Tealia Nematocyst Toxin Purification Abstract—A toxin from the nematocysts of the anemone Tealia crassicornis has been partially purified. The toxin is nondialyzable, of molecular weight greater than 3500, and is heat labile, i.e. inactivated after heating for 30 minutes at 100°0. The LD is estima- ted to be the toxin from 2:3 X 10° nematocysts per kg of the crab, Pachygrapsus crassipes. This correspon- ded to 3-68mg of protein per kg of crab. INTRODUCTION Nematocyst toxin studies were revolutionized when Phillips and Abbott (1957) developed "a method of obtaining purified suspen- sions of nematocysts from sea anemones (Actiniaria) in order to obtain a toxic preparation which could be considered nema- tocyst in origin..." Blanquet (1968) isolated mainly acontial microbasic mastigophore nematocysts from the sea anemone Aip- tasia pallida and found that the toxin caused leg autonomy and death in fiddler crabs; Hessinger and Lenhoff (1973a,b 1974a,b) found that it also affected ionic conductance in crayfish giant nerve fibers. Shapiro (1968a,b) used whole tentacle extracts from the sea anemone Condylactis gigantea and found that the -1- Tealia Nematocyst Toxin Purification extract caused rigid paralysis and death in crayfish, and af- fected the firing of all classes of lobster and crayfish axons, probably due to the toxin interacting with the nerve membrane ionic conductance. Tealia crassicornis (Muller, 1776), a brightly colored red and green sea anemone of Central California was used in this study. There have been no investigations of toxins from this animal. The predominant nematocyst types of T. crassicornis are basitrichs and microbasic p-mastigophores, along with spi- rocysts. The toxic extract from isolated, discharged nemato- cysts was characterized and assayed for toxicity in the crab, Pachygrapsus crassipes (Randall, 1839) by injection. MATERIALS AND METHODS T. crassicornis was collected subtidally from kelp beds off Hopkins Marine Station in Pacific Grove, California. The method reported by Phillips (1956) with several modifications was employed inthe isolation of undischarged nematocysts from the whole anemone. Three types of isolating media were used, 1MSodium Citrate in distilled water, 1MSucrose in O-45/Umilli- pore filtered sea water, and a combination of the two where -2- Tealia Nematocyst Toxin Purification the primary isolation was with citrate and the final purifica- tion with sucrose. Figure 1 presents a flow chart describing the isolation and purification procedures. Not all nematocysts were discharged upon addition of dis- tilled water and a hemocytometer was used to estimate the num- ber of nematocysts, both discharged and undischarged, in the extract prior to final centrifugation. A protein determination (Lowry, 1951) was performed before and following final centrifugation using a Bovine Serum Albumin Standard. The amount of protein released per nematocyst was estimated. Toxin assays were performed on the crab, P. crassipes, which is abundant in the rocky intertidal of the Hopkins Marine Station. Crabs ranging in size from 11•0 - 47-3grams were in- jected and maintained in separate containers at 16-18°0 and fresh water was supplied 3-4 times daily. The injection was into the venous sinus accessible in the upper joint of the left leg of the crab. The volume injected ranged from O-055 - 1-5ml. No effect other than death was noted. Toxin in distilled water and toxin in Crustacean Ringer's solution (Pantin, 1934) were compared. Control injections of distilled water and Crustacean Ringer's were included in the toxin assays. Toxin in Crustacean Ringer's was obtained by dissolving the toxin in this solution after concentrating distilled water pre- -3- Tealia Nematocyst Toxin Purification parations by evaporation under vacuum at 30°0. Toxin preparations were freed of isolation medium contam- inants by dialysis using Spectrapor Membrane Tubing (Spectrum Medical Industries, Inc.) against Crustacean Ringer's at 400. Thermolability of the toxin was determined by heating at 100°0 for 30 minutes in a boiling water bath. Molecular size of the toxin was estimated using gel fil- tration on BioGel P-100 (Bio Rad Laboratories) at 50-150 mesh. The effect