FRI Briefings

Toxins from Algae/Cyanobacteria

first published May 1998

prepared by M. Ellin Doyle, Ph.D.

Food Research Institute, UW-Madison

Pfiesteria piscicida — Cell from Hell
Pfiesteria spp. was identified last August 1997 as the cause of a major fish kill (30,000 fish) in Maryland’s Pocomoke River and also affected fish in two other rivers on the eastern shore of Chesapeake Bay (1). In fact, since 1991 this one-celled dinoflagellate (a type of algae) has caused numerous major fish kills along the eastern coast of the USA, including a 1995 episode along the coast of North Carolina killing an estimated 15 million fish (2,3). Its current known range includes estuarine (brackish) and coastal waters as far north as Delaware and as far south and west as Alabama and Florida (4). A report from BBC News (5) indicates that Pfiesteria has also crossed the Atlantic to the British coast, perhaps in ballast tanks of cargo ships and tankers. This has raised concerns about potential massive fish kills along the European coast.

Pfiesteria has a complex life cycle with at least 24 distinct life stages. During winter and when food is scarce, cells rest as cysts in estuarine sediments until they chemically detect fresh fish excretions or secretions. The cysts then develop into motile, flagellated zoospores which secrete toxins inducing neurological symptoms such as lethargy and skin lesions—bleeding skin ulcers and a peeling away of the skin of their prey. The dinoflagellates then feed on the tissues of the dying fish. Concentrations of Pfiesteria zoospores at sites of fish kills range from 250 to 250,000/ml. When fish are not available, Pfiesteria will also consume some other algae, bacteria, and small animals. As environmental conditions become unfavorable, the cells synthesize a protective outer coating and sink to the sediment as cysts (2,3,6).

An influx of high concentrations of nutrients into coastal waters has been observed to stimulate the growth of noxious algae, including Pfiesteria (7). Following the rupture of a large North Carolina swine waste-holding lagoon in 1995, 25.8 million gallons of effluent flowed into a nearby coastal river. The immediate effect was depletion of oxygen and high levels of ammonia causing death of 4000 fish. As the effluent proceeded downstream, nutrient levels in the water increased dramatically and species of several nuisance algae, including Pfiesteria, bloomed and thousands more fish were killed or injured.

Although the nature of the Pfiesteria toxins has not been elucidated, there is direct evidence that they are toxic to humans. Both research scientists and coastal residents and fishermen have reported skin ulcers, short-term memory loss, confusion, prominent eye irritation, and respiratory distress following immersion in Pfiesteria-infested water or inhalation of aerosols from contaminated water (6). Most of the acute symptoms reversed with time if the persons avoided further exposure. However, some effects recurred following strenuous exercise. Therefore, all work with fish-killing cultures of Pfiesteria must now be conducted in biohazard level III containment systems in a limited-access facility (3,4).

Pfiesteria produces at least two toxins—one which is water-soluble and the other lipid-soluble. The hydrophilic compound is thought to be the neurotoxin (4). Preliminary in vitro studies demonstrated that nerve cells are particularly sensitive to one toxin as measured by decreased ATP levels and leakage of lactate dehydrogenase from the cells. Recent experiments with rats exposed to Pfiesteria demonstrated that they suffered a significant impairment in learning new tasks (8). The lipid-soluble toxin may be responsible for the skin lesions that are induced in exposed fish and humans.

Since affected fish are not very appetizing, foodborne illness due to consumption of these fish by humans does not appear likely at this time, nor would estuarine or ocean water containing the toxins likely be consumed. However, shellfish and crabs ingest other dinoflagellates that produce neurotoxins and accumulate enough saxitoxin, brevetoxin, or domoic acid to cause paralytic, amnesic, or neurotoxic shellfish poisoning in humans. Outbreaks of such foodborne disease have occurred in many coastal areas.

Preliminary studies indicate that shellfish also consume Pfiesteria. In some cases, adult shellfish did not appear to be affected; however, bay scallops ceased feeding after 15 minutes exposure to Pfiesteria zoospores (4). Therefore, there is a possibility that Pfiesteria could be filtered out by shellfish and the toxins accumulated to produce a new type of shellfish poisoning. It is important to establish whether or not Pfiesteria causes foodborne illness via fish or shellfish, because there is a public perception that it may do so. Following the Chesapeake Bay outbreak last year, it was estimated that the "Pfiesteria panic" caused a reduction in total sales from $253 million to $210 million for businesses that specialize in seafood. Seafood sales in restaurants and stores dropped dramatically in September/October although they later recovered (4).

