Abstract
Biosynthesis of toxins uses precious cellular energy and it would seem unlikely that evolution would be forgiving enough to tolerate wasted metabolism. Although there is much debate about this proposition in the guise of secondary vs primary metabolites (1,2), it is a reasonable hypothesis that toxins of all kinds should play some beneficial role. This return is apparent when one considers toxins used for prey capture or self-defense as occurs with venoms. For microbial neurotoxins, however, the identity of this biological profit remains a mystery. This is especially so when one considers that the microbes that manufacture these toxins, and those microorganisms that surround them, do not possess nerves nor many of the molecular systems that characterize nerves. The few exceptions to this rule are those microbial toxins that attack generic cellular systems common to many cell types, including nerve cells. An example is the dinoflagellate toxin okadaic acid, an inhibitor of certain serine-threonine protein phosphatases, enzymes that occur widely in different cell types in animals and plants as well as microorganisms (3–5). In fact, an okadaic acid sensitive form of this enzyme has been isolated from the dinoflagellate, Prorocentrum lima, an established producer of okadaic acid (6).One can hypothesize then that okadaic acid may act as a physiological regulator of this enzyme within the dinoflagellate itself or upon unrelated microbes in its vicinity. The larger mystery lies with microbial neurotoxins that attack cellular and molecular neural processes not present in microbes.
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References
Vining, L. C. (1992) Secondary metabolism, inventive evolution and biochemical diversity: a review. Gene 115, 135–140.
Stone, M. J. and Williams, D. H. (1992) On the evolution of functional secondary metabolites (natural products). Mol. Microbiol. 6, 29–34
Takai, A., Murata, M., Torigoe, K., Isobe, M., Mieskes, G., and Yasumoto, T. (1992) Inhibitory effect of okadaic acid derivatives on protein phosphatases. Biochem. J. 284, 539–544.
Haystead, T. A., Sim, A. T., Carling, D., Honnor, R. C., Tsukitani, Y., Cohen, P., and Hardie, D. G. (1989) Effects of the tumour promoter okadaic acid on intracellular protein phosphorylation and metabolism. Nature 337, 78–81.
Solow, B., Young, J. C., and Kennelly, P. J. (1997) Gene cloning and expression and characterization of a toxin-sensitive protein phosphatase from the methanogenic archaeon Methanosarcina thermophila TM-1. J. Bacteriol. 179, 5072–5075.
Boland, M. P., Taylor, M. F., and Holmes, C. F. (1993) Identification and characterisation of a type-1 protein phosphatase from the okadaic acid-producing marine dinoflagellate Prorocentrum lima. FEBS Lett. 334, 13–17.
Sugiyama, H. (1980) Clostridium botulinum neurotoxin. Microbiol. Rev. 44, 419–448.
Pellizzari, R., Rossetto, O., Schiavo, G., and Montecucco, C. (1999) Tetanus and botulinum neurotoxins: mechanism of action and therapeutic uses. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 354, 259–268.
Park, D. L. (1995) Surveillance programmes for managing risks from naturally occurring toxicants. Food Addit. Contam. 12, 361–371.
Margulis, L. and Schwartz, K. V. (1998) Five Kingdoms: An Illustrated Guide to the Phyla of Life of Earth. W. H. Freeman and Co., San Francisco, CA.
Llewellyn, L. E. (2000) Shellfish chemical poisoning, in Foodborne Diseases Handbook, vol. 4, Seafood and Environment Toxins ( Hui, Y. H., Kitts, D. D., and Stanfield, P. S., eds.), Marcel Dekker, New York, NY, pp. 77–108.
Lewis, R. J. and Holmes, M. J. (1993) Origin and transfer of toxins involved in ciguatera. Comp. Biochem. Physiol. C. 106, 615–628.
Baden, D. G. (1989) Brevetoxins: unique polyether dinoflagellate toxins. FASEB J. 3, 1807–1817.
