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6. Palytoxin in Two Species of Philippine Crabs

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6. PALYTOXIN IN TWO SPECIES OF PHILIPPINE CRABS Takeshi YASUMOTO and Daisuke YASUMURA Faculty of Agriculture, Tohoku University, Tsutsumi-dori, Amemiyamachi, Sendai, Miyagi 980, Japan Yasushi OHIZUMI and Masami TAKAHASHI Mitsubishi-Kasei Institute for Life Science, 11 Minamiooya, Machida-shi, Tokyo 194, Japan Angel C. ALCALA and Lawton C. ALCALA Department of Zoology, Silliman University, Dumaguete City 6501, The Philippines ABSTRACT Two species of xanthid crab Lophozozymus pictor and Demania a1ca1ai collected on southern Negros, Philippines, were found to be highly lethal by mouse assays. The toxin in both species was indistinguishable from pa1ytoxin, a highly lethal toxin of zoanthids Pa1ythoa spp., in chroma­ tographic properties, lethal potencies and in ultraviolet absorption spectra. INTRODUCTION In tropical Pacific areas widespread rumors exist regarding the occurrence of toxic crabs (KONOSU and HASHIMOTO, 1978). The species most frequently implicated in human intoxication is Zosimus aeneus in which occurrence of saxitoxin analogues (HASHIMOTO, 1979; YASUMOTO et a1., 1981; KOYAMA et a1., 1981; RAJ et a1., 1983) and, more recently, tetrodotoxin (YASUMURA et a1., in press) have been confirmed. However, toxic principles in other crabs implicated in poisoning incidences have remained unidentified. TEH and GARDINER (1974) first reported the presence of a potent toxin in Lophozo­ zymus pictor and suggested the toxin to be different from both saxitoxin and tetrodotoxin on the basis of dose-death time relation ships and gel permeation chromatographic properties. Incidence of human fatalities due to ingestion of this species was reported on Negros Island, Philippines (GONZALES and ALCALA, 1977; ALCALA, 1983). In the same area, a human fatality resulting from ingestion of another species Demania toxica also took place (ALCALA and -45- HALSTEAD, 1970) and a related species Demania a1ca1ai was shown to be highly lethal (CARUMBANA et a1., 1976). We now report isolation of a toxin from specimens of L. pictor and D. a1ca1ai collected in Negros Island, Philippines. As resem­ blence between the crab toxin and palytoxin, a highly potent toxin of zoanthids, was recognized at the early stage of investigation, emphasis was laid to prove the identity of the two toxins. MATERIALS AND METHODS Materials Four specimens of Lophozozymus pictor and two specimens of Demania a1ca1ai were collected at Negros Island, Philippines, during the period from Nov. 1982 to May 1983. They were frozen immediately after catch and kept at -20°C until use for extraction. Reference palytoxin was generously donated by Professors D. UEMURA of Shizuoka University and Y. HIRATA of Meijo University. Purification Pulverized crabs were extracted with twice volume (v/w) of methanol 5 times at room temperature and the combined extracts were evaporated to dryness. The residue was suspended in water, freed of lipids with diethyl ether, and the toxin was extracted with I-butanol. The toxic residue obtained after evaporation of I-but­ anol was successively treated on columns of TSK G3000S (Toyosoda, 2.8 x 5 cm), DEAE-Sephadex A-25 (Pharmacia, 2.8 x 40 cm) and CM­ Sephadex C-25 (Pharmacia, 1 x 20 cm) following the method for puri­ fication of palytoxin described by HIRATA et a1. (1979). Purifi­ cation on the DEAE-Sephadex and CM-Sephadex columns were repeated twice. Further purification of the toxin was carried out by high performance liquid chromatography (HPLC) on Develosil ODS-I0/20 column (Nomura Kagaku, 2 x 25 cm) with alternative use of the following two solvents: methanol-O.lN acetic acid (8:2) and aceto­ nitrile-0.05N acetic acid (5:5). Separation of the toxin was monitored by mouse assays and with a UV-spectromonitor (Japan Spectroscopic Co., UVIDEC-I00-II) at wavelength 263 nm. Comparison of the toxin with reference