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Production of Tetrodotoxin by the Intestinal Bacteria of a Puffer Fish Takifugu Niphobles*1

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Production of Tetrodotoxin by the Intestinal Bacteria of a Puffer Fish Takifugu Niphobles*1 Nippon Suisan Gakkaishi 55(12), 2199-2203 (1989) Production of Tetrodotoxin by the Intestinal Bacteria of a Puffer Fish Takifugu niphobles*1 Takashi Matsui,*2 Shuichi Taketsugu,*2 Kentaro Kodama, *3 Akira Ishii,*3 Kunio Yamamori,*4 and Chiaki Shimizu5(Received August 9, 1989) We surveyed tetrodotoxin (TTX) production on 15 bactria strains isolated from the intestine of a puffer fish caught at Hakatajima, Ehime Prefecture, where the puffer fish is highly toxic. The mouse bioassay revealed that all culture broths were none toxic or very weakly toxic with the ex ception of one strain (code-named SA-4). The SA-4 strain was confirmed for its toxicity by the mouse bioassay, and mice died after showing the characteristic symptoms for TTX intoxication. The amount of toxin was 15 MU in 250ml of culture broth. After bioassays, all the remained solu tions were purified through a Toyopearl HW-40 column, an Amberlite CG-50 column (NH+ form), and a charcoal column. Chromatography of purified toxins demonstrated that 2 strains in addition to SA-4 strain contained TTX and its derivatives in their broths. The cells of SA-4 strain were proved to be lethal to mice, and the existence of TTX was confirmed. The purified toxins and authentic TTX were hydrolyzed to 2-amino-6-hydroxyl-methyl-8-hydroxyquinazoline (C9-base), and converted into its TMS-C9-bases to be analyzed by a GC-MS analyzer. Mass fragment ions m/z 407 and 392, which were specific for TMS-C9-base, appeared in the same retention time. The results from detail examinations done on SA-4 strain led us to the conclusion that SA-4 strain was Schewanella putrefaciens. Despite high toxicity, puffer fish is one of the amounts of TTX and its derivatives in many biota. most valuable fish in Japan on account of its good In fact, Yasumoto et al.6) and Noguchi et al.7) taste. Puffer fish toxin, tetrodotoxin (TTX) has independently confirmed by using the TTX ana a unique chemical structure, shows the specific lyzer that Alteromonas sp. and Vibrio sp. produced action of blocking sodium channels of excitable TTX and anhydTTX, respectively. The situation membranes, and has extensively been studied led us to survey TTX production in bacteria isolat mainly by Japanese researchers. ed from the intestine of puffer fish Takifugu ni Nevertheless, its biogenesis remains obscure. phobles caught at Hakatajima, Ehime Prefecture, We first provided experimental evidence to sug where the puffer fish has highest toxicity as far as gest its exogenous origin in puffer fish, demonstrat we examined in Japan.3) We confirmed that ing the absence of the toxin in cultured puffer fish Shewanella putrefaciens definitely produced TTX and showing the remarkable regional as well as and anhydTTX and that another 2 strains pro individual variation of toxicity.1-3) On the other duced the toxins in small amounts. The present hand, Yasumoto et al. reported the presence of paper deals with these results. anhydrotetrodotoxin (anhydTTX), 4-epi-tetrodo- toxin (4-epiTTX) and tetrodonic acid in addition Materials and Methods to TTX in two species of puffer fish4) and con structed a fluorometric HPLC analyzer (TTX Fish Specimen analyzer) for these compounds.5) The TTX Puffer fish Takifugu niphobles (female; body analyzer made possible the detection of small weight; 55g, toxicity; liver 5, 960 and intestine *1 Studies on the toxification of puffer fish-I.*2 Laboratory of Marine Biochemistry, Faculty of Agriculture, The University of Tokyo, Bunkyo, To kyo 113, Japan(松 居 隆,武次周一:東 京 大 学 農 学 部 水 産 化 学 研 究室). *3 Fermentation Research Laboratories, Sankyo Co., Shinagawa, Tokyo140, Japan(小 玉 健 太 郎,石 井 晃:三 共 株式 会 社〓 酵 研 究 所). *4 School of Fisheries Science, Kitasato University, Sanriku, Iwate O22-O1, Japan(山 森 邦 夫:北 里 大 学 水 産 学 部). *5 Daishin Marine Products Co., Ltd., Showa, Sakaiminato, Tottori684, Japan(清 水 千 秋:株 式 会社 大 伸 水 産). 