Produce, carry/position, and connect: morphogenesis using rigid materials

Animal morphogenesis can be summarized as a reconfiguration of a mass of cells. Although extracellular matrices that include rigid skeletal elements, such as cartilage/bones and exoskeletons, have important roles in morphogenesis, they are also secreted in situ by accumulated cells or epithelial cells. In contrast, recent studies of the skeleton construction of sponges (Porifera) illuminate a conceptually different mechanism of morphogenesis in which cells manipulate rather fine rigid materials (spicules) to form larger structures. Here, two different types of sponge skeleton formation using calcareous spicules or siliceous spicules are compared with regard to the concept of the production of rigid materials and their use in skeletons. The comparison highlights the advantages of their different strategies of forming sponge skeletons.

Introduction

Sponges have biomineralized skeletons consisting of assemblies of exceedingly large numbers of fine skeletal elements (about several hundred micrometers in length), known as spicules. Since sponges have fundamentally different skeletons from any other multicellular animals, we may be able to learn novel mechanisms of morphogenesis from sponges. Sponge spiculous skeletons are classified into two types: calcareous skeletons (of Class Calcarea) and siliceous skeletons (of Demospongiae, Hexactinellida and Homoscleromorpha) [1, 2, 3, 4, 5]. There are three major differences between them. In calcareous skeletons, (i) the mineralized material is CaCO₃ (mainly as crystalline magnesium-calcite), (ii) spicules are produced intercellularly, (iii) the skeleton is generally a framework of spicules, in which spicules are not connected to each other but overlapped to support the sponge body [4,5] (Table 1, row). In contrast, in siliceous skeletons, (i) the mineralized material is SiO₂ (as amorphous silica), (ii) spicules are at least initially produced intracellularly, (iii) spicules are connected to form a roughly poles and beams structure (Table 1, middle and lower rows). In most demosponges, skeletal spicules are connected by collagen matrices to build up the skeleton [2,4]. In hexactinellids, spicules are overlapped to form a framework, and can be fused by being wrapped with an additional surrounding silica layer that reinforces the spiculous skeleton [2, 3, 4,6] (Table 1, lower row). In Homoscleromorpha (a small class that used to be classified as demosponges), in species that have a skeleton, skeletal spicules are generally dispersed in the sponge body. Spicules can be overlapped surrounding the aquiferous system [7,8] (Table 1, lowest row).

The highly diversified forms of spicules have drawn much attention, and thus their forms, structures, mineral, and organic compositions have been extensively studied [3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16]. The spicule-producing cells (‘sclerocytes’ as a collective designation) have also been well studied, mostly using SEM and TEM [8,10,11,14,17]. Porifera is a large phylum, and different classes of sponges differ regarding both the production of spicules and construction of their skeleton [2, 3, 4, 5,7,18]. Since there are multiple reviews of studies of those issues [2, 3, 4, 5, 6], here, the minimum information necessary to introduce this basic knowledge is described. The commonalities of the mechanisms of spicule production, and the differences between and advantages of two different types of skeleton construction (non-connected spiculous frameworks and connected spiculous skeleton) are discussed. Considering that the shape of animals is basically defined by their skeleton, here, mechanisms of spiculous skeleton construction are proposed as multistep morphogenetic mechanisms in which cells produce, locate/carry, and connect rigid materials.