Morphogenesis of calcitic sponge spicules: a role for specialized proteins interacting with growing crystals
Joanna AizenbergJonathan C. HansonMicha IlanLeslie LeiserowitzThomas F. KoetzleLia AddadiStephen Weiner
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Crystals formed in biological tissues often adopt remarkable morphologies that are thought to be determined mainly by the shapes of the confined spaces in which they grow. Another possible way of controlling crystal shape, demonstrated only in vitro, is by means of specialized proteins preferentially interacting with certain crystal faces. In so doing, they reduce the rate of growth in these directions and consequently change the overall crystal shape. In an X-ray diffraction study of the distribution of defects within the lattice of calcite crystals produced by certain sponges, we show that a remarkable correlation exists between the defect patterns or crystal texture and the macroscopic morphology of the spicules. This was observed in two cases in which proteins are present within the spicule crystal, but not in a third case where such intracrystalline proteins are absent. Furthermore, one of the spicules exhibited marked differences in texture even within families of structurally identical crystal planes, demonstrating that the organisms exert exquisite control over the microenvironment in which crystals grow. We conclude that highly controlled intercalation of specialized proteins inside the crystals is an additional means by which organisms control spicule growth.—Aizenberg, J., Hanson, J., Ilan, M., Leiserowitz, L., Koetzle, T. F., Addadi, L., Weiner, S. Morphogenesis of calcitic sponge spicules: a role for specialized proteins interacting with growing crystals. FASEB J. 9, 262–268 (1995)Keywords:
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The spicules of male parasitic nematodes are key morphological features, which vary between species in shape and length and are used often for species identification. However, little is known about spicules and particularly if/how their length varies during growth. We first assessed the degree of variation in spicule length of male Heligmosomoides bakeri 21 days post infection (PI), and then in two follow-up experiments measured spicule lengths at half daily/daily intervals between days 6 and 14 PI. Mean spicule length in 21-day worms was 0.518 mm with a range of 94 μm, and variation between the two spicules of individual worms from 2 to 32 μm. Spicules were first detectable on day 6-6.5, after which their lengths increased until day 7 PI (mean = 0.61 and 0.59). This was followed by significant contraction, initially relatively quickly over the following 48 h and then more slowly over a longer period, stabilizing by days 10-14, with only minor further reduction in length. We conclude that the length of spicules varies significantly over the first few days after they have formed, and, consequently, the age of worms is an important factor for consideration when spicule lengths are measured for experimental/diagnostic or taxonomical purposes.
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A basal spicule of the hexactinellid sponge Monorhaphis chuni may reach up to 3 m in length and 10 mm in diameter, an extreme case of large spicule size. Generally, sponge spicules are of scales from micrometers to centimeters. Due to its large size many researchers have described its structure and properties and have proposed it as a model of hexactinellid spicule development. Thorough examination of new material of this basal spicule has revealed numerous inconsistencies between our observations and earlier descriptions. In this work, we present the results of detailed examinations with transmitted light and epifluorescence microscopy, SEM, solid state NMR analysis, FTIR and X-ray analysis and staining of Monorhaphis chuni basal spicules of different sizes, collected from a number of deep sea locations, to better understand its structure and function.Three morphologically/structurally different silica layers i.e. plain glassy layer (PG), tuberculate layer (TL) and annular layer (AL), and an axial cylinder (AC) characterize adult spicules. Young, immature spicules display only plain glassy silica layers which dominate the spicule volume. All three layers i.e. PG, TL and AL can substitute for each other along the surface of the spicule, but equally they are superimposed in older parts of the spicules, with AL being the most external and occurring only in the lower part of the spicules and TL being intermediate between AL and PG. The TL, which is composed of several thinner layers, is formed by a progressive folding of its surface but its microstructure is the same as in the PG layer (glassy silica). The AL differs significantly from the PG and TL in being granular and porous in structure. The TL was found to display positive structures (tubercles), not depressions, as earlier suggested. The apparent perforated and non-perforated bands of the AL are an optical artefact. The new layer type that we called the Ripple Mark Layer (RML) was noted, as well as narrow spikes on the AL ridges, both structures not reported earlier. The interface of the TL and AL, where tubercles fit into depressions of the lower surface of the AL, represent tenon and mortise or dovetail joints, making the spicules more stiff/strong and thus less prone to breaking in the lower part. Early stages of the spicule growth are bidirectional, later growth is unidirectional toward the spicule apex. Growth in thickness proceeds by adding new layers. The spicules are composed of well condensed silica, but the outermost AL is characterized by slightly more condensed silica with less water than the rest. Organics permeating the silica are homogeneous and proteinaceous. The external organic net (most probably collagen) enveloping the basal spicule is a structural element that bounds the sponge body together with the spicule, rather than controlling tubercle formation. Growth of various layers may proceed simultaneously in different locations along the spicule and it is sclerosyncytium that controls formation of silica layers. The growth in spicule length is controlled by extension of the top of the axial filament that is not enclosed by silica and is not involved in further silica deposition. No structures that can be related to sclerocytes (as known in Demospongiae) in Monorhaphis were discovered during this study.Our studies resulted in a new insight into the structure and growth of the basal Monorhaphis spicules that contradicts earlier results, and permitted us to propose a new model of this spicule's formation. Due to its unique structure, associated with its function, the basal spicule of Monorhaphis chuni cannot serve as a general model of growth for all hexactinellid spicules.
