Long-Read Sequencing Reveals Rapid Evolution of Immunity- and Cancer-Related Genes in Bats

Scheben, Armin, Mendivil Ramos, Olivia, Kramer, Melissa, Goodwin, Sara, Oppenheim, Sara, Becker, Daniel J, Schatz, Michael C, Simmons, Nancy B, Siepel, Adam, McCombie, W Richard (September 2023) Long-Read Sequencing Reveals Rapid Evolution of Immunity- and Cancer-Related Genes in Bats. Genome Biology and Evolution, 15 (9). ISSN 1759-6653 (Public Dataset)

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Abstract

Bats are exceptional among mammals for their powered flight, extended lifespans, and robust immune systems and therefore have been of particular interest in comparative genomics. Using the Oxford Nanopore Technologies long-read platform, we sequenced the genomes of two bat species with key phylogenetic positions, the Jamaican fruit bat (Artibeus jamaicensis) and the Mesoamerican mustached bat (Pteronotus mesoamericanus), and carried out a comprehensive comparative genomic analysis with a diverse collection of bats and other mammals. The high-quality, long-read genome assemblies revealed a contraction of interferon (IFN)-α at the immunity-related type I IFN locus in bats, resulting in a shift in relative IFN-ω and IFN-α copy numbers. Contradicting previous hypotheses of constitutive expression of IFN-α being a feature of the bat immune system, three bat species lost all IFN-α genes. This shift to IFN-ω could contribute to the increased viral tolerance that has made bats a common reservoir for viruses that can be transmitted to humans. Antiviral genes stimulated by type I IFNs also showed evidence of rapid evolution, including a lineage-specific duplication of IFN-induced transmembrane genes and positive selection in IFIT2. In addition, 33 tumor suppressors and 6 DNA-repair genes showed signs of positive selection, perhaps contributing to increased longevity and reduced cancer rates in bats. The robust immune systems of bats rely on both bat-wide and lineage-specific evolution in the immune gene repertoire, suggesting diverse immune strategies. Our study provides new genomic resources for bats and sheds new light on the extraordinary molecular evolution in this critically important group of mammals.

Item Type:	Paper
Subjects:	diseases & disorders > cancer diseases & disorders diseases & disorders > neoplasms organism description > animal organism description > animal > mammal > bats evolution organs, tissues, organelles, cell types and functions > cell types and functions > cell functions > immunity organism description > animal > mammal
CSHL Authors:	Scheben, Armin Mendivil Ramos, Olivia Kramer, Melissa R. Goodwin, Sara Schatz, Michael C. Siepel, Adam McCombie, W. Richard
Communities:	CSHL labs > McCombie lab CSHL labs > Schatz lab CSHL labs > Siepel lab CSHL Cancer Center Program CSHL Cancer Center Program > Cancer Genetics and Genomics Program CSHL Cancer Center Shared Resources > Sequencing Technology & Analysis Service
SWORD Depositor:	CSHL Elements
Depositing User:	CSHL Elements
Date:	4 September 2023
Date Deposited:	21 Sep 2023 14:13
Last Modified:	09 Feb 2024 15:50
PMCID:	PMC10510315
Related URLs:	Publisher
Dataset ID:	BioProject: PRJNA751559
URI:	https://repository.cshl.edu/id/eprint/40935

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