Abstract

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 photosynthesis1. 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 ecosystems2. 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 coral3, 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.

Highlights

  • The Xenia sp. genome encodes essential components of RNA interference, such as Dicer and Ago, and DNA repair pathway proteins, which should enable the development of gene-manipulation tools to determine the mechanism of endosymbiosis

  • We focused on studying the endosymbiotic cell lineage, the regenerative processes for the other cell clusters can be investigated in future analyses

  • Our studies suggest that Xenia endosymbiotic cells exist in five progressive states that are dynamic between homeostatic conditions and the regeneration process (Fig. 4f)

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Summary

Summary and outlook

We demonstrate the power of genomic and bioinformatic tools in studying coral biology. Our studies suggest that Xenia endosymbiotic cells exist in five progressive states that are dynamic between homeostatic conditions and the regeneration process (Fig. 4f). Transcriptomic changes with increasing algal symbiont reveal the detailed process underlying establishment of coral–algal symbiosis. H. et al Whole transcriptome analysis reveals changes in expression of immune-related genes during and after bleaching in a reef-building coral. F. et al A diverse host thrombospondin-type-1 repeat protein repertoire promotes symbiont colonization during establishment of cnidarian–dinoflagellate symbiosis. K. The scavenger receptor repertoire in six cnidarian species and its putative role in cnidarian–dinoflagellate symbiosis. Sebe-Pedros, A. et al Cnidarian cell type diversity and regulation revealed by whole-organism single-cell RNA-seq. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

Methods
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