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Recurrent expansions of B30.2-associated immune receptor families in fish

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Abstract

B30.2 domains, also known as PRY/SPRY, are key components of specific subsets of two large families of proteins involved in innate immunity: the tripartite motif proteins (TRIMs) and the Nod-like receptors (NLRs). TRIM proteins are important, often inducible factors of antiviral innate immunity, targeting multiple steps of viral cycles through a variety of mechanisms. NLRs prime and regulate systemic innate defenses, especially against bacteria, and control inflammation. Large TRIM and NLR subsets characterized by the presence of a B30.2 domain have been reported from a few fish species including zebrafish and seem to be strongly prone to gene duplication/expansion. Here, we performed a large-scale survey of these receptors across about 150 fish genomes, focusing on ray-finned fishes. We assessed the number and genomic distribution of domains and domain combinations associated with TRIMs, NLRs, and other genes containing B30.2 domains and looked for gene expansion patterns across fish groups. We then used a model to test the impact of taxonomy, genome size, and environmental variables on the copy numbers of these genes. Our findings reveal novel domain structures, clade-specific gains and losses. They also assist with the timing of the gene expansions, reveal patterns associated with the MHC, and lay the groundwork for further studies delving deeper into the forces that drive the copy number variation of immune genes on a species level.

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Availability of data and material

A list of genome assemblies used in the study, as well as links to FishBase and NCBI, collected coordinates, and the calculated copy numbers and clustering are all available in Supplementary Table 1. Supplementary Data 1 contains plots of the likelihood distributions of the lambda parameter, which were of vital importance in determining the correct input values to use for the modeling.

Code availability

The custom scripts used for the analyses are available from Github at https://github.com/jsuurvali/B302receptors

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Acknowledgements

We would like to thank the Vertebrate Genomes Project (https://vertebrategenomesproject.org/) for the early use of a number of high quality genome assemblies, and the authors of all original studies whose data contributed to this work.

Funding

J.S. and C.J.G. were supported by the Great Lakes Fishery Commission and by a Natural Sciences and Engineering Research Council of Canada Discovery Grant to C.J.G. P.B. was supported by institutional grants from INRAE.

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Authors and Affiliations

  1. Department of Biological Sciences, University of Manitoba, 50 Sifton Rd, Winnipeg, MB, R3T 2N2, Canada

    Jaanus Suurväli & Colin J. Garroway

  2. Université Paris-Saclay, INRAE, UVSQ, Virologie et Immunologie Moléculaires, 78350, Jouy-en-Josas, France

    Pierre Boudinot

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  1. Jaanus Suurväli
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Correspondence to Pierre Boudinot.

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Suurväli, J., Garroway, C.J. & Boudinot, P. Recurrent expansions of B30.2-associated immune receptor families in fish. Immunogenetics 74, 129–147 (2022). https://doi.org/10.1007/s00251-021-01235-4

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