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Siliceous Spicules and Skeleton Frameworks in Sponges: Origin, Diversity, Ultrastructural Patterns, and Biological Functions

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Siliceous Spicules and Skeleton Frameworks in Sponges: Origin, Diversity, Ultrastructural Patterns, and Biological Functions MICROSCOPY RESEARCH AND TECHNIQUE 62:279–299 (2003) Siliceous Spicules and Skeleton Frameworks in Sponges: Origin, Diversity, Ultrastructural Patterns, and Biological Functions 1 2 1 1 MARI´A-J. URIZ, * XAVIER TURON, MIKEL A. BECERRO, AND GEMMA AGELL 1Center for Advanced Studies (CSIC), Girona, Spain 2Department of Animal Biology (Invertebrates), University of Barcelona, Barcelona, Spain KEY WORDS silification; spicules; ultrastructure; sponges ABSTRACT Silica deposition is a fundamental process in sponges. Most sponges in the Classes Demospongiae and Hexactinellida secrete siliceous elements, which can subsequently fuse, inter- lock 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 pres- ence 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. Microsc. Res. Tech. 62:279–299, 2003. © 2003 Wiley-Liss, Inc. INTRODUCTION mined such diversity remained elusive until recently. Sponges, regardless of the Class to which they belong Harrison and Simpson (1976) and later authors (e.g., (i.e., Calcarea Bowerbank, Demospongiae Sollas, or Garrone et al., 1981) attributed to both the protein- Hexactinellida Schmidt), secrete mineral or protein- aceous spicule core (the axial filament) and the sur- aceous structures that give them a variety of three- rounding membrane (silicalemma) a role in shaping dimensional shapes, which minimizes the metabolic the spicules. Most of those early contributions were cost of water exchange (Vogel, 1974; Larsen and Riis- reviewed ϳ20 years ago (e.g., Volcani, 1981; Simpson, gard, 1994; Riisgard and Larsen, 1995). 1984, 1989), and here we focus on progress since then. Most Demospongiae and Hexactinellida produce sil- Recent molecular studies (Shimizu et al., 1998; Cha et ica-made skeletons consisting of individualized ele- al., 1999, 2000; Krasko et al., 2000) cast light on the ments (spicules) of lengths ranging from micrometers genetic control of spicule deposition. In contrast, the to centimeters, which can subsequently fuse or inter- role of membranes in modulating spicule ornamenta- lock with each other. The two classes differ from a tion (spines and swellings) or the terminal formations skeletal point of view in the number of symmetry axes of their megascleres, which are monaxons and tetrax- ons in demosponges and monaxons and triaxons in hexactinellids (Fig. 1). Contract grant sponsor: CICYT; Contract grant number: MAR98-1004-C02; Contract grant sponsor: Generalitat of Catalonia; Contract grant numbers: The high diversity of spicule shapes and sizes (Fig. 2) 1999SGR00184 and REN2001-2312-CO3/MAR and INTERREG-III-2002 (to in both fossil and living sponges has been repeatedly MJU and XT). reported (e.g., Hinde, 1887–1893; Hartman, 1981; *Correspondence to: Marı´a-J. Uriz, Center for Advanced Studies (CSIC), Acce´s a la Cala St. Francesc, 14 17300 Blanes, Girona, Spain. E-mail: Simpson, 1984) and has received particular attention [email protected] in taxonomic and cladistic studies (e.g., Chombard et Received 7 August 2002; accepted in revised form 20 April 2003 al., 1998; Hooper, 1990; Rosell and Uriz, 1997; Uriz and DOI 10.1002/jemt.10395 Carballo, 2001). However, the mechanisms that deter- Published online in Wiley InterScience (www.interscience.wiley.com). © 2003 WILEY-LISS, INC. 280 M.