"Industrial" Pollutants Reveal a Surprising Origin

chemicals synthesized for use as industrial flame retardants and regarded as persistent environmental pollutants.

Stuart Blackman(sblackman@the-scientist.com)
Jun 5, 2005
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After a True's beaked whale washed ashore in Virginia, Woods Hole chemist Emma Teuten toiled for seven months trying to whittle 10 kilograms of blubber down to a milligram of methoxylated polybrominated diphenyl ethers – chemicals synthesized for use as industrial flame retardants and regarded as persistent environmental pollutants. But improved carbon dating methods revealed that these PBDEs were natural compounds, possibly originating in marine sponges. The surprising find has focused a debate about the risks of exposure to synthetic compounds.

Halogenated organic compounds like PBDEs include some of the most notorious industrial pollutants: polychlorinated biphenyls (PCBs), dioxins, and the infamous pesticide DDT. Concerns over toxicity to humans and the environment have led to bans on many of these so-called persistent organic pollutants. "For a long time, whenever we found a source of chloroform or dioxin or something, it was assumed to be from pollution from pesticides or other man-made sources," says Gordon Gribble, an organic chemist at Dartmouth College, New Hampshire.

But, says Gribble, many similar compounds are produced naturally in biological and geochemical systems. "About 15 years ago, I was reading articles by Greenpeace saying that nature would never make these organohalogen compounds because they're toxic, they bioaccumulate, they don't biodegrade. I knew that wasn't true to some extent." So, he conducted a literature search that revealed "literally thousands" of such naturally occurring chemicals. In marine environments, chlorinated and brominated compounds are widely manufactured by sponges, tunicates, and nudibranchs, while dioxins are produced by volcanoes and forest fires.1 There is even evidence, as yet not replicated, says Gribble, for the emission of PCBs during the 1980 Mount St. Helens eruption.

DATING GAMES

Clues to the origin of many organohalogens can be gleaned from analyses of sediments and dated collections of whale oils, in which these lipophilic molecules tend to accumulate. "Most man-made halogenated compounds weren't synthesized until the mid-1920s," says Woods Hole environmental chemist Chris Reddy. While DDT and its derivatives are never found in the older samples, for example, PBDEs do turn up. Natural PBDE analogs – produced by certain sponges – differ from the synthetics only by the presence of a methoxy group, but this might easily be added to a flame retardant stock after it enters the food chain, explains Reddy.

To establish the origin of the methoxylated PBDE residues found in whale blubber, Reddy and Teuten employed a radiocarbon dating technique developed with their colleague Timothy Eglinton.

By the mid-1990s, improvements to both accelerator mass spectrometry (AMS) and gas chromatography had allowed Eglinton, Reddy, and colleagues to distinguish single compounds produced during the combustion of organic matter. Fossil fuel residues are radiocarbon-dead, while burning wood, for example, leaves a recent, biological 14C signature. Reddy, in turn, saw the possibility of distinguishing between fossil fuel-derived industrial organohalogens and their natural analogs.

After proving the technique on compounds of known origin, Reddy's lab set about applying it to two methoxylated PBDEs extracted from their specimen of Mesoplodon mirus. They proved to be high in 14C, indicating a natural origin.2

This shows that natural PBDEs accumulate in blubber just like their industrial analogs, according to Reddy. Jan Boon, an ecotoxicologist at the Royal Netherlands Institute for Sea Research, agrees. "I see no reason to assume that they behave differently from the commercial compounds," he says.

Elizabeth Salter-Green, UK toxics program leader at the World Wide Fund for Nature (WWF), points out that care should be taken extrapolating from a study on a single animal, but describes the work as "very interesting."

UNNATURAL DISTINCTION

Several researchers observe that the findings have implications for how society perceives the risks posed by natural versus synthetic chemicals. "In the public perception, a chemical starts to be dangerous as soon as it's called synthetic," says Boon.

Anthony Trewavas, a plant physiologist at the University of Edinburgh, points to a recent WWF campaign in which volunteers – including European politicians – were screened for synthetic residues in their blood.3 "My objection to that is that after every meal thousands of chemicals appear in your bloodstream, but they're all natural," says Trewavas. "No one bothers a whit about that. But if you test them on rodents, they're carcinogens, teratogens, estrogen mimics, nerve toxins, sterility-inducing chemicals," he says.

