Lineage dynamics of the endosymbiotic cell type in the soft coral Xenia

• Published in: Nature (London) 2020-06, Vol.582 (7813), p.534-538
• Main Authors: Hu, Minjie, Zheng, Xiaobin, Fan, Chen-Ming, Zheng, Yixian
• Format: Article
• Language: English
• Subjects: 14/1; 14/19; 38/23; 38/32; 38/71; 38/91; 45/90; 631/337/2019; 631/80; 96/31; Algae; Analysis; Animals; Anthozoa - cytology; Anthozoa - genetics; Anthozoa - immunology; Anthozoa - metabolism; Carbon; Carbon - metabolism; Cell Differentiation - genetics; Cell Lineage - genetics; Chromosomes; Coral bleaching; Coral reef ecosystems; Coral Reefs; Corals; Coupling (molecular); Dinoflagellates; Dinoflagellida - immunology; Dinoflagellida - metabolism; Dinoflagellida - physiology; Ecosystem; Ecosystem degradation; Endocytosis; Endosymbionts; Endosymbiosis; Environmental stress; Gene sequencing; Genes; Genetic aspects; Genome - genetics; Genomes; Genomics; Growth; Harbors; Humanities and Social Sciences; Identification and classification; Immunomodulation; Inorganic carbon; Ligands; Maintenance; Marine ecosystems; Microorganisms; multidisciplinary; Natural history; Phagocytosis; Photosynthesis; Proteins; Recognition; Regeneration; Ribonucleic acid; RNA; RNA sequencing; RNA-Seq; Science; Science (multidisciplinary); Single-Cell Analysis; Soft corals; Symbiosis - genetics; Symbiosis - immunology; Transcriptome; Unicellular organisms
• ISSN: 0028-0836; 1476-4687; 1476-4687
• DOI: 10.1038/s41586-020-2385-7

Many corals harbour symbiotic dinoflagellate algae. The algae live inside coral cells in a specialized membrane compartment known as the symbiosome, which shares the photosynthetically fixed carbon with coral host cells while host cells provide inorganic carbon to the algae for photosynthesis 1 . This endosymbiosis—which is critical for the maintenance of coral reef ecosystems—is increasingly threatened by environmental stressors that lead to coral bleaching (that is, the disruption of endosymbiosis), which in turn leads to coral death and the degradation of marine ecosystems 2 . The molecular pathways that orchestrate the recognition, uptake and maintenance of algae in coral cells remain poorly understood. Here we report the chromosome-level genome assembly of a Xenia species of fast-growing soft coral 3 , and use this species as a model to investigate coral–alga endosymbiosis. Single-cell RNA sequencing identified 16 cell clusters, including gastrodermal cells and cnidocytes, in Xenia sp. We identified the endosymbiotic cell type, which expresses a distinct set of genes that are implicated in the recognition, phagocytosis and/or endocytosis, and maintenance of algae, as well as in the immune modulation of host coral cells. By coupling Xenia sp. regeneration and single-cell RNA sequencing, we observed a dynamic lineage progression of the endosymbiotic cells. The conserved genes associated with endosymbiosis that are reported here may help to reveal common principles by which different corals take up or lose their endosymbionts. Single-cell RNA sequencing identifies the pattern of gene expression during lineage progression in endosymbiotic cells of the fast-growing soft coral Xenia , revealing principles that underlie uptake and maintenance of endosymbionts by this coral.