Tetrodotoxinproducing Bacteria From the Blueringed Octopus Octopus Maculosus

Blue-Ringed Octopus

Utilisation of compounds from venoms in drug discovery

Carol M. Trim , ... Steven A. Trim , in Progress in Medicinal Chemistry, 2021

1.2.8 Other venomous species

The blue-ringed octopus ( Hapalochlaena fasciata) (Fig. 1A) has tetrodotoxin (TTX) in its venom which causes pain and neurotoxic effects (paralysis) by inhibiting signal transduction by nerve cells through sodium channel blockade [75]. This toxin is synthesised by bacteria and is also found in other several species, for example in pufferfish and salamanders. Even sponges can cause pain and swelling, fire sponges are an example (Tedania spp.) [76]. Sea urchins trigger an inflammatory reaction and can cause tissue necrosis and muscular paralysis in some and the crown-of thorns starfish (Acanthaster planci) venom has strong haemolytic activity [77].

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Venomous and Poisonous Invertebrates

Rosalind Dalefield BVSc PhD DABVT DABT , in Veterinary Toxicology for Australia and New Zealand, 2017

Organisms That Employ Tetrodotoxin

Organisms in Australian waters that use tetrodotoxin include the blue-ringed octopus ( Hapalochlaena spp.) and the sea slug (Pleurobranchaea maculata) as well as blowfish, pufferfish, and toadfish (family Tetraodontidae, which includes the genera Arothron, Canthigaster, Chelonodon, Contusus, Feroxodon, Lagocephalus, Marilyna, Omegophora, Polyspina, Reicheltia, Sphoeroides, Tetractenos, Tetraodon, Torquigener, Tylerius). In New Zealand, tetrodotoxin poisoning is most commonly a result of dogs eating sea slugs that have washed up on beaches, but some species of pufferfish are found in New Zealand waters and also pose a hazard to dogs if washed ashore.

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Food additives

Michael Zeece , in Introduction to the Chemistry of Food, 2020

Tetrodotoxin

Tetrodotoxin is a potent neurotoxin found in pufferfish, porcupinefish, and blue-ringed octopus. The toxin is produced by bacteria species such as Vibrio alginolyticus and Pseudomonas tetraodonis. Bacteria live symbiotically in these marine and freshwater animals. Pufferfish, also known as blowfish or fugu, are one of the most dangerous foods eaten. The poison is a very potent neurotoxin that blocks sodium ion channels and prevents brain signals from activating muscle contraction. The toxin is concentrated in the liver and sex organs of pufferfish. If the fish is improperly prepared, tetrodotoxin can contaminate the meat of the fish. Eating low doses of the toxin causes tingling sensations in the mouth fingers and toes. Higher doses produce nausea, vomiting, and respiratory failure. Lethality of this tetrodotoxin is similar to that of cyanide poisoning. Death can be caused by ingesting as little as 1   mg of the toxin. Tetrodotoxin also has an interesting pharmaceutical application as an agent to manage pain in cancer patients. Low doses of tetrodotoxin also block signals in nerve fibers responsible for pain.

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Introduction

Ramasamy Santhanam Former Dean , in Biology and Ecology of Venomous Marine Scorpionfishes, 2019

The geographical locations of human fatalities from marine animal envenomation are given below.

Venomous marine animal	Affected area
Blue-ringed octopus	Australia, Singapore
Cone shell	Australia, Fiji, India (Banda), New Caledonia, Japan (Okinawa), Vanuatu
Sea snake	Burma, Malaysia, India (Madras), Indonesia (Java), Japan (Okinawa), Oman, Vietnam
Stingray	California, Colombia, Fiji, New Zealand, Surinam, Texas
Stonefish	Australia (Thursday Island), East Africa, Japan, Seychelles

Source: Fenner, 2004.

