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Sterols from Six Marine Sponges Elena A Biochemical Systematics and Ecology 32 (2004) 153–167 www.elsevier.com/locate/biochemsyseco Sterols from six marine sponges Elena A. Santalova, Tatyana N. Makarieva, Irina A. Gorshkova, Andrey S. Dmitrenok, Vladimir B. Krasokhin, Valentin A. Stonik ∗ Laboratory of the Marine Natural Products, Pacific Institute of Bioorganic Chemistry of Far Eastern Branch of the Russian Academy of Sciences, Pr. 100-letya Vladivostoka 159, 690022 Vladivostok, Russia Received 30 September 2002; accepted 7 April 2003 Abstract The free sterol fractions from marine sponges Darwinella australiensis, Haliclona sp., Agelas mauritiana, Clathria major, Didiscus aceratus and Teichaxinella labirintica from West- ern Australia were isolated and studied by HPLC, GLC, GLC-MS, and NMR methods. D. australiensis contained ⌬7-, ⌬5-, ⌬5,7-, ⌬5,7,9(11)-sterols, and cholest-7-en-3β-ol was shown to be a main sterol. The free sterols from A. mauritiana proved to be stanols and ⌬7-series compounds, chondrillasterol was identified as a predominant constituent. Haliclona sp. con- tained ⌬5-sterols with cholesterol as a main constituent. C. major and D. aceratus contained ⌬5-sterols, and clionasterol was shown to be a main sterol. T. labirintica was shown to contain 3β-hydroxymethyl-A-nor-sterols. Absolute configurations at C-24 of major sterols from C. major, D. aceratus and A. mauritiana were established by NMR method. Distribution of differ- ent sterols in the studied species was discussed to provide additional viewpoint on the probable application of these natural products as chemotaxonomic markers and to understand biological roles of unusual sterols in sponges using an idea of so-called biochemical coordination. 2003 Elsevier Ltd. All rights reserved. Keywords: Marine sponges; Sterols; Unusual sterols; Didiscus aceratus; Darwinella australiensis; Hal- iclona sp.; Agelas mauritiana; Clathria major; Teichaxinella labirintica ∗ Corresponding author. Tel.: +7-4232-31-1168; fax: +7-4232-31-4050. E-mail address: [email protected] (V.A. Stonik). 0305-1978/$ - see front matter 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0305-1978(03)00143-1 154 E.A. Santalova et al. / Biochemical Systematics and Ecology 32 (2004) 153–167 1. Introduction Sponges have proved to be a rich source of sterols with unusual structural features (Djerassi, 1981; Kerr and Baker, 1991; Baker and Kerr, 1993). It is of special interest that, although some sponge species provide the greatest structural diversity of mem- brane sterols in comparison with any other animals, many of the studied sponges contain the sterol compositions resembling those of animals belonging to other taxa. Why, for example, do some sponge species contain sterol mixtures with a preponder- ance of cholesterol in them, while another group of sponge species have a very complicated sterol mixture, where cholesterol is minor or absent? Why do some sponge species contain only one or two sterol constituents, with these being unusual structures? Do these unusual sterols play the same role in sponge membranes as cholesterol does in higher animals or carry out additional functions? May data con- cerning sterol distribution in sponges be utilized to provide information of value for systematic position of one or other sponge species? We hope that the further studies on sponge sterol compositions and sponge ecology may help to answer these ques- tions. Sterols of Darwinella australiensis, Haliclona sp., Clathria major, Didiscus aceratus and Teichaxinella labirintica have not been previously investigated. Agelas mauritiana from another collection, namely from the Great Barrier Reef of Australia, was previously studied by Berquist et al. (1980). Herein we report hemolytic activi- ties of the studied sponge extracts, the isolation of their free sterol fractions and the investigation of those by HPLC, GLC, GLC-MS, and NMR methods to elucidate sterol compositions. Some suggestions concerning a biological role of sponge sterols differing from cholesterol are given. 2. Materials and methods 2.1. Animals Marine sponges were collected during the 12th scientific cruise of the research vessel “Akademik Oparin” by dredging near the North-Western coast of Australia in November, 1990. Collected sponges were immediately cut, lyophilized and stored at 5 °C. Species identifications were carried out by Mr. V.B. Krasokhin (Pacific Institute of Bioorganic Chemistry, Far Eastern Branch of the Russian Academy of Sciences, Vladivostok, Russian Federation). Voucher specimens (012-103, 012-220, 012-263, 012-216, 012-238, 012-74) are on deposit in Pacific Institute of Bioorganic Chemistry, Far Eastern Branch of the Russian Academy of Sciences, Vladivostok, Russian Federation. 