Humpage, A. R., Rositano, J., Bretag, A. H., Brown, R., Baker, P. D., Nicholson, B. C., and Steffensen, D. A. (1994) Paralytic shellfish poisons from Australian cyanobacterial blooms. Aust. J. Mar. Freshwat. Res. 45, 761–771.
Schantz, E. J., Lynch, J. M., Vayvada, G., Matsumoto, K., and Rapoport, H. (1966) The purification and characterization of the poison produced by Gonyaulax catenella in axenic culture. Biochemistry 5, 1191–1195.
Kodama, M., Ogata, T., Sakamoto, S., Sato, S., Honda, T., and Miwatani, T. (1990) Production of paralytic shellfish toxins by a bacterium Moraxella sp. isolated from Protogonyaulax tamarensis. Toxicon 28, 707–714.
Kodama, M., Sato, S., Sakamoto, S., and Ogata, T. (1996) Occurrence of tetrodotoxin in Alexandrium tamerense, a causative dinoflagellate of paralytic shellfish poisoning. Toxicon 34, 1101–1105.
Noguchi, T., Jeon, J. K., Arakawa, O., Sugita, H., Deguchi, Y., Shida, Y., and Hashimoto, K. (1986) Occurrence of tetrodotoxin and anhydrotetrodotoxin in Vibrio sp. isolated from the intestines of a Xanthid crab, Atergatis floridus. J. Biochem. 99, 311–314.
Devlin, J. P., Edwards, O. E., Gorham, P. R., Hunter, N. R., Pike, R. K., and Stravic, B. (1977) Anatoxin-a, a toxic alkaloid from Anabaena floc-aquae NRC-44h. Can. J. Chem. 55, 1367–1371.
Matsunaga, S., Moore, R. E., Niemczura, W. P., and Carmichael, W. W. (1989) Anatoxin-a(s), a potent anticholinesterase from Anabaena floc-aquae. J. Am. Chem. Soc. 111, 8021–8023.
Bates, S. S., Bird, J. C., De Freitas, A. S. W., Foxall, R., Gilgan, M., Hanic, L. A., et al. (1989) Pennate diatom Nitzschia pungens as the primary source of domoic acid, a toxin in shellfish from eastern Prince Edward Island, Canada. Can. J. Fish. Aquat. Sci. 46, 1203–1221.
Do, H. K., Kogure, K., and Simidu, U. (1990) Identification of deep-sea-sediment bacteria which produce tetrodotoxin. Appl. Environ. Microbiol. 56, 1162–1163.
Kodama, M., Ogata, T., Sato, S., and Sakamoto, S. (1990) Possible association of marine bacteria with paralytic shellfish toxicity of bivalves. Mar. Ecol. Prog. Ser. 61, 203–206.
Matsui, T., Taketsugu, S., Kodama, K., Ishii, A., Yamamori, K., and Shimizu, C. (1989) Production of tetrodotoxin by the intestinal bacteria of a puffer fish Takifugu niphohles. Bull. Jap. Soc. Sci. Fish 55, 2199–2203.
Kodama, M., Ogata, T., and Sato, S. (1988) Bacterial production of saxitoxin. Agric. Biol. Chem. 52, 1075–1077.
Matsumura, K. (1995) Reexamination of tetrodotoxin production by bacteria. Appl. Environ. Microbiol. 61, 3468–3470.
Falconer, I. R. (1998) Algal toxins and human health, in Handbook of Environmental Chemistry, vol. 5, Part C, Quality and Treatment of Drinking Water II ( Hrubec, J., ed.), Springer Verlag, Berlin, Heidelberg, pp. 53–82.
Negri, A. P., Jones, G. J., and Hindmarsh, M. (1995) Sheep mortality associated with paralytic shellfish poisons from the cyanobacterium Anabaena circinalis. Toxicon 33, 1321–1329.
Sommer, H. and Meyer, K. F. (1937) Paralytic shellfish poisoning. Arch. Pathol. 24, 560–598.