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Hazards and Diseases

K. Campbell , S Haughey , in Encyclopedia of Food Safety, 2014

Occurence of Tetrodotoxin

Tetrodotoxin now has been found in a wide genre of species. Other marine organisms have been found to store tetrodotoxin and include the Australian blue-ringed octopus ( Hapaloclaena maculosa, which uses tetrodotoxin as a toxin for capturing prey), parrot fish, triggerfish, goby, angelfish, boxfish (Ostracion spp.), tobies, porcupine fish, molas or ocean sunfish, globefish, seastars, starfish (Astropecten scoparius), xanthid crabs (Eriphia spp.), a horseshoe crab (Carcinoscorpius rotundicauda), two Philippine crabs (Zosimus aeneus and Atergatis floridus), a number of marine snails, flatworms, sea squirts, several nemerteans (ribbonworms), and several species of Chaetognatha (arrow worms), which use tetrodotoxin as a venom for prey, molluscs (Nassarius spp. and the Japanese trumpet shell Boshubora), and marine algae (Jania spp.). Terrestrial organisms include the Harlequin frogs (Atelopus spp.), Costa Rican frog (Atelopus chiriquiensis), three species of California newt (Taricha spp.), and members of the Salamandridae (salamanders). The number of species found to contain tetrodotoxin continues to grow (Figure 3).

Figure 3. Examples of other species known to contain tetrodotoxin.

It is unlikely that these tetrodotoxin-bearers possess a common gene that codes for tetrodotoxin production. The ecologic environments of tetrodotoxin-bearing animals seem to have no common factor other than being closely related to an aquatic system. Bacteria, omnipresent organisms that commonly inhabit the aquatic system, are implicated as the primary source of tetrodotoxin. The bacteria believed to be involved are Shewanella alga (Figure 4), Vibrio species, Alteromonas species, and Pseudomonas species and their proposed mechanism of tetrodotoxin accumulation in marine animals was described by Noguchi and Arakawa using the flow chart (Figure 5).

Figure 4. Shewanella alga.

Figure 5. Flow diagram of mechanism of tetrodotoxin accumulation. Reproduced from Noguchi T and Arakawa O (2008) Tetrodotoxin – Distribution and accumulation in aquatic organisms, and cases of human intoxication. Marine Drugs 6: 220–242.

Therefore, the tetrodotoxin of puffer fish is not endogenous (produced by the puffer fish itself), but exogenous (taken from outside and accumulated) via the food chain. It has been suggested that the puffer fish accrue tetrodotoxin as a biological defense agent. There appears to be a symbiotic association between tetrodotoxin-producing bacteria and higher organisms, which offers distinct advantages to both partners. The bacteria have a host as a safe place to live, eat, and reproduce whereas the host uses the toxin for predation or defense or both. The normal visual defense mechanism for slow-swimming and clumsy pufferfishes is their ability to inflate to several times their normal size by swallowing air when threatened, and tetrodotoxin may be an inadvertent weapon. Generally, they are left alone by predators.

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Marine Toxins and Assorted Biological Toxins

Elijah W. Stommel M.D., PH.D. , Michael R. Watters M.D. , in Current Therapy in Neurologic Disease (Seventh Edition), 2006

TETRODOTOXIN

Tetrodotoxin is produced by marine bacteria and may be found in some (but not all) pufferfish as well as the California newt; frogs of the genus Atelopus ; the blue-ringed octopus; and some species of starfish, parrotfish, angelfish, gastropod mollusks and xanthid crabs. An initial feeling of lightness or floating is generally followed by gastrointestinal distress. These symptoms are followed by increasing paralysis with loss of limb and brainstem reflexes and respiratory compromise. Gastric lavage and activated charcoal are often helpful if given early in the course of the poisoning. No antidote exists, and treatment is supportive, with attention to cardiopulmonary support.

