Dynamic Transport and Cementation of Skeletal Elements Build Up the Pole-and-Beam Structured Skeleton of Sponges

Animal bodies are shaped by skeletons, which are built inside the body by biomineralization of condensed mesenchymal cells in vertebrates [1, 2] and echinoderms [3, 4], or outside the body by apical secretion of extracellular matrices by epidermal cell layers in arthropods [5]. In each case, the skeletons’ shapes are a direct reflection of the pattern of skeleton-producing cells [6]. Here we report a newly discovered mode of skeleton formation: assembly of sponges’ mineralized skeletal elements (spicules) in locations distant from where they were produced. Although it was known that internal skeletons of sponges consist of spicules assembled into large pole-and-beam structures with a variety of morphologies [7–10], the spicule assembly process (i.e., how spicules become held up and connected basically in staggered tandem) and what types of cells act in this process remained unexplored. Here we found that mature spicules are dynamically transported from where they were produced and then pierce through outer epithelia, and their basal ends become fixed to substrate or connected with such fixed spicules. Newly discovered “transport cells” mediate spicule movement and the “pierce” step, and collagen-secreting basal-epithelial cells fix spicules to the substratum, suggesting that the processes of spiculous skeleton construction are mediated separately by specialized cells. Division of labor by manufacturer, transporter, and cementer cells, and iteration of the sequential mechanical reactions of “transport,” “pierce,” “raise up,” and “cementation,” allows construction of the spiculous skeleton spicule by spicule as a self-organized biological structure, with the great plasticity in size and shape required for indeterminate growth, and generating the great morphological diversity of individual sponges. [Display omitted] •Live imaging shows dynamic transport and assembly of spicules in E. fluviatilis•Newly discovered “transport cells” carry and finally push spicules through epithelia•Raised-up spicules are cemented by collagen expressed in basal epithelial cells•Iteration of “transport-pierce-raise up-cementation” constructs the skeleton Nakayama et al. find that the inner body skeleton of sponges is constructed by mechanisms fundamentally different from the known skeleton formation of animals. The spicules are dynamically transported by newly discovered “transport cells,” and the iteration of sequential mechanical reactions of player cells builds up sponges’ skel