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

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 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. the 10x Genomics platform (Supplementary Table 1, Methods). Using t-distributed stochastic neighbour embedding (t-SNE) 17 , we grouped the high-quality single-cell transcriptomes, covering 23,939 genes, into 16 cell clusters with distinct gene-expression patterns (Fig. 2a, b, Extended Data Fig. 3a, Supplementary Table 2). For validation, we

Invertebrate methylomes provide insight into mechanisms of environmental tolerance and reveal methodological biases

“…Furthermore, the microhabitats created in the tissues of these two species likely differ substantially spatially (Putnam et al, 2017), creating cell-to-cell variability in methylation content. Since the likelihood of capturing multiple cell types in bulk DNA extractions varies with tissue structure, future studies should consider methods such as fluorescence-activated cell sorting (Hu et al, 2020;Rosental et al, 2017), or laser microdissection (e.g., (Liew et al, 2018)), to target specific tissues or cell types and reduce cell-to-cell methylation variability. Whereas this does not necessarily indicate a bias in our methods, it highlights the needs to account for the biological characteristics of a species when designing an experiment and evaluating results.…”

Mapping single-cell atlases throughout Metazoa unravels cell type evolution

“…There is much ongoing success in producing single-cell transcriptomic atlases to investigate the cell type diversity within individual organisms (Regev et al, 2017). With the growing diversity of cell atlases across the tree of life (Briggs et al, 2018;Cao et al, 2019;Fincher et al, 2018;Hu et al, 2020;Musser et al, 2019;Plass et al, 2018;Siebert et al, 2019;Wagner et al, 2018), a new frontier is emerging: the use of cross-species cell type comparisons to unravel the origins of cellular diversity and uncover speciesspecific cellular innovations (Arendt et al, 2019;Shafer, 2019). Further, these comparisons promise to accelerate cell type annotation and discovery by transferring knowledge from well-studied model organisms to under-characterized animals.…”

Applying model approaches in non-model systems: A review and case study on coral cell culture

“…For this, methods for immortal cell lines, cell sorting [ 75 ], and single cell analyses [e.g. 76 ] need to be developed and/or advanced.…”

“…Recent work in the starlet anemone Nematosella vectensis and the soft coral Xenia sp . are the first to assess gene expression in cnidarians using a single cell RNASeq approach, and have provided detailed gene expression signatures for eight cnidarian cell classes and subtypes [ 86 ], and identified a putative endosymbiosis gene set [ 76 ], which will be essential for further functional testing. Our knowledge of the biomineralization cells and process are relatively more advanced than endosymbiotic cells, with a putative biomineralization toolkit [ 87 , 88 ] and multiple sequenced proteomes for the skeletal organic matrix [ 87 , 89 ].…”