It's no surprise that plants produce toxins. "Plant evolution is all chemical warfare – they can't run away," says Bruce Ames of the University of California, Berkeley, who developed the Ames test for carcinogenicity and worked on the toxicology of tris (2,3,-dibromopropyl) phosphate, a flame retardant banned in the 1970s. Ames points out that "99.99% of the pesticides you eat are natural pesticides in plants."

"If people took this in properly," says Trewavas, "they would stop worrying about these microgram amounts of synthetic pesticides."

<p>A WHALE OF A PROJECT:</p>

Courtesy of Tom Kleindinst © WHOI

Emma Teuten and some of the 22 pounds of whale blubber, wrapped in a black plastic bag, from which she extracted a milligram of methoxylated polybrominated diphenyl ethers.

Ames traces fears over synthetic chemicals to Rachel Carson's influential book Silent Spring, which railed against DDT – a chemical that Ames says "saved hundreds of millions of lives" in the battle against malaria. According to Trewavas, about 2,000 cases of human poisoning by the natural toxins in potatoes have appeared in the scientific literature, compared to zero for DDT. Nevertheless, Salter-Green says that most of the natural pesticides we ingest – PBDEs aside – neither bioaccumulate nor are persistent.

Trewavas says the presence of natural analogs of synthetic organohalogens might help explain the existence of enzymes such as the cytochrome P450 complex enzyme that metabolize many industrial products. "We've been exposed to these things forever and that means we'll have defense mechanisms to deal with them."

Other industrial compounds, like DDT, have no natural analog. But nor do humans have an evolutionary history of exposure to many of the natural compounds included in the modern diet, argues Ames. "Just look at the plants that came from the New World," he says. "Europeans weren't eating corn, string beans, avocados, potatoes, or tomatoes." Ames maintains that defenses against toxins are generalized rather than chemical-by-chemical.4

Mark Hahn, a molecular toxicologist at Woods Hole, says there's no reason to think that cytochrome P450 is any better at breaking down natural compounds than synthetic. "It's evolved to be promiscuous," he adds.

POISON OR PANACEA?

There is also the question of whether exposure to environmental levels of organohalogens is actually harmful. Hahn says that while some studies show that such exposure can impair reproductive and immune function in wildlife, human studies are more controversial. "The simple answer is we just don't know," he says.

Edward Calabrese, professor of toxicology at the University of Massachusetts, Amherst, laments that toxicological studies have relied on high-dose animal tests, which are then extrapolated to low doses. While environmental exposure standards are generally based on a threshold model or, for carcinogens, a linear model, where no level of exposure is deemed safe, he argues the dose-response curve for most toxins is J-shaped. According to this hormesis model, exposure to toxins at small doses often has a protective effect. It doesn't matter whether the toxic challenge is natural or synthetic, he says. Even DDT (the archetypal bioaccumulating synthetic organohalogen) has a hormetic dose-response relationship.5

Hormesis "occurs at a frequency that is greater than any other model," says Calabrese, who contends that it should therefore replace the default models.6 Ames is impressed by the empirical support for Calabrese's ideas. "The literature's full of this hormesis business," he says. "People are really starting to take it seriously."

Meanwhile, Boon stresses that synthetic compounds are still worth paying special attention to because they add significantly to environmental levels of toxins. "The sponges that produce them are not everywhere in enormous quantities," he says. Indeed, PBDE concentrations in humans have increased by a factor of 100 in the last 30 years, although they still occur only in nanogram quantities per gram of tissues.7

Reddy's technique might prove invaluable for assessing the relative contributions of industry and nature for many compounds. His team is now trawling through other organohalogens from whale blubber. But he has his sights set on wider applications for the technique, such as tracing the origin of atmospheric chloroform. "There's a lot of debate right now over whether termites make a lot of it," he says. Gribble adds that dioxins should also be a priority, given their variety of known sources.

Eglinton says that such endeavors will be aided by imminent technological advances. He points to the development of continuous-flow AMS, which offers the potential for measuring compounds "on the fly" as they are separated from a chromatographic column. Soon, he says, "screening hundreds of compounds within a short period of time will become very feasible."