Gambierdiscus toxicus

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Classification

Higher order taxa

Eukaryota; Dinoflagellata; Dinophyceae; Gonyaulacales; Goniodomataceae; Gambierdiscus

Species

Gambierdiscus toxicus

NCBI: [1]

Description and significance

Gambierdiscus toxicus is a eukaryotic microorganism most notable for its role in causing Ciguatera fish poisoning in humans [2]. It was first discovered by Takeshi Yasumoto and Raymond Bagnis in the late 1970s on the surface of a brown microalgae in the Gambier Islands[2].

G. toxicus produces a ciguatoxin known to be the cause of ciguatera fish poisoning, an illness in humans that occurs when tropical fish containing this toxin are ingested and leads to issues in the human gastrointestinal, cardiac, and neurological systems. In 1986, it was found that between 600 and 2000 G. toxicus cells were sufficient to produce enough toxin to kill a 20-gram mouse in 24 hours, indicating the extremely high toxicity level of ciguatoxins [3].

Genome structure

As of right now, the whole genome of Gambierdiscus toxicus has not yet been sequenced and there is a limited amount of published data on the genetics or proteins of the organism. The ribosomal DNA of Gambierdiscus toxicus shows that the organism is composed of more than four distinct lineages [4]. The chromosomes in the nucleus of G. toxicus are mostly condensed, with 162 x 10-12 grams per cell of DNA [3].

Cell structure

Gambierdiscus toxicus is a species of photosynthetic, unicellular eukaryote that belongs to the Sar (Harosa) and Alveolata clades, defined by the presence of a cortical alveoli and a distinct flagella structure.

There are three different morphological forms of Gambierdiscus toxicus: typical armored cells, deformed cells, and small motile cells and cysts [3]. All these unicellular cell types have a diameter ranging from 50 to 120 µm.

Typical Gambierdiscus toxicus cells are circular in the apical view (at the tip) and flat in the lateral view, with a dorso-ventral diameter averaging 70 µm (60 to 90 µm range) and a vertical diameter of 30-50 µm [3]. These cells have two flagella: a longitudinal flagellum of 50 µm and a transverse flagellum in the cingulum. The eukaryote appears orange brown in its natural habitat of seawater. The outer structure of Gambierdiscus toxicus is a thick theca (membrane complex) or amphiesma composed of an outer membrane, plate layer, dense pellicle, a double membrane, and many trichocystic pores [3]. This unique membranous envelope is used to attach to Jania and other algal host species through a mucus thread [2], and as such, this attachment does not occur in dry environments [5]. The nucleus of the organism is 30 µm in diameter [3]. Within the dense cytoplasm, there are hundreds of trichocysts and pseudo-nuclear vesicles [3].

Deformed Gambierdiscus toxicus cells are larger (80-100 µm) and have an embossed shaped (apical view) and a round shape (lateral view). The thecal plate in the deformed cells is disorganized. The cells also have reduced motility and undergo mitosis [3].

Small motile cells and cysts of Gambierdiscus toxicus are results of survival behavior or are possibly a stage of hynoid cyst formation [3]. These cells do not have a theca.

Metabolic processes

Gambierdiscus toxicus produces a variety of polyether natural products, including ciguatoxin, maitotoxin, gambieric acid, and gambierol[3][6]. Gambierol is a marine polycyclic ether toxin which blocks voltage-gated potassium channels [6]. Additionally, mixotrophy, or the combination of phototrophy and phagotrophy, in this case, is utilized by Gambierdiscus toxicus. G. toxicus has been observed to be photosynthetic and also contain food vacuoles [7].

Optimal Growth Conditions

The optimal growth conditions for Gambierdiscus toxicus is 26±1oC, 20 Wm-2, and a light-dark cycle of 10 to 14 hours [3]. The maximum and minimum temperatures for growth were found to be 30 degrees C and 22 degrees C [3][8]. Low light tolerance of G. toxicus is due to the epiphytic, or growth on plant surface, habits of G. toxicus on the macroalgal substrates in nature [3]. The organism exhibited horizontal phototactic migrations, in which they moved toward the light source in low-light conditions, and away from the light source in high-light conditions [3].

G. toxicus will not divide when agitated [3]. Instead, the organism will attach to its host, macroalgae, when disturbed by light or water movement [9]. When undisturbed, the organism will act planktonic [5] and swim freely around macroalgal thalli on coral reefs [9].