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Toxic Neuropathies

Patrick M. Grogan , Jonathan S. Katz , in Clinical Neurotoxicology, 2009

Tetrodotoxin-related Neuropathy

Tetrodotoxin is an exceptionally potent sodium channel blocker that is found in high concentrations in the skin and viscera of tetraodontiform fish, including puffer fish (Fugu poecilonotus) and porcupine fish (Diodon hystrix), as well as in blue-ringed octopus (Hapalochlaena maculosa) and certain amphibians (Figure 14-3). ^{87, 88} The toxin is best recognized in tales of fatal poisonings following ingestion of improperly prepared fugu, an expensive Japanese delicacy of raw puffer fish that should only be eaten when prepared by a specially licensed chef.

Tetrodotoxin poisoning causes a rapidly progressive sensorimotor polyneuropathy that may affect bulbar and respiratory muscles. Acral and perioral paresthesias and sensory loss develop within minutes to hours of ingestion. ^{87, 88} Limb weakness develops soon after and may result in flaccid quadriparesis. ⁸⁸ Autonomic neuropathy symptoms, including hyperhydrosis, excessive salivation, hypotension, bradycardia, and temperature dysregulation, are common. Clinical severity depends on the amount of the toxin ingested, and it is recommended that the skin, liver, gonads, and intestines be avoided as these tissues contain the greatest concentrations of toxin. ⁸⁹

The underlying pathophysiology of tetrodotoxin poisoning relates to sodium channel blockade that impairs propagation of the nerve action potential. This conduction abnormality can be detected by electrophysiological studies that disclose evidence of profound sensorimotor conduction velocity slowing (less than 30 m/sec for upper extremities and less than 23 m/sec for lower extremities) without conduction block or temporal dispersion. ⁸⁸ Prolonged terminal motor and F wave latencies are typically the most notable electrodiagnostic features. ⁸⁸ Sensory nerve action potential amplitudes may be mildly reduced, but motor studies retain normal amplitudes and morphology. These abnormalities gradually resolve as the toxin clears.

Treatment is supportive, and recoveries may be dramatic. The literature contains examples of rapid improvements from a dense quadriparesis with respirator dependency back to normal, provided adequate supportive care is initiated early. ^{87, 88}

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Self-Defense

Michael D. Breed , Janice Moore , in Animal Behavior (Third Edition), 2022

Aposematism

Chemical deterrents can be used before or after a predator's attack. Poisons, along with repellants, are effective. They can favor the evolution of aposematic coloration, in which a brightly colored, easy-to-remember appearance, when combined with the disastrous experience of tangling with such a noxious prey, causes predators to avoid an animal with that appearance in the future. Aposematism (Greek, apo = away, sematic = sign) is the use of warning coloration to inform potential predators that an animal is poisonous, venomous, or otherwise dangerous. Oftentimes orange or red patterns may be warnings (as in coral snakes), but do not assume that red is always a warning (see Chapter 7). Examples of warning colors and patterns are shown in Figure 10.16.

Figure 10.16. Three examples of potentially aposematic coloration. Right: A toxic tetrio sphinx caterpillar. This caterpillar may also mimic the color pattern of a coral snake! Center: The seed-feeding bug (family Coreidae) has red and yellow patterning that may warn that it contains toxins. Left: The poison frog is mildly toxic and certainly stands out against the monotonous greens and browns of the rainforest.

Photos: left and center, Michael Breed; right, Jeff Mitton.

The blue-ringed octopus combines startle behavior and aposematism to warn away predators. When disturbed, this venomous octopus can flash iridescent blue rings at the rate of three flashes per second. The blue rings are patches of special cells called iridophores; they contain layers that reflect light in the form of iridescent colors. The rapid flashes are the result of muscular contraction and relaxation of pouches of skin that surround the iridophores; when the pouch opens, there is a flash. And that is the true story of how the blue-ringed octopus got its flashing blue rings. ²⁵ The so-called "disco" clam (Ctenoides ales) has a similar strategy. When threatened by mantis shrimp predators, the clam opens and exposes colorful tissues to the predator while flashing. The flashes are not bioluminescent, but the result of reflective silica. Mantis shrimp are fearsome predators (stomatopods), and the clam uses chemical defenses along with the display to ward off the stomatopods. ⁹⁵ The flash of fireflies attracts mates, but it may also advertise the fact that many fireflies are noxious. ⁹⁶ When fireflies were painted to conceal their flashing abdomens, bats did not learn to avoid them as readily.

