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Metamorphosis is a key process in the life history of sea urchin Heliocidaris crassispina. However, the understanding of its molecular mechanisms is still lacking, especially the basic cell biology pre-metamorphosis and post-metamorphosis. Therefore, we employed single-cell RNA sequencing to delineate the cellular states of larvae and juveniles of H. crassispina. Our investigation revealed that the cell composition in sea urchins comprises six primary populations, encompassing nerve cells, skeletogenic cells, immune cells, digestive cells, germ cells, and muscle cells. Subsequently, we identified subpopulations within these cells. Our findings indicated that the larval peripheral nerves were discarded during metamorphosis. A decrease in the number of spicules was observed during this process. Additionally, we examined the differences between larval and adult pigment cells. Meanwhile, cellulase is highlighted as an essential factor for the development of competent juveniles. In summary, this study not only serves as a valuable resource for future research on sea urchins but also deepens our understanding of the intricate metamorphosis process.
2018YFD0901605 Special Project on Blue Granary Science and Technology Innovation under the National Key R & D Program, 2021J01826 Natural Science Foundation of Fujian Province
Figure 1. The cell atlas of the sea urchin H. crassispina. (a) t-SNE analysis was performed on cells obtained from eight-armed larvae, competent larvae, new juveniles, and competent juveniles, resulting in the identification of twenty-two cell clusters. These clusters were tagged with different colors and assigned to six groups: NCs (nerve cells), SCs (skeletogenic cells, including PMC [primary mesenchymal cell] and SMC [secondary mesenchymal cell]), ICs (immune cells, containing PCs [pigment cells, C13] and NPCs [non-pigment cells]), DCs (digestive cells), GCs (germ cells), and MCs (muscle cells). (b) Violin plots were utilized to depict the expression patterns of marker genes used for NC population identification. (c) Representative genes of the SC population are displayed using violin graphs to highlight their expression profiles. (d) The predominant genes of the IC group were visualized using violin plots. The violin plot represents the expression abundance of a gene in a cell cluster. The X-axis represents the cell cluster, and the Y-axis represents the expression level. (e) The distribution of marker genes for the DC population identification was illustrated. (f) t-SNE plots displayed the expression levels of marker genes used in discerning the GC population. (g) The identification of the MC population benefits from the expression levels of a few key genes.
Figure 2. The cell cluster profiles during metamorphosis. (a) Line charts show the changes in cell frequency for the five modules. Each sample’s total cell abundance sums up to 100%, with the Y-axis denoting the proportion of a specific cluster within the sample. (b–f) Except for Module 2 (c), common biological processes enriched by at least three clusters in Module 1 (b), 3 (d), 4 (e), and 5 (f) are displayed on the left. Venn diagrams visually represent the shared upregulated genes within each GO in terms of different clusters on the right. It should be noted that genes with the same name represent different transcripts.
Figure 3. The cellular heterogeneity in the NC subsets. (a) The UMAP graph shows the NC subsets at a resolution of 0.5. (b) The marker genes used to identify subsets. (c) The cell abundances of 19 NC subsets.
Figure 4. Cell classification of C6 in the SC population. (a) The UMAP plot illustrates the C6 subclusters at a resolution of 0.5. (b) The cell frequencies of the four subclusters. (c) The heatmap displays the top five upregulated genes (based on fold change) in each subcluster. (d) The distribution of the four subclusters along the pseudotime trajectory. (e) The distribution and clustering of symbolic genes with different differentiation fates. Note: “Isoform” means unknown; genes sharing the same name represent different transcripts; the “SPU” genes can be found in the Echinobase (https://www.echinobase.org/entry/, accessed on 20 April 2022).
Figure 5. The overall landscape of C13 in PC. (a) The UMAP graph represents the C13 subgroups at a resolution of 0.2 (left), while the bubble graph displays the expression levels of Dmbt, A2ml1, and Fmo6l in each subgroup (right). (b) The UMAP graph portrays the C13 subgroups at a resolution of 0.5 (left); the bubble graph shows the expression levels of Dmbt, A2ml1, and Fmo6l in each subgroup (middle), alongside the cell abundances of the four subgroups (right). (c) The bubble graph demonstrates the expression profiles of marker genes in two subclasses of subgroup 1 at a resolution of 0.8 (left), accompanied by the cell frequencies of the two subclasses. (d) A comparison of GO terms between the two subclasses. (e) The distribution of these subclusters on the pseudotime trajectory using PAGA analysis. (f) The pseudotime trajectory using Monocle based on samples. Note: “Isoform” means unknown, and genes with the same name represent different transcripts.
Figure 6. The overall landscape of the DC population. (a) The UMAP graph illustrates the distribution of the DC population at a resolution of 0.5 (left) and the cell abundances of the seven subpopulations (right). (b) The heatmap displays the top five upregulated genes of each subpopulation based on fold change. (c) The distribution of subpopulations 0, 3, and 5 on the pseudotime trajectory. (d) PAGA analysis was utilized to display the distribution of the seven subpopulations on the pseudotime trajectory (above); the pseudotime trajectory of subpopulations 0, 1, 3, and 5 (below). (e) The distribution of cellulase on the UMAP plot. Note: “Isoform” means unknown, and genes with the same name represent different transcripts.