palytoxin by HPLC was carried out on an ERC ODS-1282 column (Erma Optical Works, 0.6 x 25 cm) with the aforementioned two solvents and on a TSK G3000SW column (Toyosoda, 0.75 x 60 cm) using 0.03N acetic acid as eluant. Thin layer chromatography (TLC) TLC was carried out on Silica gel 60 and NH2F254s plates (Merck, precoated) with two different solvent systems: l-amyl­ alcohol-py.ridine-water( 7: 7: 6) and pyridine-water-l-butanol-acetic acid (10:12:15:13). The toxin on Silica gel 60 plates was detected by heating the plates after spraying sulfuric acid, and that on NH2- F254s plates by exposure to UV light (254 nm). -46- Bioassay of toxin A bioassay method proposed by TEH and GARDINER (1974) for the toxin in L. pictor was employed. Groups of 3 male mice of ddY strain with body weight of 17 g were injected intraperitoneally with suitable volumes of sample solutions and the death times noted Toxin amounts in mouse unit (MU) was calculated from the equation Y = 225.19 X-0 •99 • Spectra UV spctra were taken in aqueous solution with a Hitachi 124 spectrophotometer. RESULTS In all the chromatographic experiments, the toxin in L. pictor and D. a1ca1ai were indistinguishable from palytoxin. Chromato­ grams of the crab toxin on columns of DEAE-Sepahdex and CM-Sephadex superimposed on those of palytoxin are shown in Figs. 1 and 2. Separation of the toxin from buffer salts are achievable on the TSK G3000S polystyrene gel column, which retained the toxin from aqueous solutions and released it with 75% ethanol in a similar manner described for palytoxin by HIRATA et a1. (1979). As shown in Fig. 3, the retention times for the crab toxin on an ERC ODS- 1282 column are identical with that of palytoxin with two different solvent systems. The crab toxin is also indistinguishable from palytoxin in gel permeation chromatography on a TSK G3000SW column (Fig. 3). Thin layer chromatography on two different types of plates using two solvent systems does not distinguish the toxin (Fig. 4). Like palytoxin the crab toxin exhibits absorption maxima at 233 and 263 nm in UV spectra. Molecular extinction coefficients at 263 nm were 23,570 for the toxin of L. pictor and 19,600 for the toxin of D. a1ca1ai, if we assume the crab toxin to have the same molecular weight (2,680 dalton) with palytoxin. These values are compatible with that reported for palytoxin (MOORE et a1., 1975). All these data unamimously support that the toxin isolated from L. pictor and D. a1ca1ai is palytoxin. The amounts of pure toxin isolated from L. pictor and D. a1ca1ai a1ca1ai were 1.0 and 0.8 mg, respectively. The lethal potency as measured by the mouse assay method of TEH and GARDINER (1974) was 0.5 pg/kg for individual toxin samples. The value is compatible with that measured on the reference palytoxin. The toxin contents of crabs and anatomical distribution of the toxin in the body are summarized in Table 1. All specimens tested ar~ lethal. One specimen of D. a1ca1ai contained as high as 1.2 x 10 MU of the toxin in the body. The toxin was found in all the tissue and organs but higher concentration was found in gills and the viscera consisting of the liver and gonad. Chelipeds, espe­ cially the flesh, were low in lethal potency. Eggs of L. pictor showed the highest toxin level in the body. -47- DISCUSSION The results obtained in this study strongly indicate that the toxic principle in L. pietor and D. alealai is palytoxin. Al­ though further confirmation by ordinary spectral analysis, e.g. H NMR spectrometry, was unattainable due to the extremely large molecular size of palytoxin, C129H223N3054, supportive data were obtained by OHIZUMI and TAKAHASHI (unpublished) who found pharma­ cological properties of the crab toxin to be identical with those of palytoxin previously reported by OHIZUMI and SHIBATA (1980). To our best knowledge the present study is the first to evidence the occurrence of palytoxin in crabs and to confirm its implica­ tion in human intoxication. It is not certain at