Wright, J. L. C., Falk, M., McInnes, A. G., and Walter, J. A. (1990). Identification of isodomoic acid D and two new geometrical isomers of domoic acid in toxic mussels. Can. J. Chem. 68, 22–25.
Schantz, E. J., Ghazarossian, V. E., Schnoes, H. K., Strong, F. M., Springer, J. P., Pezzanite, J. O., and Clardy, J. (1975) The structure of saxitoxin. J. Am. Chem. Soc. 97, 1238–1239.
Tsuda, K., Ikuma, S., Kawamura, M., Tachikawa, R., and Sakai, K. (1964) Tetrodotoxin. VII. On the structure of tetrodotoxin and its derivatives. Chem. Pharm. Bull. 12, 1357–1374.
Goto, T., Kishi, Y., Takahashi, S., and Hirata, Y. (1965) Tetrodotoxin. Tetrahedron 21, 2059–2088.
Woodward, R. B. (1964) The structure of tetrodotoxin. Pure Appl. Chem. 9, 49–74.
Koskinen, A. M. P. and Rapaport, H. (1985) Synthetic and conformational studies on anatoxin-a: a potent acetylcholine agonist. J. Med. Chem. 28, 1301–1309.
Matsunaga, S., Moore, R. E., Niemczara, W. P., and Carmichael, W. W. (1989) Anatoxin-a(s), a potent anticholinesterase from Anabaena flos-aquae. J. Am. Chem. Soc. 111, 8021–8023.
Lin, Y., Risk, M., Ray, S. M., van Engen, D., Clardy, J., Golik, J., James, J. C., and Nakanishi, K. (1981) Isolation and structure of brevetoxin B from “red tide” dinoflagellate Ptychodiscus brevis (Gymnodinium breve). J. Am. Chem. Soc. 103, 6773–6776.
Murata, M., Legrand, A. M., Ishibashi, Y., and Yasumoto, T. (1989) Structures of ciguatoxin and its congener. J. Am. Chem. Soc. 111, 8929–8931.
Chang, F. H., Anderson, D. M., Kulis, D. M., and Till, D. G. (1997) Toxin production of Alexandrium minutum (Dinophyceae) from the Bay of Plenty, New Zealand. Toxicon 35, 393–409.
Oshima, Y. (1995) Postcolumn derivatization liquid chromatographic method for paralytic shellfish toxins. J. AOAC Int. 78, 528–532.
Oshima, Y., Blackburn, S. I., and Hallegraeff, G. M. (1993) Comparative study on paralytic shellfish toxin profiles of the dinoflagellate Gymnodinium catenatum from three different countries. Mar. Biol. 116, 471–476.
Betz, J. L., Brown, P. R., Smyth, M. J., and Clarke, P. H. (1974) Evolution in action. Nature 247, 261–264.
Satin, J., Limberis, J. T., Kyle, J. W., Rogart, R. B., and Fozzard, H. A. (1994) The saxitoxin/tetrodotoxin binding site on cloned rat brain IIa Na channels is in the trans-membrane electric field. Biophys. J. 67, 1007–1014.
Lipkind, G. M and Fozzard, H. A. (1994) A structural model of the tetrodotoxin and saxitoxin binding site of the Na+ channel. Biophys. J. 66, 1–13.
Strichartz, G. (1984) Structural determinants of the affinity of saxitoxin for neuronal sodium channels. Electrophysiological studies on frog peripheral nerve. J. Gen. Physiol. 84, 281–305.
Atchison, W. D., Luke, V. S., Narahashi, T., and Vogel, S. M. (1986) Nerve membrane sodium channels as the target site of brevetoxins at neuromuscular junctions. Br. J. Pharmacol. 189, 731–738.
Lombet, A., Bidard, J. N., and Lazdunski, M. (1987) Ciguatoxin and brevetoxins share a common receptor site on the neuronal voltage-dependent Na+ channel. FEBS Lett. 219, 355–359.
