‘Harmless’ Alga Indicted for Mussel Poisoning

Over the past decade, scores of Europeans have been poisoned by eating mussels harvested at various sites along the coast of Ireland. In one of the more-notorious events, 12 people on the small island of Arranmore in 1997 succumbed to severe nausea, vomiting, cramps, headaches, and diarrhea. The irony was that although pesticides or other pollutants were at first suspected, this bout of food poisoning traced to the Irish community’s first commercial crop of mussels from an aquaculture project on Arranmore, an enterprise meant to revive the ailing local fishing economy.

Chemist Kevin J. James of the Cork Institute of Technology was among scientists brought in to identify what was poisoning the shellfish—and reputation—of his nation’s mussel fishery. It took a technically heroic effort to find the culprit, he notes. Eventually, his team isolated a suite of novel toxins, which they call azaspiracids, from a native planktonic alga. To the scientists’ surprise, the agent proved none other than a species that biologists had previously assumed was benign: Protoperidinium crassipes. It and closely related algal species inhabit coastal waters throughout the world.

In the recently released September 2004 Food Additives and Contaminants, James’ team described their tortuous route to identifying the algal source of toxins that provoked gut-wrenching illness in mussel eaters on Arranmore.

It’s not surprising that mussels proved the means by which P. crassipes toxins made people sick, because environmental scientists have for years looked to these mollusks—called bivalves—as sentinels of waterborne contaminants. As filter feeders, shellfish pick up and accumulate pollutants from water, and researchers have in fact used the animals as monitors of contamination. Through this bioaccumulation of contaminants—including bacteria, viruses, and algae—mussels and other shellfish also bring food-poisoning agents to the dinner table.

That’s one reason health-care professionals advise many people, especially those with weakened immune systems, against eating raw shellfish. But cooking isn’t always the answer. Heat doesn’t detoxify azaspiracids-laced seafood, for instance. Indeed, many of the people poisoned by tainted Irish mussels had eaten commercially cooked and processed products, James notes.

James’ group has studied only shellfish off the Irish coast, but he says that shellfish tainted with P. crassipes don’t appear to be restricted to those waters. His team cites reports of azaspiracids in shellfish from Norway, England, Spain, and France. Although mussels appear to be the shellfish most apt to accumulate the toxins, James reports the chemicals’ presence in some scallops, clams, cockles, and oysters. Of that group, however, only oysters accumulate toxins in amounts comparable to what mussels pick up.

Despite circumstantial evidence, linking human disease to azaspiracids hasn’t been easy. There is no test for the poisons’ presence in people, so researchers have based their findings on tests of P. crassipes and shellfish from areas harvested for mussels. Currently, James points out, “there are only a handful of labs in the world—including ours—that can identify this toxin.” Japanese colleagues of the Cork team were the first scientists to determine the structure of the toxic chemicals, which resemble molecules produced by other algal phytoplankton.

Symptoms associated with azaspiracids poisoning can easily be mistaken for those produced by many other food-poisoning agents, including some algal toxins that trigger what is known as diarrheal shellfish poisoning. As such, James suspects that a “lot of [azaspiracids-poisoning] events go undetected,” being misidentified as more-conventional food poisoning or flu.

Detective work

Especially in coastal communities, “algal blooms,” such as a red tide, frequently make news. These phenomena result when a plume of plant nutrients—from agricultural runoff, a sewer overflow, or some other event—flows from inland to coastal waters and triggers the explosive growth of certain floating, single-celled algae called phytoplankton.

Phytoplankton species can temporarily tint the water red, blue-green, or brown. When blooms are big and persistent, the algae growth can temporarily deplete oxygen from large parcels of water, producing suffocating dead zones (see Dead Waters).

Not all algal blooms color the water, however. Indeed, James notes, off Ireland’s coast, algal blooms tend to occur about 5 meters down and offer no visible surface clues. So mussels growers get no warning of an impending poisoning event. Moreover, mussels don’t seem to suffer harm from the azaspiracids. That may reflect their having evolved a resistance to the compounds from the mollusks’ frequent exposure to them, James says.

The algae that produce azaspiracids are “scavengers” living off the dying blooms of other algae, James explains. Also, P. crassipes doesn’t tend to bloom, so its relatively small numbers among blooming phytoplankton concealed for many years the alga as the source of azaspiracids.

Early in his research, James needed huge numbers of P. crassipes cells to yield enough azaspiracids to detect. “Now we can perform our analyses with as few as 20 cells,” he says. When isolated and administered to mice, these toxins produced the characteristic poisoning symptoms, confirming their role in the gastrointestinal symptoms plaguing some European seafood eaters.

So far, the Cork scientists have identified three azaspiracids in P. crassipes cells and eight other, less toxic ones that appear to form in shellfish as their bodies attempt to break down the compounds, James says.

Still unresolved, he says, is whether P. crassipes creates the three most potent azaspiracids or merely acquires them when it feeds upon other, toxic, algae. In fact, “we don’t believe they scavenge them,” James told Science News Online, “because we’ve searched and searched everything else in the actual [aquatic] community in which we find the toxin, and we find [azaspiracids] in only the one algal species.”

More than just a gut feeling

No death has yet been ascribed to azaspiracids poisoning. As such, the toxin doesn’t appear to have the potentially devastating acute toxicity of paralytic-shellfish-poisoning (PSP) toxins produced by Alexandrium algae. Those poisons can induce respiratory arrest within 24 hours after a person eats tainted shellfish.

However, people who survive a PSP episode tend to recover fully, James notes. Animal studies now suggest that azaspiracids poisoning may have potentially serious long-term impacts, which could make it far more insidious than it first appeared.

For instance, in mice, low doses of azaspiracids reduced the size of the normal fingerlike protrusions, or villi, on the interior wall of the animals’ small intestines, James and his colleagues recently showed. When villi shrink, nutrient absorption plummets (see Target: Celiac Disease). In the azaspiracids experiments, villi shortening caused the mice to lose weight.

James notes that in another experiment, long-term azaspiracids administration to mice led to the development of pneumonia and lung tumors.

These latter impacts suggest that widespread screening for azaspiracids might be warranted, James says, so that any tainted shellfish beds can be quarantined—as Ireland’s have been—until the toxins disappear. Indeed, James says, it may be that P. crassipes produces the toxin only when stressed, so the mere presence of this species may not signal harm.