Although many foul-tasting prey are aposematic, some animals use chemical defense as a last resort and do not advertise it. This seems to be true in the well-camouflaged silkmoth caterpillars. When discovered and attacked, they emit a series of clicks using their mandibles, accompanied by regurgitation of deterrent liquid. This phenomenon was first discovered by neuroethologist Jayne Yack, ²⁶ who brought caterpillars home with her when no one was on campus to care for them. In truth, it was first discovered by Yack's cat, who was, in turn, discovered (by Yack) gagging in the presence of a caterpillar and its regurgitant. This led to a series of experiments that confirmed the hypothesis that both acoustic aposematic signals and chemical deterrents are used by these caterpillars when camouflage fails. (The cat, which gagged for years thereafter any time it saw a similar caterpillar, also seemed to confirm the hypothesis.)

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Nitrogen-Containing Metabolites from Marine Bacteria

William H. Gerwick , Namthip Sitachitta , in The Alkaloids: Chemistry and Biology, 1999

H VIBRIO

A Vibrio sp. isolated from the Okinawan sponge Hyrtios altum was grown in seawater medium to produce an antibiotic EtOAc extract (58). Bioassay guided isolation yielded two antibiotic substances, the diketopiperazine brevianamide F ( 62 ) and a new compound, trisindoline ( 63 ). Its structure was formulated from various spectrochemical data, with HMBC data providing the critical link between the indole subunits.

Marine Vibrio sp. are producers of the well-known neurotoxin, tetrodotoxin (TTX, 46 ), first obtained from the internal organs of puffer fish, and subsequently isolated from a variety of vertebrates and invertebrates. This was first demonstrated with an isolate from the intestines of the xanthid crab, Atergatis floridus (59). Culture of a suspension of intestinal materia] in enriched ½-strength seawater yielded a Vibriosp. as one of the dominant bacteria. Extracts of both the cell mass, as well as the culture material, were analyzed by HPLC and showed peaks corresponding to TTX and anhydro-TTX. Alkaline hydrolysis of these collected materials, conversion to the corresponding trimethylsilyl derivative, and analysis by GCMS confirmed the identities of these two toxins. Subsequently, a Vibrio alginolyticus was cultured from the intestines of the puffer fish, Fugu vermicularis vermicularis, the traditional source of TTX, and was shown by methods similar to those described above to produce both TTX and anhydro-TTX, as well as a possible epimeric substance, in a ½-strength seawater-based culture medium (60).

Additional isolates of TTX-producing bacteria have been made from a starfish, the 'blue-ringed octopus', and the 'lined moon snail'. Strains of V. alginolyticus, V. damsela, and a Staphylococcus sp. isolated from intestines of the starfish Astropecten polyacanthus were found to produce TTX (61). Similarly, TTX production was demonstrated from 2 strains of Alteromonas, 2 strains of Bacillus, and strain each of Vibrio and Pseudomonas isolated from various tissues of Philippine and Japanese specimens of the 'blue-ringed octopus', Octopus maculosus (62). More recently, V. alginolyticus and Aeromonas spp. were isolated from the digestive gland and muscle of the Taiwanese 'lined moon snail', Natica lineata, and shown to produce TTX or related substances (63).