Microcystins

These toxins, produced by cyanobacteria (sometimes called blue-green algae), were also in the news recently as they caused acute liver failure in more than 100 Brazilian hemodialysis patients (9). Symptoms were first manifested Feb. 17–20, 1996, and within 7 months at least 50 patients died of the acute hepatotoxic effects of these toxins. Microcystin concentrations in liver samples from the victims were comparable to those found in laboratory animals given lethal doses of this toxin. An investigation of the outbreak revealed that visibly turbid reservoir water was supplied to the center by truck. Despite some water treatment at the dialysis facility (filtration, carbon adsorption, and deionization), the patients were exposed to high levels of microcystins probably because the filters and carbon adsorption tank had not been changed for at least 3 months. No chemical treatment (chlorination) step was used. Since the toxins were introduced directly into the bloodstream, these patients were more severely exposed than persons who might have drunk the contaminated water.

In most cases, water treatment systems should be adequate to remove cyanobacteria by coagulation and filtration and microcystins can be removed by charcoal filters and degraded by chlorination (10). However, we all remember the Cryptosporidium outbreak in Milwaukee a few years ago when lack of proper maintenance of a water treatment system allowed this protozoan to pass through the filtration system and into the city’s drinking water. (See previous FRI update on Cryptosporidium.) Tests with domestic water filters indicated that they could remove some cyanobacteria and microcystins but none of the models tested removed all the cells or toxins (11).

Cyanobacterial toxins have also been reported to cause epidemic gastroenteritis in humans in Brazil (9) and death in cattle and other animals who drank contaminated water. Poisoning of cattle and other domestic animals often occurred when their drinking water source was a eutrophic pond receiving significant agricultural runoff (12). Occasionally, toxin-producing cyanobacteria are reported from remote oligotrophic lakes which are low in plant nutrients and have high oxygen levels (13).

Although there have been no reported incidents of poisoning with cyanobacterial toxins present in foods, shellfish can filter cyanobacteria from water and could accumulate these toxins. Saltwater mussels (Mytilus edulis) fed Microcystis accumulated microcystins which persisted for several days after transfer of the mussels to clean water (14). Fresh fruits and vegetables washed in contaminated water could also acquire these toxins. Dietary supplements containing blue-green algae may contain microcystins (pers. comm., Dr. F. S. Chu) and are another potential source of human exposure to cyanobacterial toxins.

Cyanobacteria are common in fresh water throughout the world and are known to produce several types of toxins: microcystins which are heat-stable, cyclic heptapeptide hepatotoxins and also promote tumor growth and inhibit protein phosphatases; anatoxin, a neurotoxin, which inhibits acetylcholinesterase; and paralytic shellfish poisoning (PSP) toxins, such as saxitoxin, which are also neurotoxic. Lyngbya wollei, commonly found in some lakes and reservoirs in the southeastern USA, and one strain of Aphanizomenon flos-aquae also produce potent neurotoxins, related to PSP toxins (15). Toxin levels produced by Anabaena spp. were much greater in older cultures and in cultures supplemented with phosphorus (16). Therefore, a reduction of phosphorus loads in ponds and reservoirs might aid in preventing toxic cyanobacterial blooms.

Algae are important as the base of nearly all aquatic food chains but some varieties have become a nuisance fouling our lakes. Unicellular eukaryotic algae and prokaryotic blue-green algae are widespread in various bodies of water throughout the world. But they are often overlooked until their populations explode (bloom) and/or they produce toxins affecting humans or domestic animals. Several investigators have reported that such incidents are becoming more common and attribute this to addition of more nutrients to water: runoff from agricultural lands or concentrated farming operations or from nearby homeowners adding excess fertilizer to their lawns. An issue of the journal Limnology and Oceanography (17) last summer was devoted to the ecology of harmful algal blooms (2).

Since some of these organisms have the potential to cause significant outbreaks of illness in humans and animals, we must be vigilant in maintaining our water purification systems and also be aware of the quality of the water used by our domestic animals. The U.K. and the State of Oregon have set limits of 1 ppm for microcystins in water and dietary supplements. The U.S. government has developed and published a National Harmful Algal Bloom Research and Monitoring Strategy which will initially focus on Pfiesteria outbreaks (18). Many experts believe that we will experience additional outbreaks of illness related to blooms of cyanobacteria or dinoflagellates until we understand how to control the environmental factors that limit their growth.

