The architecture of cell differentiation in choanoflagellates and sponge choanocytes

The architecture of cell differentiation in choanoflagellates and sponge choanocytes
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领鞭毛虫与海绵领细胞中细胞分化的结构特征

DOI:
10.1371/journal.pbio.3000226
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发表时间:
2019-04-01
期刊:
影响因子:
9.8
通讯作者:
Burkhardt, Pawel
Burkhardt, Pawel
中科院分区:
生物学1区
文献类型:
--
作者:
Laundon, Davis;Larson, Ben T.;Burkhardt, Pawel

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尽管项圈细胞在动物及其近亲--脊椎动物中都是保守的,但人们对它们的祖先、亚细胞结构或如何分化知之甚少。脊椎动物Salpingoeca Rosetta表达动物发育所必需的基因,并可以在单细胞和多细胞状态之间切换,使其成为研究动物多细胞起源和细胞分化机制的强大模型。为了比较罗塞塔单细胞领细胞与多细胞“玫瑰花环”集落和海绵领细胞的亚细胞结构,我们在超薄切片上用透射电子显微镜重建了整个细胞的三维结构。对我们的3D重建的结构分析表明,单个和集落节节细胞之间存在重要的差异,集落细胞表现出更多的阿米巴形态,与更高水平的大吞饮细胞吞噬活动相一致。多个重组玫瑰花环菌落的比较突出了细胞大小、细胞间接触网络和菌落排列的不同性质。重要的是,我们发现在一些玫瑰状集落中存在细长的细胞,这些细胞可能代表一种不同的分化细胞类型,指向空间细胞分化。脊椎动物菌落内的细胞间桥表现出各种形态,并连接一些但不是所有邻近细胞。海绵后鼻孔细胞的重建显示了超微结构的共性,但主要细胞器的组成也与后鞭毛虫不同。总之,我们的比较重建揭示了脊椎动物和海绵脊椎动物的细胞分化结构,并构成了重建动物最后共同祖先的细胞生物学的重要一步。
Although collar cells are conserved across animals and their closest relatives, the choanoflagellates, little is known about their ancestry, their subcellular architecture, or how they differentiate. The choanoflagellate Salpingoeca rosetta expresses genes necessary for animal development and can alternate between unicellular and multicellular states, making it a powerful model for investigating the origin of animal multicellularity and mechanisms underlying cell differentiation. To compare the subcellular architecture of solitary collar cells in S. rosetta with that of multicellular 'rosette' colonies and collar cells in sponges, we reconstructed entire cells in 3D through transmission electron microscopy on serial ultrathin sections. Structural analysis of our 3D reconstructions revealed important differences between single and colonial choanoflagellate cells, with colonial cells exhibiting a more amoeboid morphology consistent with higher levels of macropinocytotic activity. Comparison of multiple reconstructed rosette colonies highlighted the variable nature of cell sizes, cell-cell contact networks, and colony arrangement. Importantly, we uncovered the presence of elongated cells in some rosette colonies that likely represent a distinct and differentiated cell type, pointing toward spatial cell differentiation. Intercellular bridges within choanoflagellate colonies displayed a variety of morphologies and connected some but not all neighbouring cells. Reconstruction of sponge choanocytes revealed ultrastructural commonalities but also differences in major organelle composition in comparison to choanoflagellates. Together, our comparative reconstructions uncover the architecture of cell differentiation in choanoflagellates and sponge choanocytes and constitute an important step in reconstructing the cell biology of the last common ancestor of animals.