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Serotonin in Porifera? Evidence from Developing Tedania Ignis, the Caribbean Fire Sponge (Demospongiae)

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Serotonin in Porifera? Evidence from Developing Tedania Ignis, the Caribbean Fire Sponge (Demospongiae) SEROTONIN IN PORIFERA? EVIDENCE FROM DEVELOPING TEDANIA IGNIS, THE CARIBBEAN FIRE SPONGE (DEMOSPONGIAE) SIMON WEYRER, KLAUS RÜTZLER AND REINHARD RIEGER Weyrer, S., Rützler, K. & Rieger, R. 19990630: Serotonin in Porifera ? Evidence from developing Tedania ignis, the Caribbean tire sponge (Demospongiae). Memoirs of the Queensland Museum 44: 659-665. Brisbane. ISSN 0079-8835. Histochemical study of larvae and freshly settled juveniles of the Caribbean tire sponge Tedania ignis (Tedaniidae, Poecilosclerida) reveals evidence of serotonin-like immuno-reactivity, a possible indication for the presence ofprecursors ofnerve cells in this species. Already in the earliest stages ofits life, T. ignis is made up oftwo discernable cell types: monociliated cells arranged in quasi-epithelial fashion and covering the larva and the developing settled organism, and mesohylal cells (archeocytes). In the adult sponge, several mesohylal cell types can be distinguished which form a complex connective tissue. Serotonin-like immuno-reactivity demonstrated by us occurs only in two cell types: in sorne archeocytes ofthe parenchymella larvae, and in similar archeocytes and in a second, bipolar cell type ofthe settled, juvenile sponge. The discovery ofa neuroactive substance in cells of developing sponges before and after metamorphosis provides new insights into the origin and evolution of nerve and muscle cells in the Eumetazoa. 0 Pori/era, histochemistry, serotonin, Tedania ignis, larval development, evolution. Simon Weyrer & Reinhard Rieger, Institute of Zoology and Limnology, University of Innsbruck. Technikerstrasse 25, A-6020 Innsbruck, Austria; Klaus Rützler (email: [email protected]), Department ofInvertebrate Zoology, National Museum ofNatural History, Smithsonian Institution, Washington D. C. 20560, USA; 18 January 1999. Although sponges, one ofthe oldest metazoan Phagocytella hypothesis (see Hyman, 1951; groups, possess the greatest diversity of Ivanov, 1988; Rieger et al., 1991; Ax, 1995) biologically active compounds of any marine encouraged the authors to search for precursors phylum, the neurotransmitter serotonin of nerve and muscle cells in sponge larvae in (5-hydroxytryptamine, 5-HT) has been reported early developmental stages rather than in adults, a only once, in myocyte-like cells of Sycon neglected area ofresearch so far (Harrison & De ciliatum (Sycettidae, Calcarea) (Lenz, 1966). Vos, 1991; Woollacott & Pinto, 1995). Such Serotonin appeared early in the evolution of precursors of nerve cells and myocytes in eucaryotes. For example, it is used in chemical sponges could represent the first stage in the signal chains in Protista where, in a species ofthe evolution ofintegrative systems (e.g. Payans de ciliate Blepharisma, a serotonin-like substance is Ceccatty, 1974a, 1989; Mackie, 1990). known to function as a mating pheromone (Haldane, 1954; Miyake, 1984). It has also been MATERIALS AND METHODS shown that a number of lower organisms use serotonin as an internai messenger in their neuro­ Larvae of Tedania ignis (Durchassaing & transmitter-receptor systems (Carr et al., 1989) Michelotti) (Tedaniidae, Poecilosclerida, Demo­ and that sorne of these characteristics of spongiae) were sampled in the laboratory molecular structure that arose in unicellular seawater system of the Smithsonian Coral Reef organisms may have been inherited and modified Field Station at Carrie BowCay, Belize, in March bymetazoans(Mackie, 1990; Van Houten, 1990). 1994 and November 1995. Larval release was induced in adult specimens collected in the It seems obvious that nerve cells developed nearby mangrove ofTwin Cays (Rützler & Feller, gradual1y over a long period of time but the 1996) and maintained in aerated seawater by sequences ofchanges that must have occurred are exposing them to natural sunlight fol1owing a difficult to establish. Being a primitive outgroup 12-24hr period of dark adaptation (Woollacott, ofthe Eumetazoa, Porifera do not have neurons 1993). The larvae were kept in seawater-rinsed or myocytes that are present in organisms of glass dishes (lOcm diameter) and fixed higher levels'of organisation. A common immediately after release and 80-100hrs after phylogenetic hypothesis such as the Planula or attachment to the substrate. Ta pravide a 660 MEMOIRS OF THE QUEENSLAND MUSEUM substrate suitable for fixation and removal for lie embedded among mesohyl cells (Fig. 2A). subsequent processing, the bottom of these Using a whole-mount fluorescence technique, dishes was coated with polymerised epoxy resin we found serotonin-like immuno-reactivity in (Spurr). special mesohyl cells ofboth larval andjuvenile