Jeglitsch, G., Rein, K., Baden, D. G., and Adams, D. J. (1998) Brevetoxin-3 (PbTx-3) and its derivatives modulate single tetrodotoxin-sensitive sodium channels in rat sensory neurons. J. Pharmacol. Exp. Ther. 284, 516–525.
Huang, J. M., Wu, C. H., and Baden, D. G. (1984) Depolarizing action of a red-tide dinoflagellate brevetoxin on axonal membranes. J. Pharmacol. Exp. Ther. 229, 615–621.
Sheridan, R. E. and Adler, M. (1989) The actions of a red tide toxin from Ptychodiscus brevis on single sodium channels in mammalian neuroblastoma cells. FEBS Lett. 247, 448–452.
Biscoe, T. J., Evans, R. H., Headley, P. M., Martin, M., and Watkins, J. C. (1975) Domoic and quisqualic acids as potent amino acid excitants of frog and rat spinal neurones. Nature 255, 166–167.
Michaelis, E. K. (1998) Molecular biology of glutamate receptors in the central nervous system and their role in excitotoxicity, oxidative stress and aging. Prog. Neurobiol. 54, 369–415.
Ozawa, S., Kamiya, H., and Tsuzunki, K. (1998) Glutamate receptors in the mammalian central nervous sytem. Prog. Neurobiol. 54, 581–618.
Adams, D. J., Dwyer, T. M., and Hille, B. (1980) The permeability of endplate channels to monovalent and divalent metal cations. J. Gen. Physiol. 75, 493–510.
Sargent, P. B. (1993) The diversity of neuronal nicotinic acetylcholine receptors. Annu. Rev. Neurosci. 16, 403–443.
Swanson, K. L., Allen, C. N., Aronstam, R. S., Rapoport, H., and Albuquerque, E. X. (1986) Molecular mechanisms of the potent and stereospecific nicotinic receptor agonist (+)-anatoxin-a. Mol. Pharmacol. 29, 250–257.
Hyde, E. G. and Carmichael, W. W. (1991) Anatoxin-a(s), a naturally occurring organo-phosphate, is an irreversible active site-directed inhibitor of acetylcholinesterase (EC 3.1.1.7). J. Biochem. Toxicol. 6, 195–201.
Dyer, J. R., Johnston, W. L., Castellucci, V. F., and Dunn, R. J. (1997) Cloning and tissue distribution of the Aplysia Na+ channel alpha-subunit cDNA. DNA Cell. Biol. 16, 347–356.
Spafford, J. D., Spencer, A. N., and Gallin, W. J. (1998) A putative voltage-gated sodium channel alpha subunit (PpSCN1) from the hydrozoan jellyfish, Polyorchis penicillatus: structural comparisons and evolutionary considerations. Biochem. Biophys. Res. Commun. 244, 772–780.
Jeziorski, M. C., Greenberg, R. M., and Anderson, P. A. (1997) Cloning of a putative voltage-gated sodium channel from the turbellarian flatworm Bdelloura candida. Parasitology 115, 289–296.
Guy, H. R. and Durell, S. R. (1995) Structural models of Nat Ca’, and K+ Fhannels. Soc. Gen. Physiol. Ser. 50, 1–16.
Heinemann, S. H., Terlau, H., Stuhmer, W., Imoto, K., and Numa, S. (1992) Calcium channel characteristics conferred on the sodium channel by single mutations. Nature 356, 441–443.
Lee, R. Y., Lobel, L., Hengartner, M., Horvitz, H. R., and Avery, L. (1997) Mutations in the alpha subunit of an L-type voltage-activated Cat+ channel cause myotonia in Caenorhabditis elegans. EMBO J. 16, 6066–6076.
Le Paslier, M. C., Pierce, R. J., Merlin, F., Hirai, H., Wu, W., Williams, D. L., et al. (2000) Construction and characterization of a Schistosoma mansoni bacterial artificial chromosome library. Genomics 65, 87–94.
