Large-scale genome sampling reveals unique immunity and metabolic adaptations in bats
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Comprising more than 1,400 species, bats possess adaptations unique among mammals including powered flight, unexpected longevity, and extraordinary immunity. Some of the molecular mechanisms underlying these unique adaptations includes DNA repair, metabolism and immunity. However, analyses have been limited to a few divergent lineages, reducing the scope of inferences on gene family evolution across the Order Chiroptera. We conducted an exhaustive comparative genomic study of 37 bat species, one generated in this study, encompassing a large number of lineages, with a particular emphasis on multi-gene family evolution across immune and metabolic genes. In agreement with previous analyses, we found lineage-specific expansions of the APOBEC3 and MHC-I gene families, and loss of the proinflammatory PYHIN gene family. We inferred more than 1,000 gene losses unique to bats, including genes involved in the regulation of inflammasome pathways such as epithelial defence receptors, the natural killer gene complex and the interferon-gamma induced pathway. Gene set enrichment analyses revealed genes lost in bats are involved in defence response against pathogen-associated molecular patterns and damage-associated molecular patterns. Gene family evolution and selection analyses indicate bats have evolved fundamental functional differences compared to other mammals in both innate and adaptive immune system, with the potential to enhance antiviral immune response while dampening inflammatory signalling. In addition, metabolic genes have experienced repeated expansions related to convergent shifts to plant-based diets. Our analyses support the hypothesis that, in tandem with flight, ancestral bats had evolved a unique set of immune adaptations whose functional implications remain to be explored.
Moreno Santillán , D D , Lama , T M , Gutierrez Guerrero , Y T , Brown , A M , Donat , P , Zhao , H , Rossiter , S J , Yohe , L R , Potter , J H , Teeling , E C , Vernes , S C , Davies , K T J , Myers , E , Hughes , G M , Huang , Z , Hoffmann , F , Corthals , A P , Ray , D A & Dávalos , L M 2021 , ' Large-scale genome sampling reveals unique immunity and metabolic adaptations in bats ' , Molecular Ecology , vol. Early View . https://doi.org/10.1111/mec.16027
Copyright © 2021 John Wiley & Sons Ltd. This work has been made available online in accordance with publisher policies or with permission. Permission for further reuse of this content should be sought from the publisher or the rights holder. This is the author created accepted manuscript following peer review and may differ slightly from the final published version. The final published version of this work is available at https://doi.org/10.1111/mec.16027.
DescriptionSCV was supported by a Max Planck Research Group awarded by the Max Planck Gesellschaft, a Human Frontiers Science Program Grant (RGP0058/2016) and a UKRI Future Leaders Fellowship (MR/T021985/1).
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