References

1. Pelley J. 1997. Toxic Pfiesteria outbreak triggers federal–state research plan. Environ. Sci. Technol. 31:A 503

2. Burkholder J.M., and H.B. Glasgow. 1997. Pfiesteria piscicida and other Pfiesteria-like dinoflagellates: behavior, impacts, and environmental controls. Limnol. Oceanogr. 42:1052–1075.

3. NCSU Aquatic Botany Laboratory—Pfiesteria piscicida Homepage. http://www2.ncsu.edu/unity/lockers/project/aquatic_botany/pfiest.html

4. University System of Maryland. Fish health in the Chesapeake Bay: About Pfiesteria piscicida. http://www.mdsg.umd.edu/fish-health/pfiesteria/index.html

5. BBC News. http://news.bbc.co.uk/hi/english/sci/tech/newsid_20000/20403.stm

6. Glasgow H.B., J.M. Burkholder, D.E. Schmechel, P.A. Tester, and P.A. Rublee. 1995. Insidious effects of a toxic estuarine dinoflagellate on fish survival and human health. J. Toxicol. Environ. Health 46:501–522.

7. Burkholder J.M., M.A. Mallin, H.B. Glasgow, L.M. Larsen, M.R. McIver, G.C. Shank, N. Deamermelia, D.S. Briley, J. Springer, B.W. Touchette, and E.K. Hannon. 1997. Impacts to a coastal river and estuary from rupture of a large swine waste holding lagoon. J. Environ. Qual. 26:1451–1466.

8. Levin E.D., D.E. Schmechel, J.M. Burkholder, H.B. Glasgow, N.J. Deamermelia, V.C. Moser, and G.J. Harry. 1997. Persisting learning deficits in rats after exposure to Pfiesteria piscicida. Environ. Health Perspect. 105(12):1320–1325.

9. Jochimsen E.M., W.W. Carmichael, J.S. An, D.M. Cardo, S.T. Cookson, C.E.M. Holmes, M.B.D. Antunes, D.A. Demelo, T.M. Lyra, V.S.T. Barreto, S.M.F.O. Azevedo, and W.R. Jarvis. 1998. Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. New Engl. J. Med. 338:873–878.

10. Tsuji K., T. Watanuki, F. Kondo, M.F. Watanabe, H. Nakazawa, M. Suzuki, H. Uchida, and K.I. Harada. 1997. Stability of microcystins from cyanobacteria—IV. Effect of chlorination on decomposition. Toxicon 35(7):1033–1041.

11. Lawton L.A., B.J.P.A. Cornish, and A.W.R. Macdonald. 1998. Removal of cyanobacterial toxins (microcystins) and cyanobacterial cells from drinking water using domestic water filters. Water Res. 32(3):633–638.

12. Frazier K., B. Colvin, E. Styer, G. Hullinger, and R. Garcia. 1998. Microcystin toxicosis in cattle due to overgrowth of blue-green algae. Vet. Human Toxicol. 40(1):23–24.

13. Mez K., K.A. Beattie, G.A. Codd, K. Hanselmann, B. Hauser, H. Naegeli, and H.R. Preisig. 1997. Identification of a microcystin in benthic cyanobacteria linked to cattle deaths on alpine pastures in Switzerland. Eur. J. Phycol. 32:111–117.

14. Williams D.E., S.C. Dawe. M.L. Kent, R.J. Andersen, M. Craig, and C.F.B. Holmes. 1997. Bioaccumulation and clearance of microcystins from salt water mussels, Mytilus edulis, and in vivo evidence for covalently bound microcystins in mussel tissues. Toxicon 35(11):1617–1625.

15. Carmichael, W.W., W.R. Evans, Q.Q. Yin, P. Bell, and E. Moczydlowski. 1997. Evidence for paralytic shellfish poisons in the freshwater cyanobacterium, Lyngbya wollei (Farlow ex Gomont) comb. nov. Appl. Environ. Microbiol. 63(8):3104–3110.

16. Rapala J., K. Sivonen, C. Lyra, and S.I. Niemela. 1997. Variation of microcystins, cyanobacterial hepatotoxins, in Anabaena spp. as a function of growth stimuli. Appl. Environ. Microbiol. 63(6):2206–2212.

17. Anderson D.M., and D.J. Garrison, eds. 1997. The ecology and oceanography of harmful algal blooms. Limnol. Oceanogr. 42(5, part 2):1009–1305

18. National Harmful Algal Bloom Research and Monitoring Strategy. http://www.redtide.whoi.edu/hab/announcements/pfiesteria/pfiesteriastrategy.html

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