Myler, P. J., Audleman, L., deVos, T., Hixson, G., Kiser, P., Lemley, C., et al. (1999) Leishmania major Friedlin chromosome 1 has an unusual distribution of protein-coding genes. Proc. Natl. Acad. Sci. USA 96, 2902–2906.
Mongan, N. P., Baylis, H. A., Adcock, C., Smith, G. R., Sansom, M. S., and Sattelle, D. B. (1998) An extensive and diverse gene family of nicotinic acetylcholine receptor alpha subunits in Caenorhabditis elegans. Receptors Channels 6, 213–228.
Maricq, A. V., Peckol, E., Driscoll, M., and Bargmann, C. I. (1995) Mechanosensory signalling in C. elegans mediated by the GLR-1 glutamate receptor. Nature 378, 78–81.
Maclntyre, J. G., Cullen, J. J., and Cembella, A. D. (1997) Vertical migration, nutrition and toxicity in the dinoflagellate Alexandrium tamarense Mar. Ecol. Prog, Ser. 148, 201–216.
Ogata, T., Ishimura, T., and Kodama, M. (1987) Effect of water temperature and light intensity on growth rate and toxicity change in Protogonyaulax tamarensis. Mar. Biol. 95, 217–220.
Selvin, R. C., Lewis, C. M., Yentsch, C. M., and Hurst, J. W. (1984) Seasonal persistence of resting cyst toxicity in the dinoflagellate Gonyaulax tamarensis var. excavata. Toxicon 22, 817–820.
Oshima, Y., Bolch, C. J., and Hallegraeff, G. M. (1992) Toxin composition of resting cysts of Alexandrium tamarense (Dinophyceae). Toxicon 30, 1539–1544.
Stevens, D. K. and Krieger, R. I. (1991) Stability studies on the cyanobacterial nicotinic alkaloid anatoxin-A. Toxicon 29, 167–179.
Boczar, B. A., Beitler, M. K., Liston, J., Sullivan, J. J., and Cottolico, R. A. (1988) Paralytic shellfish toxins in Protogonyaulax tamarensis and Protogonyaulax catanella in axenic culture. Plant Physiol. 88, 1285–1290.
Subba Rao, D. V., De Freitas, A. S. W., Quilliam, M. A., Pocklington, R., and Bates, S. S. (1990) Rates of production of domoic acid, a neurotoxin amino acid in the pennate marine diatom Nitzschia pungens, in Toxic Marine Phytoplankton ( Graneli, E., Sundstrom, B., Edler, L., and Anderson, D. M. eds.), Elsevier, New York, NY, pp. 413–417.
Fersht, A. (1985) Enzyme Structure and Mechanism. W.H. Freeman, New York.
Herbert, R. A. (1999) Nitrogen cycling in coastal marine ecosystems FEMS Microbiol. Rev. 23, 563–590.
Rapala, J., Sivonen, K., Luukkainen, R., and Niemala, S. I. (1993) Anatoxin-a concentration in Anabaena and Aphanizomenon under different environmental conditions and cornparison of growth by toxic and non-toxic Anabaena-strains: a laboratory study. 1 Appl. Phycol. 5, 581–591.
Bumke-Vogt, C., Mailahn, W., Rotard, W., and Chorus, I. (1996) A highly sensitive analytical method for the neurotoxin anatoxin-a, using GC-ECD, and first application to laboratory cultures. Phycologia 35 (Suppl. 6), 51–56.
Anderson, D. M. and Cheng, T. P. (1988) Intracellular localization of saxitoxins in the dinoflagellate Gonyaulax tamarensis. J. Phycol. 24, 17–22.
Hallegraeff, G. M. (1993) A review of harmful algal blooms and their apparent global increase. Phycologia 32, 79–99.
Teegarden, G. J. (1999) Copepod grazing selection and particle discrimination on the basis of PSP toxin content. Mar. Ecol. Prog. Ser. 181, 163–176.