present whether the toxin in crabs is of endogenous or exogenous origin. It is likely, however, that crabs accumulate the toxin by feeding on Palythoa spp., which were commonly seen in the sampling areas. In four specimens. the stomachs were empty and in two specimens only skeletons of unidentified crastacea and sponges were recognized in the stomach. Effort will be continued to test the occurrence of remnants of zoanthids in the stomach of crabs. The extremely high lethal potency of the crabs is worth to note and urges that people should be well informed of the potential danger of the crabs. The case report for a human fatality caused by ingestion of D. toxiea (ALCALA and HALSTEAD, 1970) suggests that the causative toxin was also palytoxin. Effort is being made to obtain specimens of D. toxiea for analysis. REFERENCES ALCALA, A.C. and HALSTEAD, B.W. (1970) Human fataly due to inges­ tion of the crab Demania sp. in the Philippines. Clin. Toxieol., 3, 609. ALCALA, A.C. (1983) Recent cases of crab, cone shell, and fish in­ toxication on southern Negros Island, Philippines, Toxieon, Suppl., 3, 1. CARUMBANA, E.E., ALCALA, A.C. and ORTEGA, E.P. (1976) Toxic marine crabs in southern Negros, Philippines. , 23, 265 GONZALES, R.B. and ALCALA, A.C. (1977) Fatalities from crab poi­ soning on Negros Island, Philippines. Toxieon, 15, 169. HASHIMOTO, Y. (1979) Marine Toxins and Other Bioactive Marine Metabolites. Tokyo: Japan Scientific Societies Press. HIRATA, Y., UEMURA, D., UEDA, K. and TAKANO, S. (1979) Several compounds from Palythoa tubereulosa (Coelenterata). Pure Appl. Chem. 51, 1875. MOORE, R.E., DIETRICH, R.F., HATTON, B., HIGA, T. and SCHEUER, P.J. (1975). The nature of the 263 chromophore in the palytoxins. J. Org. Chem., 40, 540. -~- KONOSU, S. and HASHIMOTO, Y. (1978) Venoms of crastacea and merostomata.
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  • Co-Occurrence of Tetrodotoxin and Saxitoxins and Their Intra-Body Distribution in the Pufferfish Canthigaster Valentini

    Co-Occurrence of Tetrodotoxin and Saxitoxins and Their Intra-Body Distribution in the Pufferfish Canthigaster Valentini

    toxins Article Co-Occurrence of Tetrodotoxin and Saxitoxins and Their Intra-Body Distribution in the Pufferfish Canthigaster valentini Hongchen Zhu 1, Takayuki Sonoyama 2, Misako Yamada 1, Wei Gao 1, Ryohei Tatsuno 3, Tomohiro Takatani 1 and Osamu Arakawa 1,* 1 Graduate School of Fisheries and Environmental Sciences, Nagasaki University. 1-14, Bunkyo-machi, Nagasaki, Nagasaki 852-8521, Japan; [email protected] (H.Z.); [email protected] (M.Y.); [email protected] (W.G.); [email protected] (T.T.) 2 Shimonoseki Marine Science Museum. 6-1, Arcaport, Shimonoseki, Yamaguchi 750-0036, Japan; [email protected] 3 Department of Food Science and Technology, National Fisheries University, Japan Fisheries Research and Education Agency. 2-7-1, Nagatahonmachi, Shimonoseki, Yamaguchi 759-6595, Japan; tatsuno@fish-u.ac.jp * Correspondence: [email protected]; Tel.: +81-95-819-2844 Received: 9 June 2020; Accepted: 2 July 2020; Published: 3 July 2020 Abstract: Pufferfish of the family Tetraodontidae possess tetrodotoxin (TTX) and/or saxitoxins (STXs), but the toxin ratio differs, depending on the genus or species. In the present study, to clarify the distribution profile of TTX and STXs in Tetraodontidae, we investigated the composition and intra-body distribution of the toxins in Canthigaster valentini. C. valentini specimens (four male and six female) were collected from Amami-Oshima Island, Kagoshima Prefecture, Japan, and the toxins were extracted from the muscle, liver, intestine, gallbladder, gonads, and skin. Analysis of the extracts for TTX by liquid chromatography tandem mass spectrometry and of STXs by high-performance liquid chromatography with post-column fluorescence derivatization revealed TTX, as well as a large amount of STXs, with neoSTX as the main component and dicarbamoylSTX and STX itself as minor components, in the skin and ovary.