Ecology

Discoveries of Gambierdiscus toxicus have been made in a variety of geographical locations as it can live in a diverse range of climates. However, a preference for more temperate, warmer conditions of the South Pacific has been observed [10]. In addition to the initial discovery of G. toxicus in the Gambier Islands, this microorganism has also been linked to disease in the Kermadec Islands, Cook Islands, Northern New Zealand, Australia, and Florida [10].

G. toxicus is most often found in the benthic layer, attached to the surface of brown or red microalgae and dead coral reefs [2]. The organism can live in dead corals, macroalgae, or in volcanic sands in tropical regions [10].

Although less sensitive to salinity than to temperature, G. toxicus strongly prefers an environment of high salinity. In optimal salinity experiments, Gambierdiscus cells generally did not grow in salinity levels below 20 or above 50 ppt [8].

G. toxicus also exhibits different behaviors within different hosts. For example, it tends to swim in the presence of Jania spp., Amphiroa spp., and Galaxaura marginata, where growth is also stimulated [5]. On the other hand, in the presence of Turbinaria ornata or Laurencia spp., G. toxicus does not swim. Additionally, some hosts inhibit early growth, such as Portieria hornemannii, or late growth, such as Dictyota and Microdictyon spp. [5].

Pathology

Gambierdiscus toxicus was first confirmed as a producer of ciguatoxins—toxins involved in Ciguatera poisoning—in 1980 by Bagnis et al. [11] and has since been supported by several studies that demonstrate ciguatoxin production by G. toxicus both in the wild and in culture[12][13][14]. Ciguatera fish poisoning is the most frequently reported fish-borne food illness in the world with most studies estimating approximately 25,00 to 50,000 reported annual cases worldwide [15][16], with some studies claiming up to 500,000 [17]. Exact case numbers are unknown, as it is estimated that only 2-10% of cases are actually reported [18].

G. toxicus is largely found in macroalgae on dead coral in shallow waters, which are frequently consumed by reef fish. The ciguatoxins in G. toxicus infect reef fish upon digestion, and the toxicity level is thought to increase as it moves up the food chain, ultimately leaving predatory fish such as barracuda, lionfish, and moray eels, with the highest toxin levels ([19], see also [20][21][22][23]). These fish and the ciguatoxins they contain may then be consumed by humans leading to ciguatera poisoning. Due to the optimal habitat for G. toxicus, ciguatera is most prevalent in coastal towns in tropical and subtropical regions and in warmer seasons [8][24]. The toxins in these fish cannot be diminished by food preparation or storage efforts ([15] for review, [25] for study). Once consumed by humans, the toxin leads to gastrointestinal and cardiac symptoms such as nausea, diarrhea, vomiting, abdominal pain, abnormally fast heart rate (tachycardia), and high blood pressure that usually last 1-2 days [6][26][27]. Furthermore, some cases cause lasting neurological symptoms such as numbness, tingling, temperature perception changes, and weakness that have been reported to persist up to a year though more frequently resolve after weeks to months [19].

Gambierdiscus toxicus proliferates on dead coral reefs, which means that ciguatera fish poisoning is on the rise, and suspected to continue increasing, due to more reef death caused by climate change [23][27]. There are currently no specific treatments for ciguatoxin poisoning itself, nor are there any known biomarkers, but patients can receive symptom-specific treatment to reduce severity of symptoms [15] [18].

Current Research

Current research on Gambierdiscus toxicus is focusing on how the microorganism is being affected by global warming and rising water temperatures. The genus Gambierdiscus is well known in the tropical coral reef temperatures (24 to 29 degrees Celsius) because of their ability to develop a relationship with coral [28]. G. toxicus can create ciguatoxins (CTXs). While G. toxicus lives in areas with very little human population, it can make its way through the food web and create ciguatera problems. In other words, G. toxicus impacts on society increases with the warming of the equator by being less present living with coral and more present as plankton and infecting fish and therefore fisheries that are located on the equator [5].

