Bat genomes illuminate adaptations to viral tolerance and disease resistance
Open accessPublished version of a preprint
Abstract
Abstract Bats carry viruses that can cause severe disease in other mammals. Asymptomatic infections in bats suggest limited tissue-damaging inflammation and immunopathology. To investigate the genomic basis of disease resistance, the Bat1K project generated reference-quality genomes of ten bat species. A systematic analysis showed that signatures of selection in immune genes are more prevalent in bats compared with other mammals. We found an excess of immune gene adaptations in the ancestral Chiroptera and many descending bat lineages, highlighting viral entry and detection factors, and regulators of antiviral and inflammatory responses. ISG15, an antiviral gene contributing to hyperinflammation during COVID-19, exhibits a deletion of a cysteine, required for homodimer formation, in rhinolophid and hipposiderid bats. Cellular infection experiments showed enhanced intracellular protein conjugation of bat ISG15 and lack of secretion into extracellular space, where human ISG15 stimulates inflammation. Our work highlights molecular mechanisms contributing to viral tolerance and disease resistance in bats.
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References 222 · Cited by 78
- Authors
- Morales, A. E., Dong, Y., Brown, T., Baid, K., Kontopoulos, D. G., Gonzalez, V., Huang, Z., Ahmed, A.-W., Bhuinya, A., Hilgers, L., Winkler, S., Hughes, G., Li, X., Lu, P., Yang, Y., Kirilenko, B. M., Devanna, P., Lama, T. M., Nissan, Y., Pippel, M., Dávalos, L. M., Vernes, S. C., Puechmaille, S. J., Rossiter, S. J., Yovel, Y., Prescott, J. B., Kurth, A., Ray, D. A., Lim, B. K., Myers, E., Teeling, E. C., Banerjee, A., Irving, A. T., & Hiller, M.
- Affiliations
- Goethe University Frankfurt (DE)
- Zhejiang University-University of Edinburgh Institute (CN)
- University of Saskatchewan (CA)
- University College Dublin (IE)
- Max Planck Institute of Molecular Cell Biology and Genetics (DE)
- Max Planck Institute for Psycholinguistics (NL)
- Smith College (US)
- Tel Aviv University (IL)
- Stony Brook University (US)
- University of St Andrews (GB)
- Queen Mary University of London (GB)
- Robert Koch Institute (DE)
- Texas Tech University (US)
- Royal Ontario Museum (CA)
- University of British Columbia (CA)
- Second Affiliated Hospital of Zhejiang University (CN)
- Corresponding author
- Irving, Aaron T.
- Hiller, Michael
- ORCID
- Morales, Ariadna E.
- Dong, Yue
- Brown, Thomas
- Baid, Kaushal
- Kontopoulos, Dimitrios - Georgios
- Gonzalez, Victoria
- Huang, Zixia
- Ahmed, Alexis-Walid
- Bhuinya, Arkadeb
- Hilgers, Leon
- Winkler, Sylke
- Hughes, Graham
- Li, Xiaomeng
- Lu, Ping
- Yang, Yixin
- Kirilenko, Bogdan M.
- Devanna, Paolo
- Lama, Tanya M.
- Nissan, Yomiran
- Pippel, Martin
- Dávalos, Liliana M.
- Vernes, Sonja C.
- Rossiter, Stephen J.
- Yovel, Yossi
- Prescott, Joseph B.
- Kurth, Andreas
- Ray, David A.
- Lim, Burton K.
- Myers, Eugene
- Teeling, Emma C.
- Banerjee, Arinjay
- Irving, Aaron T.
- Hiller, Michael
- Venue
- Nature
- Published
- 2025-01-29
- Volume
- 638
- Issue
- 8050
- Pages
- 449-458
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC11821529
- OpenAlex
- W4406956854
- Cited by
- 78
- References
- 222
- Citations by year
- 2026: 36 · 2025: 34 · 2024: 3 · 2023: 5
- FWCI
- 65.99
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Nature (publishedVersion, cc-by)
- Research Square (acceptedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- St Andrews Research Repository (St Andrews Research Repository) (acceptedVersion)
- HARVEST (University of Saskatchewan) (submittedVersion, cc-by)
- Smith ScholarWorks (Smith College) (submittedVersion)
- HAL (submittedVersion, cc-by-nc-nd)
- RePEc: Research Papers in Economics (submittedVersion)
- Queen Mary Research Online (Queen Mary University of London) (submittedVersion, cc-by-nc-nd)
- Funders
- National Science Foundation (2010853, 2031906, 1838273, 2032063, 0344430)
- UK Research and Innovation (MR/T021985/1)
- Innovation Saskatchewan
- Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology
- Science Foundation Ireland (19/FFP/6790)
- Deutsche Forschungsgemeinschaft (INST 269/768-1)
- Irish Research Council (IRCLA/2017/58)
- Technische Universität Dresden
- Hessisches Ministerium für Wissenschaft und Kunst (519/03/03.001—)
- Max-Planck-Gesellschaft
- Institut Universitaire de France
- Zhejiang University
- Robert Koch Institut
- Canadian Institutes of Health Research (192089_1, 183995_1)
- Natural Sciences and Engineering Research Council of Canada (569587-2022, rgpin-2022-03010)
- H2020 European Research Council (101001702)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Bat Biology and Ecology Studies
- Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- bats, zoonotic viruses, disease resistance, virus tolerance, ISG15, antiviral proteins, protein conjugation, SARS-CoV-2, hyperinflammation, COVID-19 pandemic, viral reservoir
- MeSH terms
- COVID-19, SARS-CoV-2, Adaptation, Physiological, Animals, Chiroptera, Disease Reservoirs, Humans, Immune Tolerance, Phylogeny, Selection, Genetic, Species Specificity, Ubiquitins, Cytokines, Genome, Genomics, Disease Resistance
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