of the toxin on the circumesophageal connective nerve of the lobster, Homarus americanus, was tested. The nerve was placed over a series of chloride coated silver wires with a plastic container in the middle for the Crustacean Ringer's. Stimulation was given upstream and propagated action potentials recorded downstream from the Crustacean Ringer's. The Crustacean Ringer's was then replaced by the toxin and action potentials a- gain recorded. The recordings themselves were made with P8A.C. pre-amplifiers (Grass Instrument). The outputs were viewed on a Tektronix 502 oscilliscope and permanent recordings before and after the change to toxic extract were made on photographic film. (Kao and Fuhrman, 1967). The stimulus was set at 8volts, duration 0•82msecs., frequency 8°6pulses per sec., and 20volts per om sen¬ sitivity. -4- Tealia Nematocyst Toxin Purification RESULTS Nematocyst Isolation Using the sodium citrate as an isolation medium, 7•5 X io nematocysts were isolated from 500ml. of anemone. Of the total number, 36% were dischargeable upon treatment with distilled water; in the sodium citrate with final washing in sucrose, 1•94 X 10' nematocysts were isolated, 32% were dischargeable; and with the use of sucrose throughout isolation, 7°8 X 10°ne- matocysts were obtained with 40% dischargeable. Toxic Extract from Purified Nematocysts The toxic preparation obtained from nematocysts isolated using sodium citrate alone contained 1e5mg of protein per ml re¬ leased from 9.0 X 102 nematocysts per ml. or 1-67 X 10-2Ug of protein per nematocyst. Toxin prepared from nematocysts iso- lated using sucrose in the final washing contained 2•8mg of pro- tein per ml. released from 2•0 X 10° nematocysts per ml. or 1•4 X 10 JUg of protein per nematocyst. The amount of protein released per nematocyst for preparations obtained using sucrose alone was not determined. These preparations were assayed for toxicity at one or two dose levels. The results are presented in Table 1. All toxin preparations caused death of the assay animal. The lack of such response at the lower dose level of -5- Tealia Nematocyst Toxin Purification namatocysts prepared with sucrose above may indicate a slight difference in relative toxicity. The time to death of crabs injected with the toxin in Crustacean Ringer's appears to be somewhat shorter than for distilled water preparations. Dial- ysis against Crustacean Ringer's did not result in a loss of toxicity indicating that the molecular size of the toxin is greater than 3500. Heat treatment destroyed toxicity. The LD of the toxin from citrate prepared nematocysts and dialyzed against Crustacean Ringer's was estimated by tes- ting groups of three crabs at the following dilutions: full strength, 32/100, 1/10, 32/1000, and 1/100. The LD appears to be close to an amount of toxin present in 2'3 X 10° nemato¬ cysts or 3-68mg of protein per kg of crab. Gel filtration resulted in the separation of the protein into two fractions, one with a molecular size excluded and, therefore, larger than 100,000, the other, a smaller sized molecular component greater than the marker, cytochrome C, of molecular weight 12,270, utilized in the fractionation. Neither of these preparations could be shown to possess the toxicity alone, although the high molecular weight component seemed to produce an anesthetic effect on all injected crabs. As is shown in Figure 2, the high molecular weight fraction appears to block axonal conductance when tested on the circumesophageal connective nerve of the lobster. -6- Tealia Nematocyst Toxin Purification DISCUSSION Nematocysts from the sea anemone T. crassicornis have been isolated, their discharge collected and tested for tox- icity. An injection of 1°25 X 10' nematocysts per kg of crab, P. crassipes, or about 20mg. of protein per kg crab generally produced death. The approximate LDgo of 2:3 X 10° nematocysts per kg P. crassipes, or 3°68mg protein per crab, was about 1/3000 as toxic as that observed by Shapiro (1967) for Condyl- actis gigantea using the crayfish as an assay animal. Due to the pore size used in dialysis, the molecular weight must be greater than 3500 because upon injection after dialysis, death was still evident. That the toxin