Vibrio parahaemolyticus was cultured from dilutions of the stress-induced ichthyotoxic mucus of the box fish Ostracion cubicus (64). The EtOAc extract of the enriched NaCl-containing medium (2.5   g/L) was chromatographed over silica gel to give two indolic compounds, the known natural product 2,2-di(3-indolyl)-3-indolone ( 64 ), and a new indole dimer named 'vibrindole' ( 65 ). The structure of the new substance was developed from ID and 2D NMR arguments in combination with MS information. Both compounds gave appreciable zones of inhibition to Gram positive bacteria at 100   µg/disk.

The fish pathogen Vibrio anguillarum was the source of a fundamentally new class of siderophore, anguibactin ( 66 )(65). Production of this substance is closely tied to virulence of this bacterium. Culture of the organism was accomplished in a minimal medium containing a non-assimilable iron chelator (66). Isolation of anguibactin from culture medium was by absorption onto XAD-7 resin, elution with MeOH, and then partial purification on Sephadex LH-20 (67). This was followed by repetitive silica gel chromatography and an additional Sephadex LH-20 step to yield pure anguibactin ( 66 ). A derivative, anhydroanguibactin ( 67 ), was produced via acetylation of anguibactin, and formed crystals from EtOH/Et₂O suitable for X-ray analysis. This analysis, in concert with NMR and MS analyses of anguibactin itself, allowed formulation of its unique, modified peptide, structure. It appears to derive from histidine, cysteine, and 2,3-dihydroxybenzoic acid subunits, with basic atoms in each subunit (o-hydroxy group, thiazoline N, hydroxamate, deprotonated N of imidazole) contributing to metal ligation.

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Occurrence of Natural Toxins in Seafood

Samanta S. Khora , Soumya Jal , in Microbial Contamination and Food Degradation, 2018

3.1 Species Commonly Inhibiting TTX

After TTX was isolated from newts, several other organisms were also reported to produce this toxin. Most of the TTX bearers belong to diverse Phyla, which is prompted to consider the possibility of its origin to be exogenous. Organisms reported to contain TTX are pufferfish: Takifugu rubripes, T. pardalis, T. obscurus (Tani, 1945); gobies: Yongeichthys criniger (Noguchi and Hashimoto, 1973), Y. nebulosus (Lin et al., 2000); newts: T. torosa (Mosher et al., 1964), Cynops ensicauda, Cynops pyrrhogaster (Yasumoto et al., 1988); frogs: Atelopus varius varius, Atelopus chiriquiensis (Kim et al., 1975), Atelopus oxyrhynchus (Yotsu et al., 1992a); horseshoe crab: Carcinoscorpius rotundicauda (Banner and Stephens, 1966); xanthid crab: Atergatis floridus (Noguchi et al., 1983 ); blue-ringed octopus: Hapalochlaena maculosus (Sheumack and Howden, 1978); gastropods: Charonia sauliae (Narita et al., 1981), Natica lineata (Hwang et al., 1990); starfish: Astropecten polyacanthus (Noguchi et al., 1982), Astropecten vappa (Tsai et al., 2004); flatworms: Planocera multitentaculata (Miyazawa et al., 1986), P. reticulate (Jeon et al., 1986); ribbon worms: Lineus fuscoviridis, Tubulanus punctatus (Miyazawa et al., 1988); annelids: Pseudopotamilla occelata (Yasumoto et al., 1989a,b); arrow worms: Eukrohnia hamate, Spadella angulate (Thuesen et al., 1988); red calcareous alga: Jania sp. (Kotaki et al., 1983; Yasumoto et al., 1989a,b); dinoflagellates: Alexandrium tamarense (Kodama et al., 1996); bacteria: Vibrio sp. (Noguchi et al., 1986), Pseudomonas sp. (Yasumoto et al., 1986), Aeromonas (Yang et al., 2010), Bacillus (Wang et al., 2010), Lysinibacillus (Wang and Fan, 2010), Raoultella (Yu et al., 2011), Shewanella (Hien et al., 2011). With its discovery in such vast diversity of organisms, the origin of TTX from the microbial consortium has become a prerogative.

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