Specimens were fixed in 4% paraform­ T. ignis. Spherical serotonergic cells appear to be aldehyde (PFA) in phosphate-buffered saline randomly distributed and occur alone or in (PBS; O.lM, pH 7.4) for 6-8hrs, rinsed in PBS, clusters (Figs lB, 2B). In one larva, for example, and. treated with Triton X-IOO (0.2%, 1hr) to 6 clusters of such serotonin positive ceIls were permeabilise membranes. After labelling with found, each composed of 2-4 single spherical the primary antibody (rabbit anti-serotonin, cells with a diameter of4-6J..lm. In some clusters IMMUNOTECH 0601; 2.5%) ovemight at 4°C, as weIl as in several single cells the nuclei are fluorescence-labelling was done for Ihr with a clearly visible and appear as non-fluorescent tetrarhodamine-isothiocyanate-(TRITC)­ regions (Fig. lB). conjugated secondary antibody (swine anti-rabbit; In the juvenile, settled sponge, a few bipolar DAKO, 1%) for 1hr. Specimens were then rinsed cells were found in addition to the spherical cells in PBS, whole-mounted (Gelmount) on slides, that superficially resemble bipolar neurons or and examined under a REICHERT Polyvar 'myocyte-like' ceIls (actinocytes) reported by epifluorescence microscope. Incubation in Bagby (1966) (Fig. 2B, C). These bipolar cells bovine-serum albumin-Triton (BSA-T) without have a maximum length of20-50J..lm. Both types primary antibody was used as the control for ofserotonin-positive cells (spherical and bipolar) nonspecific binding of the secondary antibody. appear to be located in the mesohyl as spicules Three larvae and three settled juvenile sponges can be seen ontop ofthe labelled cells (Fig. 2C). were sectioned (epoxy-embedded, 1J..lm thick, No information is yet available on whether stained with toluidin blue) and investigated in interactions between these morphological types detail. The immuno-staining of both larvae and ofserotonin-positive cells occur, nor do we know freshly settled sponges was carried out by the whether the bipolar cells differentiate from the labelled streptavidin-biotin method (LSAB kit; spherical type. Ifthese serotonergic cells are part DAKO). Histochemical staining of peroxidase ofan integrative system, both cellular commun­ with amino-ethyl-carbazole (AEC, substrate ication at a distance (spherical ceIls) or cell-eell buffer) was used to enhance visibility of the contacts (bipolar ceIls) could be expected. labelled cells. DISCUSSION RESULTS Our study is the tirst to report serotonergic cells Tedania ignis has a parenchymella larva in Demospongiae, a spherical type in both larva composed oftwo types ofcells (Bergquist et al., and post-metamorphosed sponge, and a second 1979). PeripheraIly, flagellated epithelium-like bipolar cell type that is exclusive to the post­ cells coyer the organism. This "epithelium" is larval developing organism . Up to now, monociliated and 10-25 J..lm high. The free­ serotonin was only demonstrated histo­ swimming larva exhibits coordinated ciliary chemically in myocyte-like cells ofCalcarea (see action. A distinct basal lamina and typical below). Among the most primitive Eumetazoa, eumetazoan apical junctional complexes are serotonin is weIl known to act as a neuro­ apparently lacking (but see below). Interior, appar­ transmitter (e.g. in Anthozoa, Umbriaco et al., ently motile mesenchymal cells (mesohyl ceIls) 1990). ActuaIly, 5-HT has a wide range of are arranged beneath the epithelium-like sheath functions in invertebrates, such as control of (Woollacott, 1990, 1993; Amano & Hori, 1994) regeneration processes in Planaria (Kimmel & (Fig. lA). The live larvae are ovoid and have a Carlyon, 1990) and ofbeat ofcilia in echinoderm size of 700-900J..lm long, 500-600J..lm wide, but embryo (Mogami et al., 1992), and as inhibitors the necessary Triton X-100 treatment weakens and activators of muscle of molluscs (Welsh, the cell membranes and larvae usually shrink and 1953; Twarog, 1988). As in Porifera, members of collapse (Fig. lA, B). In the juvenile, settled the phylum Placozoado not differentiate nerve or sponge to(}-- as in the' adult-the exopinacoderm muscle cells and are therefore counted among the which covers the ectosome acts as the protective most primitive eumetazoans (GreIl, 1974; Ax, layer. Inside the sponge, choanocyte chambers 1989; GreIl &, Ruthmann, 1991). Schuchert connected by canals lined with endopinacocytes (1993) demonstrated in Trichoplax adherens SEROTONIN IN PORIFERA ? 661 FIG. 1. Tedania ignis, histology of larva. A, Longitudinal section of an entire larva stained by toluidin blue showing epithelial-like celllayer (e) and dark-staining cells (archaeocytes, arrow) in c1usters near the posterior pole CP) (scale bar=lOOJlm). B, Serotonin-positive cells (s) are randomly distributed in the larval body; at least 6 c1usters of2-4 labelled cells are evident (one marked, asterisk). The nucleus in sorne ofthe cells is visible as a non-fluorescent region (arrow).
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