is proteinaceous seems likely when molecular size is considered along with thermolability. Fur- ther investigation is required to elucidate the effect of the tox- in on axonal conduction. Acknowledgements—A thank-you is not enough for the untiring patience, guidance, and advice shown to me by Dr. F.A. Fuhrman and Dr. J.H. Phillips, Jr. Not only did they make this investigation possible, but they gave me something much more meaningful -- a better understanding of the way in which all true "pursuers of knowledge" must reason and act. -7- e Tealia Nematocyst Toxin Purification LITERATURE CITED Blanquet, R., 1968. Properties and Composition of the Nemato- Toxin of the Sea Anemone, Aiptasia Pallida. Comp. Bio- chem. Physiol., 25:893-902. Kao, C.Y. and Fuhrman, F.A., 1967. Differentiation of the Ac- tions of Tetrodotoxin and Saxitoxin. Toxicon, 5:25. Lowry, O.H., Rosenbrough, N.J., Farr, A.L., and Randall, R.J, 1951. Protein Measurement with the Folin phenol reagent. J. Biol. Chem., 193:265-272. Phillips, J.H., 1956. Isolation of Active Nematocysts of Metri¬ dium Senile and Their Chemical Compositions. Nature, London, 178:93 Phillips, J.H., and Abbott, D.P., 1957. Isolation and Assay of the Nematocyst Toxin of Metridium Senile Fimbriatum. Bio. Bull., 113, No.2:296-301. Shapiro, B.I., 1968. Purification of a Toxin from Tentacles of the Anemone Condylactis Gigantea. Toxicon, 5:253-259. Shapiro, B.I. and Lilleheil, G., 1969. The Action of Anemone Toxin on Crustacean Neurons, Comp. Biochem. Physiol., 28:1225-1241. -8- 0 Tealia Nematocyst Toxin Purification FIGURE CAPTIONS Figure 1 Procedure for the isolation of toxin from purified nematocysts. Figure 2 Effect of the toxin on axonal conductance of the circumesopha- geal connective nerve of a lobster, Homarus americanus. Axonal conductance before the toxin was added. (a) (b) Axonal conductance 2 minutes following the replacement of Crustacean Ringer's by the toxin. Axonal conductance 4 minutes following the replacement of (c) Crustacean Ringer's by the toxin. I VOLUME IM SODIUM CITRATE IN DISTILLED WATER I VOLUME T. CRASSICORNIS (500 ml.) OR I VOLUME IM SUCROSE IN 0-45 U MILLIPORE FILTERED SEA WATER MACERATE IN WARING BLENDER (APPROXIMATELY 15 MINUTES) FILIER THROUGH CHEESECLOTH WITH VACUUM DISCAD EESOUE FILTRATE (NEMATOCYSTS, TISSUE, CITRATE OR SUCROSE CENTRIFUGE (15 MINUTES, 5°c, 750G) DISCARD SUPERNATANT WASH, RESUSPEND, AND RECENTRIFUGE IN IM SODIUM CITRATE OR IM SUCROSE UNTIL SUPERNATANT CLEAR DRAIN THOROUGHLY, RINSE RESIDUAL ISOLATION MEDIUM FROM INSIDE SURFACE OF CENTRIFUGE TUBE WITHOUT DISTURBING PELLET DISCHARGE NEMATOCYSTS BY ADDING A VOLUME OF DISTILLED WAIER APPROXIMATELY EQUINALENT TO PELLET VOLUME, LET STAND 12-18hrs. CENTRIFUGE (2000 G, 15 MINUTES) DISCAR0 PELET ERNAL FIGURE 1 Simulus stimulus G. h. ARA Figure 2 e Tealia Nematocyst Toxin Purification TABLE CAPTIONS Table 1 Results of nematocyst toxicity using the crab, Pachygrapsus crassipes. e ISOLATION MEDIUM sucrose sucrose citrate citrate/ sucrose ontrol/ distilled water ISOLATION MEDIUM citrate citrate/ sucrose control/ Crustacean Ringer s TOXIN IN DISTILLED WATER DOSE PER KG. CRAE INJECTION nematocyst no. mg. protein (volume:ml) .O5mi/iog- 1.O X 10 O.lml O.5ml/iog- 1.05 X 10 1.O5ml .O5m1/iog- O.27mg 1.7 X 10 .187m1 .O5m1/iog- O.65mg 5.O X 10 O.24m1 O.5mi/iog- O. Omg O.O 1.08m1 TOXIN IN CRUSTACEAN RINGER'S DOSE PER KG. CRAB INJECTION mg. protein nematocyst no. (volume:ml) O.l1mg 6.8 X 10 O.O5ml/iog- .O8m1 1.2 X 10 .O5ml/iog- O.16mg O.O6ml O.O O.5mi/iog- O. Omg O.88m1 CRAB WEIGHT 19.9g 21.0g 37.Ag 47.38 21.6g CRAB WEIGHT 15.0g 11.og 17.6g TIME TO LEATH 36hrs. 3éhrs. 36hrs. TIME TO DEATH 24hrs. 24hrs. TABLE ro ISOLATION MEDIUM citrate citrate citrate/ sucrose control/ Crustacean Ringer's ISOLATION MEDIUM citrate INJECTION (volume:ml) .O5m1/iog- .081m1 O. 5ml/iog- .67m1 .O5ml/iog- .81m1 O.5ml/log- .12m1 INJECTION (volume:ml) .O5m1/iog- .O7m1 DIALYZED TOXIN LOSE PER KG. CRAB mg. protein nematocyst no. 7.3 X 10 O.12mg O.96mg 6.0 X 102 O.31mg 2.4 X 100 O. Omg O.O TOXIN AFTER HEATING DOSE PER KG. CRAB mg. protein nematocyst no. 6.3X 10 O. 1mg CRAB WEIGHT 16.2g 13.4g 24.Ag 16.2g CRAB WEIGHT 13.2g TIME TO DEATH 12hrs. 12hrs. 12hrs. TIME TO DEATH TABLE 1 (CONT