Siliceous spicules and skeleton frameworks in sponges: Origin, diversity, ultrastructural patterns, and biological functions

Abstract

Silica deposition is a fundamental process in sponges. Most sponges in the Classes Demospongiae and Hexactinellida secrete siliceous elements, which can subsequently fuse, interlock with each other, or form three-dimensional structures connected by spongin. The resulting skeletal frameworks allow sponges to grow upwards and facilitate water exchange with minimal metabolic cost. Several studies on sponge skeletogenesis have been published. We are beginning to understand the mechanisms of spicule secretion and the role of spicules and skeletal frameworks in the biology, ecology, and evolution of sponges. Molecular techniques and ecological experiments have demonstrated the genetic control of the process and the contribution of environmental factors to the expression of a sponge spicule, respectively. However, other classic topics such as the role of membranes in silicon transport or whether spicules are formed in situ or secreted anywhere in the sponge mesohyl and then transported to the skeletal framework require further investigation. We review the process of silica deposition in sponges at the molecular and cellular levels, as well as the biological and ecological functions of spicules and skeletons. The genetic control of spicule shapes makes them useful in the reconstruction of sponge phylogeny, although recent experiments have demonstrated the influence of environmental factors in modulating spicule size, shape, and the presence or absence of one or more spicule types. The implications of such variations in sponge taxonomy may be important. Besides supporting sponge cells, spicules can help larvae stay buoyant while in the plankton or reach the bottom at settlement, enhance reproduction success, or catch prey. Conversely, the role of spicules and skeletons in deterring predation has not been demonstrated. Knowledge of several aspects is still based on a single or a few species and extrapolations should be made only with caution. With the advent of new molecular techniques, new lines of research are presently open and active in this field.

Formation of giant spicules in the deep-sea hexactinellid Monorhaphis chuni (Schulze 1904): electron-microscopic and biochemical studies

“…The major reason for studying the structure of the spicules here has been to understand the growth pattern of the spicules in an axial and radial direction. All (or almost all) spicules of M. chuni are open at their tips (Schulze 1904;Uriz 2006;Uriz et al 2003); their axial canals occasionally expose the axial filaments. This finding has contributed to the understanding of the axial growth of the spicules (see below).…”

“…Electron-microscopic studies have revealed that the tips of the spicules from this hexactinellid can be distinguished from those found in Demospongiae (Uriz et al 2003), since all of them are open (Schulze 1904). The images show that the characteristic quadratic opening, viz., the axial canal, occasionally possesses an axial filament that reaches the upper edges of the top orifice.…”

Митохондријални Геноми Класе Demospongiae Sollas 1885

“…Поткласа Традиционално се систематика разреда Porifera заснивала на спикулама, чија се морфологија и еволуција исцрпно истраживала (Dendy, 1921;Jones, 1997;Uriz et al, 2003), али информације које оне пружају су ограничене да би се могла ријешити проблематика класификације спужви. Друге морфолошке особине попут облика, грађе и боје, зависе од услова средине, па се не могу узети као таксономски карактер.…”

Assessing the Potential of Sponges (Porifera) as Indicators of Ocean Dissolved Si Concentrations

“…Through complex enzymatic and metabolic processes (Wang et al, 2011a(Wang et al, ,b, 2012a, siliceous species of Hexactinellida, Demospongiae and Homoscleromorpha take up Si (predominantly present as silicic acid, H 4 SiO 4 and conventionally referred to as dissolved silica; dSi) from their surrounding water to secrete individual structures known as spicules which provide skeletal support to the organic components of the sponge (Uriz et al, 2003). In some species of hexactinellids and demosponges, skeletal structures are massive and hypersilicified, with stony consistency and can form agglomerates and build reef-like formations (Conway et al, 2001;Uriz et al, 2003;Leys et al, 2004;Maldonado et al, 2015a,b) or "sponge grounds" (Klitgaard and Tendal, 2004).…”

“…In some species of hexactinellids and demosponges, skeletal structures are massive and hypersilicified, with stony consistency and can form agglomerates and build reef-like formations (Conway et al, 2001;Uriz et al, 2003;Leys et al, 2004;Maldonado et al, 2015a,b) or "sponge grounds" (Klitgaard and Tendal, 2004). Sponges of these groups may be important players in the global silicon cycle due to their widespread occurrence and high preservation potential (Maldonado et al, 2005(Maldonado et al, , 2010.…”