2200 Matsui, Taketsugu, Kodama, Ishii, Yamamori, and Shimizu Table 1. Composition of the medium for isolation purification was performed through a Toyopearl HW-40 column (2 •~ 100 cm; solvent 0.05N acetic Glucose 5 g Polypeptone (Daigo) 5 g acid). The TTX fractions from HW-40 column were •@ concentrated and put on an Amberlite CG-50 Beef ex. (Difco) 5 g Agar 15 g column (1 •~ 5cm, NH+ form), washed with 10ml Artificial sea water 1,000 ml of water and then eluted with 20ml of 0.5N acetic pH 7.2 acid. The eluate was concentrated and treated with second charcoal column chromatography. The TTX fraction finally obtained was concentrat 3,890 MU/g) was caught by line fishing at Haka ed to 0.5ml and analyzed by a TTX analyzer. tajima in November 1985, fasted for 3 days and The bacteria, code-named SA-4 of which culture transported alive to our laboratory. broth was confirmed to contain TTX and its •@ de rivatives, were harvested by centrifugation from Isolation of Bacteria 1l medium and the bacterial cells were suspended The intestine was removed from the fish, weigh in 0.1 % acetic acid and heated in a boiling bath ed, cut into pieces, and homogenized with several for 10 min. The suspension was centrifuged at volumes of sterilized artificial sea water (Jamarine 10,000 rpm for 20 min and the precipitates were S). After homogenization, the suspension of re-extracted in the same manner. The combined microorganisms was diluted, spreaded with glass supernatants were concentrated to 6ml and the rod on agar medium of which composition is test solutions were checked for TTX or its de shown in Table 1. After incubation for 3-7 days rivatives as mentioned above. at 23•Ž, colonies appearing on the agar plate were •@ divided into several types according to cultural Fluorometric HPLC Analysis and morphological characteristics. Each of them A TTX analyzer, which was developed by Yasu was picked up and streaked on the surface of agar moto et al.5) was used for detection of TTX or its medium for purification. Finally, 15 kinds of derivatives. The mobile phase was prepared by bacteria were isolated from the puffer fish in adding conc. NH4OH to an aqueous solution testine and code-named from SA-1 through SA-15. containing 3% MeCN, 0.005 N heptafluorobutyric acid and 0.05N acetic acid (pH5.0). The flow Fermentation of TTX rates of the mobile phase and of 4N NaOH were A loopful growth of isolates was incubated in a kept at 0.5ml/min. For detecting the fluorescent 500ml Sakaguchi flask containing 100ml of the products, the excitation and emission wavelengths medium which was composed of phytone (BBL) were set at 363 and 510nm, respectively. 10g, artificial sea water 500ml, and distilled water 500ml, pH7.2. The flasks were incubated without GC-MS Spectrography shaking at 26•Ž for 10 to 15 days. Authentic TTX or partially purified toxins from bacteria cells and culture broths, which were con Screening of Toxin from the Culture Borth or firmed to contain TTX by mouse bioassay and by Bacterial Cell the TTX analyzer, were converted into trimethy The culture broths of 15 strains were examined lsilyl(TMS)-2-amino-6-hydroxyl-methyl-8-hydro- for the presence of TTX and its derivatives. The xyquinazoline (C9-base) by the method of Ohtsuka culture broths (250ml each) were acidified to pH et al.9) as follows: TTX or the bacterial toxins were 5.0 with acetic acid and centrifuged at 8,000 rpm. hydrolyzed in 7.4% KOH for 30min in a boiling The supernatant was diluted to 750ml with water water both. The alkali hydrolyzates were neutraliz and then passed through a charcoal column (2 •~ ed with HC•¬ and passed •@ through a C18-SEP-PAC 30cm). After washing the column with 200ml cartridge column. The column was washed with of water, the adsorbate was eluted with 20% EtOH 2ml of water and then 2ml of 20% MeOH. The containing 1% acetic acid. The eluate was eva adsorbed C9-base was eluted with 5ml of MeOH porated, made up to 6ml with water, and used as and concentrated to dryness. The residue was a test solution. One ml of the test solution was dissolved in 50ƒÊl of N, N-dimethylformamide employed for the determination of lethal toxicity (DMF), and then 200 ƒÊl of N,O-Bis(trimethylsily1) to mice according to the standard method de trifluoroacetamide and 10ƒÊl of trimethylchloro scribed in Shokuhin Eisei Kensa Shishin II. 8) silane were added. The reaction mixture was Using remained 5ml of the test solution, further heated at 100•Ž for 30 min in order to convert C9- - TTX Production by Bacteria from a Puffer Fish 2201 base into its TMS derivatives . The TMS-deriva- tives were subjected to GC-MS on a Shimadzu GC- MS QP-1,000 [column: 5% SE-52 (Uniport HP 60-80 mesh), 3 mm •~ 1m, temp. 220-260•Ž (5•Ž/ min); •@ ionization voltage 70V, carrier gas helium 30ml/min]. Identification of Bacteria The media for identification was prepared with artificial sea water. All of the phenotypic char acteristics and DNA base composion were de termined by the method of Kodama et a1.10) Ex traction and purification of quinones were carried out by the method described by Tamaoka et al. 11) Ubiquinone systems and menaquinone systems were determined by HPLC analysis and mass ana lysis, respectively. Results and Discussion Yasumoto et al.6) isolated TTX and anhydTTX from the culture broth of Alteromonas sp. isolated from a red calcareous alga, Jania sp.
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