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ABSTRACT The early stages in the form-development of the perforated-plate and stool spicules of Cucumariidæ and other holothurians have been described and figured by many previous observers, as e. g. by Théel (10) in 1882, by Hérouard (4) in 1890, by Mortenson (7) and Kishinouye (5) in 1894, by Gerould (2) in 1896, and others, but in no case has the morphogenesis of the spicule been systematically studied in relation to the disposition of the scleroblasts or cells concerned in the deposition of the spicule. It is true that Hérouard (4) has provided a very detailed account of this very subject—as to the manner in which the direction of growth of the holothurian plate spicule is due to the number and disposition of the formative cells,—but since he does not provide any figures in confirmation of his statements, and since my own observations tell a very different tale, I see no reason to qualify the assertion I have just made.
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When the oscular tube grows the spicules tend to separate from one another, but the separation is not uniform; local displacements of spicules occur with respect to other spicules in the vicinity. The same is found when the tube elongates while constricting, or changes shape in other ways. The spicule displacements reveal that the mesogloeal matrix is plastic. The spicules are probably anchored to the surface epithelia, the system of anchorage varying with time and from one spicule to another. Small growing spicules may rotate through considerable angles and move relative to the fully grown spicules in their vicinity. The relative movements are most frequently towards the osculum. They are attributed to displacements of either the mesogloeal matrix or the internal epithelium, each relative to the other. They are not likely to be caused by the concerted amoeboid activity of the founder calcoblasts. The monaxons tend to maintain their positions and orientations relative to the tri- and quadri-radiate spicules, apart from small localized displacements. Thus no significant movement of the pinacoderm relative to the rest of the wall could be deduced. Fragments of broken spicules likewise tend to retain their relative positions and orientations in the spicule arrangement, though some moved or rotated by quite considerable amounts. Spicules occasionally disappeared from the wall of some tubes. Monaxons were shed relatively easily, probably as a result of the spicule crowding associated with contraction of the tube. Some tri- and quadri-radiates were also shed through the pinacoderm. In some tubes spicule protrusion occurred at the oscular edge.
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The present study focuses on spicule number, length, and positioning in larvae of two confamilial species of demosponge, Halichondria coerulea Bergquist, 1967 and Hymeniacidon heliophila (Parker, 1910). The anatomy and spiculation of newly emergent larvae were examined. On hatching, larvae of Halichondria coerulea are approximately one-half as long as larvae of Hymeniacidon heliophila. The spicules of adults and larvae of Halichondria coerulea are oxeas whereas those of Hymeniacidon heliophila adults and larvae are styles. Oxeas and styles are straight or slightly curved, and needle-shaped. In both species, spicules in larvae are significantly shorter (in mean length) than spicules of adults. This observation parallels previous reports on other species of demosponge. Mean spicule number per larva was significantly different between the two species, but the respective mean spicule lengths were indistinguishable ; some overall constraints may dictate spicule size independently of larval size. In contrast, within-species comparisons of adult spicule length versus larval length, larval spicule number versus larval length, and larval spicule number versus spicule length yielded no pairwise correlations. These data indicate that broad plasticity exists in spiculation patterns of newly hatched larvae in both species. Finally, the spicular mass of Hymeniacidon heliophila is asymmetrically positioned in the posterior region of the larva whereas the spicules of Halichondria coerulea are situated in the central region. This difference in the distribution of spicules may affect the swimming properties of the larvae of the two species differently and, possibly, also determine their positioning in the water column. It is proposed that the architecture of the flagellated epithelium governs the exclusion of spicules from the posterior region of Halichondria coerulea but is not similarly restricting in Hymeniacidon heliophila.