A study assessed the affinity that G. toxicus has with a variety of macroalgal species (which play important roles in the ecology of coral reefs) and to see which of these macroalgal species have a harmful effect on G. toxicus. Some notable species that form relationships with G. toxicus in this paper are Galaxaura marinata, Jania spp., and Chaetomorpha spp. which proliferate the G. toxicus population throughout the 29-day period of the experiment; others like Portieria hornemannii which G. toxicus grow very little in. Parsons et al. classifies the macroalgae by their relationship with G. toxicus after the end of the experiment, these groups are: alive and attached, alive and unattached, and dead [5]. G. toxicus is not an obligate epiphyte and can be either free swimming or found in plankton, but the understanding as to why G. toxicus prefers one or the other is not well understood.

A relationship is studied between gambierol, a product made by G. toxicus, and analogs it has in cultured cerebellar neurons [29]. All three compounds cause potassium channels to lose function at very low concentrations (0.1nM). Only the heptacyclic analog created a decrease in cell viability of cerebellar neurons. The main takeaway is that only the heptacyclic analog can kill directly, meaning that G. toxicus is not a direct killer at low concentrations.

Biotechnology

Using chromatographic and spectral comparisons, CTX4A - a toxin created by G. toxicus - was shown to be structurally similar to scaritoxin, or SGI- a mixture of toxins that contain CTX4A present in parrotfish (the first link in the food chain) [13]. This study confirms that CTX4A is created through dinoflagellates (including gambierol and G. toxicus) by seeing that CTX4A, which is created by dinoflagellates, is present in poisoned parrot fish which will go on to spread the poison throughout the food chain.

References

[1] Schoch, C. L., et al. 2020. NCBI Taxonomy: a comprehensive update on curation, resources and tools. Database (Oxford). 2020: baaa062. PubMed: 32761142 PMC: PMC7408187.

[2] [Yasumoto, T., I. Nakajima, R. Bagnis, and R. Adachi. 1977. Finding of a Dinoflagellate as a Likely Culprit of Ciguatera. Bulletin of Japanese Society of Scientific Fisheries 43(8):1021-1026]

[3] Durand-Clement, M. 1986. A Study of Toxin Production by Gambierdiscus toxicus in Culture. Toxicon 24(11-12):1153-1157

[4] Richlen, M. L., S. L. Morton, P. H. Barber, and P. S. Lobel. 2008. Phylogeography, Morphological Variation and Taxonomy of the Toxic Dinoflagellate Gambierdiscus toxicus (Dinophyceae). Harmful Algae 7(5):614-629

[5] Parsons, M. L., C. J. Settlemier, and J. M. Ballauer. 2011. An Examination of the Epiphytic Nature of Gambierdiscus toxicus, a Dinoflagellate Involved in Ciguatera Fish Poisoning. Harmful Algae 10(6):598-605

[6] Cuypers, E., et al. 2008. Gambierol, a Toxin Produced by the Dinoflagellate Gambierdiscus toxicus, is a Potent Blocker of Voltage-Gated Potassium Channels. Toxicon 51(6):974-983

[7]Stoecker, D.K. 1999. Mixotrophy among Dinoflagellates. Journal of Eukaryotic Microbiology 46(4):397-401

[8] Xu, Y., et al. 2016. Influence of Environmental Variables on Gambierdiscus spp. (Dinophyceae) Growth and Distribution. PLoS One 11(4)

[9] Nakahara, H., T. Sakami, M. Chinain, and Y. Ishida. 1996. The Role of Macroalgae in Epiphytism of the Toxic Dinoflagellate Gambierdiscus toxicus (Dinophyceae). Phycological Research 44(2):113-117

[10] Rhodes, L. L., K. F. Smith, S. Murray, D. T. Harwood, T. Trnski, and R. Munday. 2017. The Epiphytic Genus Gambierdiscus (Dinophyceae) in the Kermadec Islands and Zealandia Regions of the Southwestern Pacific and the Associated Risk of Ciguatera Fish Poisoning. Marine Drugs 15(7):219

[11] Bagnis, R., S. Chanteau, E. Chungue, J.M. Hurtel, T. Yasumoto, A. Inoue. 1980. Origins of ciguatera fish poisoning: a new dinoflagellate, Gambierdiscus toxicus Adachi and Fukuyo, definitively involved as a causal agent. Toxicon 18(2):199-208