Teegarden, G. J. and Cembella, A. D. (1996) Grazing of toxic dinoflagellates, Alexandrium spp., by adult copepods of coastal Maine: implications for the fate of paralytic shellfish toxins in marine food webs. J. Exp. Mar. Biol. Ecol. 196, 145–176.
Haney, J. F., Sasner, J. J., and Ikawa, M. (1995) Effects of products released by Aphanizomenonflos-aquae and purified saxitoxin on the movements ofDaphnia carinata feeding appendages. Limnol. Oceanogr. 40, 263–272.
Ishida, H., Muramatsu, N., Kosuge, T., and Tsuji, K. (1996) Study of neurotoxic shellfish poisoning involving New Zealand shellfish, Crassostrea gigas, in Harmful and Toxic Algal Blooms ( Yasumoto, T., Oshima, Y., and Fukuyo, Y., eds.). UNESCO, Paris, pp. 491–494.
Trudeau, L. E. and Castellucci, V. F. (1993) Excitatory amino acid neurotransmission at sensory-motor and interneuronal synapses of Aplysia californica. J. Neurophysiol. 70, 1221–1230.
Fieber, L. A. (1998) Characterization of Na+ and Cat+ currents in bag cells of sexually immature Aplysia californica. J. Exp. Biol. 201, 745–754.
Twarog, B. M., Hidaka, T., and Yamaguchi, H. (1972) Resistance to tetrodotoxin and saxitoxin in nerves of bivalve molluscs. A possible correlation with paralytic shellfish poisoning. Toxicon 10, 273–278.
Kvitek, R. G. and Beitler, R. M. (1991) Relative insensitivity of butter clam neurons to saxitoxin: a pre-adaptation for sequestering paralytic shellfish poisoning toxins as a chemical defense. Mar. Ecol. Prog. Ser. 69, 47–54.
Satin, J., Kyle, J. W., Chen, M., Bell, P., Cribbs, L. L., Fozzard, H. A., and Rogart, R. B. (1992) A mutant of TTX-resistant cardiac sodium channels with TTX-sensitive properties. Science 256, 1202–1205.
Wohlgeschaffen, G. D., Mann, K. H., Subba Rao, D. V., and Pocklington, R. (1992) Dynamics of the phycotoxin domoic acid: accumulation and excretion in two commercially important bivalves. J. Appl. Phycol. 4, 297–310.
Sheumack, D. D., Howden, M. E., Spence, I., and Quinn, R. J. (1978) Maculotoxin: a neurotoxin from the venom glands of the octopus Hapalochlaena maculosa identified as tetrodotoxin. Science 199, 188–189.
Sheumack, D. D., Howden, M. E., and Spence, I. (1984) Occurrence of a tetrodotoxinlike compound in the eggs of the venomous blue-ringed octopus (Hapalochlaena maculosa). Toxicon 22, 811–812.
Flachsenberger, W. and Kerr, D. I. (1985) Lack of effect of tetrodotoxin and of an extract from the posterior salivary gland of the blue-ringed octopus following injection into the octopus and following application to its brachial nerve. Toxicon 23, 997–999.
Hwang, D. F., Arakawa, O., Saito, T., Noguchi, T., Simidu, U., Tsukamoto, K.,et al. (1989) Tetrodotoxin-producing bacteria from the blue-ringed octopus Octopus maculosus. Mar. Biol. 100, 327–332.
Sommer, H. (1932) The occurrence of the paralytic shellfish poison in the common sand crab. Science 76, 574–575.
Noguchi, T., Konosu, S., and Hashimoto, Y. (1969) Identity of the crab toxin with saxitoxin. Toxicon 7, 325–326.
Noguchi, T., Uzu, A., Koyama, K., Maruyama, J., Nagashima, Y., and Hashimoto, K. (1983) Occurrence of tetrodotoxin as the major toxin in a Xanthid crab Atergatis floridus. Bull. Jpn. Soc. Sci. Fish. 49, 1887–1892.
Daigo, K., Noguchi, T., Miwa, A., Kawai, N., and Hashimoto, K. (1988) Resistance of nerves from certain toxic crabs to paralytic shellfish poison and tetrodotoxin. Toxicon 26, 485–490.