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The morphology, chemical composition, and optical properties of long monoaxonic spicules were studied in several species of marine deep-sea hexactinellid sponges of different orders and families: Asconema setubalense (Hexasterophora, Lyssacinosida) and Monorhaphis chuni Schulze (Monorhaphiidae). Their macrostructural organization is a system of thin layers laid around the central cylinder containing a square canal filled with organic matter. A significant role in spicule organization is played by the organic matrix. The macrostructural of organization of the spicule in Monorhaphis chuni is a system of the “cylinder-within-a-cylinder” type. However the spicule surface is covered with ridges. They penetrate a few layers into the spicule. Analysis of the elemental composition of the basalia spicule of Monorhaphis chuni demonstrates a heterogeneous allocation of C, O, Si on the spicule surface, subsurface layers, and on ridges. All studied spicules have the properties of anisotropic crystals and they demonstrate a capability to the birefrigence. On the other hand we discovered unique property of spicules—their capacity for triboluminescence. The discovery of triboluminescence in composite organosilicon materials of which the spicules of hexactinellid sponges are built may contribute to the creation of biomimetic materials capable of generating light emission.
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Spicule matrix proteins are the products of primary mesenchyme cells, and are present in calcite spicules of the sea urchin embryo. To study their possible roles in skeletal morphogenesis, monoclonal antibodies against SM50, SM30 and another spicule matrix protein (29 kDa) were obtained. The distribution of these proteins in the embryo skeleton was observed by immunofluorescent staining. In addition, their distribution inside the spicules was examined by a ‘spicule blot’ procedure, direct immunoblotting of proteins embedded in crystallized spicules. Our observations showed that SM50 and 29 kDa proteins were enriched both outside and inside the triradiate spicules of the gastrulae, and also existed in the corresponding portions of growing spicules in later embryos and micromere cultures. The straight extensions of the triradiate spicules and thickened portions of body rods in pluteus spicules were also rich in these proteins. The SM30 protein was only faintly detected along the surface of spicules. By examination using the spicule blot procedure, however, SM30 was clearly detectable inside the body rods and postoral rods. These results indicate that SM50 and 29 kDa proteins are concentrated in radially growing portions of the spicules (normal to the c‐axis of calcite), while SM30 protein is in the longitudinally growing portions (parallel to the c‐axis). Such differential distribution suggests the involvement of these proteins in calcite growth during the formation of three‐dimensionally branched spicules.
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Abstract Germanium (Ge), in the form of germanic acid, at a Ge/Si molar ratio of 1.0 inhibits gemmule development and silica deposition in the marine demosponge Suberites domuncula . Lower Ge/Si ratios inhibit the growth in length of the silica spicules (tylostyles) producing short structures, but with relatively normal morphology and close to normal width; spherical protuberances occasionally occur on these spicules. A few of the short spicules possess completely round rather than pointed tips. Many of the latter develop when Ge is added (pulsed) to growing animals, thus inducing a change in spicule type. These results indicate that the growth in length of the axial filament is more sensitive to Ge inhibition than is silica deposition and that pointed spicule tips normally develop because the growth of the axial filament at the spicule tip is more rapid than silica deposition. Newly formed spicules initiate silica deposition at the spicule head but the absence of Ge‐induced bulbs as in freshwater spicules (oxeas) leaves open the question of whether there is a silicification center(s) present in Suberites tylostyles. The morphogenesis of freshwater oxeas and of marine tyolstyles appears fundamentally different‐bidirectional growth in the former and unidirectional growth in the latter. X‐ray analysis demonstrate relatively uniform Ge incorporation into the silica spicules with considerable variation from spicule to spicule in the incorporated level. Increased silicic acid concentration induces the formation of siliceous spheres, suggesting that the axial filament becomes prematurely encased in silica.
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