A Single-Cell Transcriptome Atlas of the West African Lungfish Highlights the Respiratory Evolution of a Fish Adapted to Water and Land

Abstract The six species of lungfish possess both lungs and gills and are the closest extant relatives to tetrapods. Here, we report a single-cell transcriptome atlas of the West African lungfish (Protopterus annectens). This species manifests the most extreme form of terrestrialization, a life history strategy to survive dry periods in five lungfish species that can last for years, manifested by dormancy and reversible adaptive changes of the gills and lungs. Our atlas highlights the cell type diversity of the West African lungfish, including gene expression consistent with phenotype changes of terrestrialization. Comparisons with terrestrial tetrapods and ray-finned fishes revealed broad homology between the swim bladder and lung cell types and shared and idiosyncratic changes of the repressed, external gills of the West African lungfish and the internal gills of Atlantic salmon. The single-cell atlas presented here provides a valuable resource for further exploration of the evolution of the vertebrate respiratory system and the diversity of lungfish terrestrialization.