2.2. Extraction and isolation of free sterols Lyophilized sponges were extracted with ethanol at room temperature. Alcoholic extract of each species was evaporated in vacuo to give a dark brown solid. The material was chromatographed using preparative TLC. Obtained sterol fractions were E.A. Santalova et al. / Biochemical Systematics and Ecology 32 (2004) 153–167 155 acetylated with pyridine-Ac2O (1:1), 16 h. Column chromatography of the sterol acetates over a column with silica gel L 40/100µ (Chemapol, the former Czechoslovakia) eluting with the system hexane–ethylacetate (10:0.1) to give the purified sterol fractions. 2.3. Separation of free sterol fractions Free sterols from marine sponges A. mauritiana, D. australiensis and T. labirintica were separated by HPLC analysis using an Altex Ultrasphere-Si column (10 mm × 25 cm) with the system hexane–ethylacetate (5:1) as eluent. All products isolated were monitored as the corresponding acetates by GLC and were analyzed by GLC-MS and NMR. Identification of sterols was possible by comparing their relative retention times (RRT) during GLC on a capillary column with those calcu- lated using separation factors for OV-1 phase from Itoh et al. (1982a), and also by using mass and NMR spectra. Cholesterol (Sigma Grade: 99%), β-sitosterol (Sigma Grade: 98%) and clionasterol, isolated from the sponge Baicalospongia bacilifera (Makarieva et al., 1991) were used as standards. 2.4. Analytical methods GLC analyses were performed on a Sigma 2000 Perkin Elmer chromatograph using a capillary column (50 m × 0.33 mm) with CBP-5 at 290 °C, helium was the carrier gas. GLC-MS analyses were done on Hewlett Packard HP6890 GC System, HP-5MS capillary column (30.0 m × 0.25 mm) at 270 °C, helium was used as the carrier gas, and the ionizing voltage was of 70 eV. 1H NMR spectra were recorded on a Bruker DPX-300 spectrometer in CDCl3 with TMS as an internal standard. HPLC was carried out on a Du Pont Series 8800 Instrument with refractometer index unit RIDK-102 on an ALTEX Ultrasphere-Si column (10 mm × 25 cm) in the system hexane–ethylacetate (5:1). TLC was performed using glass plates (6 × 9 cm) coated with silica gel L 5/40µ (Chemapol, the former Czechoslovakia) in the system chloroform–ethanol (10:0.2) for free sterols. Column chromatography was performed on silica gel L 40/100µ (Chemapol, the former Czechoslovakia) using system hexane–ethylacetate (10:0.1) for sterol acetates. 2.5. Hemolysis Mouse erythrocytes were washed three times using centrifugation (600×g, 5 min) in cold 150 mM NaCl, 10 mM Tris–HCl (pH 7.4). The pellet was resuspended in the same solution to a final concentration of 0.2%. Erythrocytes were incubated with dried residues of ethanol extracts from marine sponges (50–250 µg/ml) for 30 min at room temperature and then centrifuged (600×g, 5 min). Optical densities of super- natants were measured spectrophotometrically at 540 nm. 156 E.A. Santalova et al. / Biochemical Systematics and Ecology 32 (2004) 153–167 Table 1 Classification and area of collection of the species studied Species Taxonomic position Locality of collection Depth (m) Porifera Demospongiae Dendroceratida D. australiensis Darwinellidae 14°04,01 S; 121°56,66 E 10 Agelasida A. mauritiana Agelasiidae 14°7,4 S; 121°45,7 E 35 Haplosclerida Haliclona sp. Haliclonidae 14°03,38 S; 121°46,6 E 15 Poecilosclerida C. major Microcionidae 16°44,5 S; 121°16,6 E 48 Halichondrida D. aceratus Desmoxyidae 14°03,38 S; 121°46,6 E 15 Halichondrida T. labirintica Axinellidae 16°41,4 S; 121°09,6 E 54 3. Results The collected sponges belong to five different orders of the class Demospongiae. Taxonomic positions and geographical coordinates of areas of collection for the spec- ies studied are listed in Table 1. Alcoholic extracts of the sponges collected were tested for hemolytic activities. Results of biotesting showed that extracts of two species (D. australiensis and A. mauritiana) have higher hemolytic properties in comparison with others (Table 2). We isolated free sterol fractions from these sponges and established their sterol compositions by NMR, GLC and GLC-MS methods. Fifty known C26–C29-sterols were identified (Stonik et al., 1998; Kolesnikova et al., 1992; Itoh et al., 1983; Bohlin Table 2 Hemolytic activities of sponge extracts µ Species HD50 ( g/ml) D. australiensis 15 A. mauritiana 50 Haliclona sp. Ͼ100 C. major Ͼ100 T. labirintica Ͼ300 D. aceratus Ͼ500 E.A. Santalova et al. / Biochemical Systematics and Ecology 32 (2004) 153–167 157 et al., 1981; Bonini et al., 1983; Teshima and Patterson, 1981; Delseth et al., 1979) and their structures are presented in Fig. 1. The percentage sterol composition for each species is given in Table 3. 3.1. Darwinella australiensis ⌬5 ⌬7 ⌬5,7 ⌬5,7,9(11) ⌬7 This sponge contained -, -, - and -sterols. C27 sterol was shown to be the main sterol. The ratio of ⌬5:⌬7:⌬5,7:⌬5,7,9(11) compounds was found to be 3:4:1:1, while the ratio of C27:C28:C29 was 8:5:1. 3.2. Agelas mauritiana The fraction from A. mauritiana had stanols, ⌬5- and ⌬7-sterols with chondrillas- terol (Itoh et al., 1982b) as a major sterol. The ratio of stanols:⌬5:⌬7compounds in this sponge was found to be 19:1:15, while the ratio of C27:C28:C29 was Ϸ2:1:1.
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