-J. URIZ ET AL. Fig. 1. Typical megascleres of demo- sponges and hexactinellids. A,B: Light mi- croscope image of tetraxons (triaenes) of several families of astrophorid Demo- spongiae. C: SEM photograph of a triaxon (hexactine). D: SEM acanthotriaene of Thrombus (C, modified from Uriz, 1988; D, modified from Uriz, 2002). of desma arms (which interlock to form rigid skeletons) Geodiidae, Ancorinidae, or Tethyidae). An accessory are only implicitly accepted (e.g., Garrone et al., 1981). role of microscleres in the sponge skeleton can be as- sumed after observing sponge species that grow and SPICULE DIVERSITY reproduce normally but lack one or several types of Siliceous sponge spicules have traditionally been microsclere. In adverse environmental conditions, such separated into two categories termed, according to as limited silicic acid availability (Yourassowsky and their size, megascleres and microscleres (e.g., Le´vi, Rasmont, 1983; Maldonado et al., 1999), sponges may 1973). However, size alone does not suffice to separate not produce microscleres, which has no detectable ef- the two categories in all cases. Some microscleres (e.g., fect on the main skeleton framework, species shape, or toxas of Microciona, sigmas of Mycale or onychaetes of thickness or ecological success. For instance, Crambe Tedania) can be larger than some megascleres (e.g., crambe is one of the few sponge species that competes oxeas in Haliclona). Moreover, there are species with successfully for the substrate with seaweeds in the spicules of intermediate size (e.g., family Plakinidae), western and central Mediterranean sublittoral (e.g., which are called mesoscleres only in hexactinellid Uriz et al., 1992), although silica concentration in these sponges (Reiswig, 2002). On the other hand, several waters does not allow the species to produce its char- spicule shapes are exclusively present among either acteristic microscleres (Uriz and Maldonado, 1995). megascleres or microscleres, but there are also a num- Siliceous spicules are highly diverse in sponges and ber of exceptions (e.g., microxeas and microstrogyles the selection pressures responsible are difficult to en- are similar in shape to, but smaller than, oxeas and visage. There are over 12 basic types of megasclere and strongyles). 25 types of microsclere reported in Demospongiae, A more “functional” diagnostic character used to sep- 20 basic types of megasclere, and 24 types of micro- arate megascleres from microscleres is their role in sclere in Hexactinellida, besides a long list of varia- skeleton organization. Megascleres usually form the tions of the basic types (Fig. 3) (Boury-Esnault and main skeletal framework. In contrast, microscleres are Ru¨ tzler, 1997; Tabachnick and Reiswig, 2002). widespread in the sponge body and only rarely are they In several orders of demosponges, some megascleres embedded in collagenous material (e.g., when they are or microscleres (desmas) become hypersilified and in- concentrated in a peripheral layer—the cortex—as in terlock to form a compact (“lithistid”) skeleton (Fig. 4) SILICEOUS SPICULES AND SKELETON FRAMEWORKS 281 Fig. 2. SEM images of microscleres from different orders of Demospongiae and Hexactinellida. A: spirasters of Spi- rastrella. B: asterose microacanthostyle of Discorhabdella. C: discorhabds of La- trunculia. D: sterrasters of Geodia. E: microscleres of Paradesmanthus. F: flo- ricome (microhexaster) of Sympagella (B,C,F, modified from Uriz, 1988; E, modified from Boury-Esnault et al., 1994). that may confer a stony consistency to the sponge. In pressed (e.g., C. crambe, Maldonado et al., 1999). Con- species that have the genetic potential to produce des- versely, in high Si concentrations, no desmoid spicules mas, the concentration of silicic acid in the environ- accumulate additional silica, giving rise to “abnormal- ment may determine whether these spicules are ex- ities” (Fig. 5). In upwelling regions such as the Namibia 282 M.-J. URIZ ET AL. Fig. 4. SEM image of interlocked desmas of Crambe acuata (Mod- ified from Uriz, 1988). Spicules up to several cm long (e.g., Le´vi, 1989) and strongly hypersilified skeletons are typical of many hexactinellid sponges. SKELETAL FRAMEWORKS Spicules and most particularly megascleres can be distributed throughout the sponge mesohyl but they generally frame two- or three-dimensional structures joined by spongin (most demosponges), interlock with each other (lithistids), or are cemented by additional silica (Hexactinellids). In contrast to the high diversity
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