[12] Holmes, M. J., R. J. Lewis, M. A. Poli, and N. C. Gillespie. 1991. Strain Dependent Production of Ciguatoxin Precursors (Gambiertoxins) by Gambierdiscus toxicus (Dinophyceae) in Culture. Toxicon 29(6):761-775

[13] Satake, M., Y. Ishibashi, A. M. Legrand, T. Yasumoto. 1996. Isolation and Structure of Ciguatoxin-4A, a New Ciguatoxin Precursor, from Cultures of Dinoflagellate Gambierdiscus toxicus and Parrotfish Scarus gibbus. Bioscience, Biotechnology, and Biochemistry 60(12):2103-2105

[14] Yasumoto, T., 2005. Chemistry, etiology, and food chain dynamics of marine toxins. Proceedings of the Japan Academy, Series B, 81(2):43-51

[15] Friedman, M. A., et al. 2017. An Updated Review of Ciguatera Fish Poisoning: Clinical, Epidemiological, Environmental, and Public Health Management. Marine drugs 15(3):72

[16] Lewis, R. J., Sellin, M. 1992. Multiple ciguatoxins in the flesh of fish. Toxicon 30(8):915-9

[17] Fleming, L.E., Baden, D.G., Bean, J.A., Weisman, R., Blythe, D.G. 1998. Seafood Toxin Diseases: Issues in Epidemiology and Community Outreach. Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO (Galicia, Spain) 1998:245–248

[18] Friedman, M. A., et al. 2008. Ciguatera fish poisoning: treatment, prevention, and management. Marine drugs 6(3):456–479

[19] Pearn, J. 2001. Neurology of ciguatera. Journal of Neurology, Neurosurgery, Psychiatry 70(1):4-8

[20] Leite, I., et al. 2021. Experimental Evidence of Ciguatoxin Accumulation and Depuration in Carnivorous Lionfish. Toxins 13(8):564

[21] Lewis, R. J., M. Sellin, M.A. Poli, R.S. Norton, J.K. MacLeod, M.M. Sheil. 1991. Purification and characterization of ciguatoxins from moray eel (Lycodontis javanicus, Muraenidae). Toxicon 29(9):1115-1127

[22] Lewis, R.J., M.J. Holmes. 1993. Origin and transfer of toxins involved in ciguatera. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology 106(3):615-628

[23] Llewellyn, L.E. 2010. Revisiting the association between sea surface temperature and the epidemiology of fish poisoning in the South Pacific: Reassessing the link between ciguatera and climate change. Toxicon 56(5):691-697

[24] Liefer, J.D., et al. 2021. Asynchrony of Gambierdiscus spp. Abundance and Toxicity in the U.S. Virgin Islands: Implications for Monitoring and Management of Ciguatera. Toxins 13(6):413

[25] Abraham, A., E.L.E Jester, H.R. Granade, S.M. Plakas, R.W. Dickey. 2012. Caribbean ciguatoxin profile in raw and cooked fish implicated in ciguatera. Food Chemistry 131(1):192-198

[26] Hung, Y. M., et al. 2005. Short Report: Persistent Bradycardia Caused by Ciguatoxin Poisoning After Barracuda Fish Eggs Ingestion in Southern Taiwan. American Society of Tropical Medicine and Hygiene 73(6): 1026-1027

[27] Dickey, R.W., S.M. Plakas. 2010. Ciguatera: a public health perspective. Toxicon 56(2):123-36

[28] Kohli, G.S., et al. 2014. High abundance of the potentially maitotoxic dinoflagellate Gambierdiscus carpenteri in temperate waters of New South Wales, Australia. Harmful Algae 39:134–145]

[29] Pérez, S., et al. 2012. Effect of gambierol and its tetracyclic and heptacyclic analogues in cultured cerebellar neurons: a structure-activity relationships study. Chemical research in toxicology 25(9):1929–1937

Authorship Contributions

Written by Makenna Graham, Sarah Goldstein, Daniel Garcia, Reyna Flores, and Cambria Jensen. MicrobeWiki page edited by Cambria Jensen, student of Jennifer Bhatnagar for BI 311 General Microbiology, 2021, Boston University.

MG wrote the classification section and introduction. SG wrote the section on cell structure and optimal growth conditions. CJ wrote the sections on pathology and metabolic processes. DG wrote the section on current research. RF wrote the section on ecology. CJ reviewed the references. All authors edited the final draft.