Yamamori, K., Yamaguchi, S., Maehara, E., and Matsui, T. (1992) Tolerance of shore crabs to tetrodotoxin and saxitoxin and antagonistic effect of their body fluid against the toxins. Bull. Jap. Soc. Sci. Fish. 58, 1157–1162.
Llewellyn, L. E. (1997) Haemolymph protein in xanthid crabs: its selective binding of saxitoxin and possible role in toxin bioaccumulation. Mar. Biol. 128, 599–606.
Noguchi, T., Hwang, D. F., Arakawa, O., Sugita, H., Deguchi, Y., Shida, Y., and Hashimoto, K. (1987) Vibrio alginolyticus, a tetrodotoxin-producing bacterium, in the intestines of the fish Fugu vermicularis vermicularis. Mar. Biol. 94, 625–630.
Yotsu, M., Yamazaki, T., Meguro, Y., Endo, A., Murata, M., Naoki, H., and Yasumoto, T. (1987) Production of tetrodotoxin and its derivatives by Pseudomonas sp. isolated from the skin of a pufferfish. Toxicon 25, 225–228.
Matsumura K. (1995) Tetrodotoxin as a pheromone. Nature 378, 563–564.
Kodama, M., Sato, S., Ogata, T., Suzuki, Y., Kaneko, T., and Aida, K. (1986) Tetrodotoxin secreting glands in the skin of puffer fishes. Toxicon 24, 819–829.
Fritz, L., Quilliam, M. A., and Wright, J. L. C. (1992) An outbreak of domoic acid poisoning attributed to the pennate diatom Pseudonitzschia australis. J. Phycol. 28, 439–442.
Scholin, C. A., Gulland, F., Doucette, G. J., Benson, S., Busman, M., Chavez, F. P., et al. (2000) Mortality of sea lions along the central California coast linked to a toxic diatom bloom. Nature 403, 80–84.
Geraci, J. R., Anderson, D. M. Timperi, R. J., St. Aubin, D. J., Early, G. A., Prescott, J. H., and Mayo, C. A. (1989) Humpback whales (Megaptera novaeangliae) fatally poisoned by dinoflagellate toxin. Can. J. Fish. Aquat. Sci. 46, 1895–1898.
Davis, C. G. (1947) Gymnodinium breve, n. Sp. A cause of discolored water and animal mortality in the Gulf of Mexico. Bot. Gaz. 109, 358–360.
Bossart, G. D., Baden, D. G., Ewing, R. Y., Roberts, B., and Wright, S. D. (1998) Brevetoxicosis in manatees (Trichechus manatus latirostris) from the 1996 epizootic: gross, histologic, and immunohistochemical features. Toxicol. Pathol. 26, 276–282.
Saimi, Y., Martinac, B., Delcour, A. H., Minorsky, P. V., Gustin, M. C., Culbertson, M. R., et al. (1992) Patch clamp studies of microbial ion channels. Methods Enzymol. 207, 681–691.
Oami, K., Naitoh, Y., and Sibaoka, T. (1995) Voltage-gated ion conductances correspoding to regenerative positive and negative spikes in the dinoflagellate Noctiluca miliaris. J. Comp. Physiol. A 176, 625–633.
Andrivon, C. (1988) Membrane control of ciliary movement in ciliates. Biol. Cell 63, 133–142.
Liu, J. Z., Dapice, M., and Khan, S. (1990) Ion selectivity of the Vibrio alginolyticus flagellar motor. J. Bacteriol. 172, 5236–5244.
Hirota, N. and Imae, Y. (1983) Na+-driven flagellar motors of an alkalophilic Bacillus strain YN-1. J. Biol. Chem. 258, 10577–10581.
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Llewellyn, L.E. (2002). Ecology of Microbial Neurotoxins. In: Massaro, E.J. (eds) Handbook of Neurotoxicology. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-59259-132-9_13
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