire and microbiome structure during coral evolution. https://doi.org/10.1101/2023.04.26.538298

Acknowledgements
The authors would like to acknowledge many contributors for their field assistance during past collections of Global Coral Microbiome Project data reanalyzed in this manuscript, including: Rebecca Vega Thurber, a leader of the original GCMP project; Tasman Douglass, Margaux Hein, Frazer McGregor, Kathy Morrow, Katia Nicolet, Cathie Page, and Gergely Torda for their field assistance in Australia; Valeria Pizarro, Mateo López-Victoria, Styles Smith, Alaina Weinheimer, Claudia Tatiana Galindo for Assistance in Colombia; Chris Voolstra, Maren Ziegler, Anna Roik, and many others at KAUST for field assistance in Saudi Arabia; Mark Vermeij, Kristen Marhaver, Pedro Frade, Ben Mueller, and others at CARMABI for field assistance during sampling in Curaçao; Danwei Huang for field assistance in Singapore; Ruth Gates, Katie Barrott, Courtney Couch, Keoki Stender for field assistance in Hawai’i; Le Club de Plongee Suwan Macha and Jean-Pascal Quod for field assistance, and Amelia Foster and Jerome Payet for sampling in Isle de la Réunion; the Burkepile lab for field assistance in Mo’orea; Yossi Loya, Raz Tamir for sampling assistance in Israel; and Lyndsy Gazda, Jamie Lee Proffitt, Gabriele Swain, and Alaina Weinheimer for their assistance in the laboratory. The authors also acknowledge the staff of the Coral Bay Research Station, Lizard Island Research Station, Lord Howe Island Marine Park, Lord Howe Island Research Station, and RV Cape Ferguson for their logistical support. This work was supported by a The GCMP dataset was supported by a National Science Foundation Dimensions of Biodiversity grant (#1442306) to Rebecca Vega Thurber and MM, with sequencing provided by an in-kind UC San Diego Seed Grant in Microbiome Science grant to JZ. Analysis in this manuscript was supported by NSF IoS CAREER grant (# 559 1942647) and an in-kind UC San Diego Seed Grant in Microbiome Science grant to JZ. 560 GCMP data collection was supported by a National Science Foundation Dimensions of Biodiversity grant (#1442306) to M.M.

Publisher
Cold Spring Harbor Laboratory

DOI
10.1101/2023.04.26.538298

Additional Links
http://biorxiv.org/lookup/doi/10.1101/2023.04.26.538298

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