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Biochemical Warfare on the ReefIn a co-evolutionary struggle, invertebrate adversaries develop weapon and counter-weapon |
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Kristen Whalen
Graduate Student
MIT WHOI Joint Program Just beneath the tranquil, clear waters of the tropical Caribbean,
unseen by all but a few keen-eyed divers, two foes have engaged in a
life-and-death struggle every day for thousands of millennia. Their
limestone battlefield is peppered with a limitless variety of soft
coral that look like easy targets for any hungry passerby. However,
looks can be deceiving. These outwardly innocuous corals, commonly
known as gorgonians, have a few tricks up their soft sleeves. They have
evolved a powerful arsenal of chemical toxins that leave all who dare
to consume them with a mouthful of distasteful compounds and a lesson
they won’t soon forget.
The gorgonians’ chemical defenses do an excellent job of deterring most
fishes and other large predators. But a handful of reef inhabitants
have learned how to navigate the gorgonians’ toxic chemical mine-field
and exploit these abundant corals for both food and shelter, giving
themselves an edge over their fellow reef competitors.
A sea snail’s all-you-can-eat (toxic) buffet
At first glance the reclusive sea snail Cyphoma gibbosum,
known as a “flamingo tongue” to most Floridians, appears harmless even
skittish. It retracts its ornate mantle tissues inside its
cream-colored shell at the mere passing of a shadow overhead. Yet, this
single species of sea snail, no bigger than a postage stamp, has an
insatiable appetite for gorgonians. This predator inflicts damage to
more gorgonian colonies per year than even the most destructive
hurricane.
Cyphoma leaves an unmistakable trail of feeding scars on
gorgonians. The snails usually feed in roving hordes, munching their
way through toxin-saturated tissue down to the corals’ hard
skeleton. The sea snails use a modified tooth called a radula,
chewing through tissue in a fashion similar to mowing a lawn. How this
molluscan predator can overcome the gorgonians’ toxic chemical defenses
– a feat unparalleled by the thousands of competing consumers on the
reef—was the mystery that I hoped to solve.
Before I entered the WHOI/MIT Joint Program in 2002, I was introduced
to the field of chemical ecology as an undergraduate at the University
of North Carolina, Wilmington. Three times a year, we would pack up the
lab, grab our wetsuits, and head south to the Florida Keys and the
Bahamas to conduct experiments to assess the chemical defenses of
Caribbean sponges.
Sponges in many ways are similar to their gorgonian cousins in that
both are attached to the bottom and exposed to predators. Furthermore,
both use similar noxious compounds to defend themselves against hungry
consumers.
During forays into the field to study sponges, my attention strayed to
their coral neighbors, where I caught my first glimpse of Cyphoma
happily nibbling away on its toxic coral diet. I wondered how this
snail was able to beat the system and consume a diet so rich in toxins
and yet appear no worse for the wear? Little did I know that the answer
to my question would come from understanding how the human body is able
to cope with chemicals.
PharmEcology
In humans, the liver acts as the body’s filter. It breaks down and
excretes a wide range of chemicals including drugs, alcohol, man-made
toxicants and naturally-derived compounds found in our food. The
processes controlling this incredible feat are carried out by a network
of genes and enzymes, collectively termed a “defensome”, affording our
bodies protection from chemical intoxication. Akin to the human liver,
the digestive gland in Cyphoma
is thought to contain genes and enzymes that carry out functions
similar to their human counterparts, albeit fine tuned over
evolutionary time scales to handle the marine toxins these snails
encounter.
Working with my Ph.D. advisor Mark Hahn, senior scientist in the
Biology Department at Woods Hole Oceanographic Institution, I have
attempted to identify the genes and enzymes in the gut of Cyphoma
that allows them to overcome the biochemical barrier imposed by the
coral. We used our knowledge of gorgonian coral chemistry to identify
those families of genes and enzymes in humans that would likely be
responsible for metabolizing such compounds. Using this knowledge as a
blueprint, we then looked for these same families of genes and enzymes
in Cyphoma.
Once we identified several possible sea snail detoxification genes, the
next step was to examine how these genes responded to the gorgonian
compounds. In 2006, I collected sea snails and gorgonians from shallow
reefs near the Perry Institute of Marine Science (PIMS) in the Bahamas.
Back at the PIMS laboratory I allowed the sea snails to either feed on
a gorgonian diet or a control diet lacking any coral compounds to
examine how the expression of the genes varied when the sea snail was
exposed to gorgonian compounds.
I found that the expression of one group of detoxification genes is “ramped up” in the digestive glands of Cyphoma
feeding on specific gorgonian diets. These sea snail genes likely
encode enzymes that are able to metabolize the very coral compounds
responsible for their increased expression. These enzymes work by
slapping an oxygen molecule onto the chemical intruder making it more
water soluble and easier for the cell to excrete. But it seems that
this family of enzymes is only capable of responding to and detoxifying
a narrow range of coral compounds.
In contrast, a second family of enzymes was highly expressed in the digestive gland of Cyphoma regardless
of the gorgonian diet. These enzymes assist by tagging the toxin with a
special chemical flag, signaling the cell to expel out the toxin
through gated pumps in the cell membrane. A follow-up series of
experiments concluded that these proteins likely function as
“all-purpose” detoxification enzymes, capable of “tagging” a broad
range of gorgonian compounds.
Together, these results suggest that Cyphoma’s defensome is
comprised of genes and enzymes that have both specific and varied
detoxification roles, but work in concert to protect this predator from
its toxin-laden prey.
For now the score appears to be Cyphoma 1, gorgonians 0—but
I wouldn’t count the corals out of this co-evolutionary arms race just
yet. If evolutionary theory has taught us anything, gorgonians are
quietly developing novel toxins through spontaneous genetic mutation
events that may one day confer an adaptive advantage in their
direction. My advice to spectators: Stay tuned for the next 10,000
years of co-evolution.
This research was supported by a National Science Foundation
Graduate Research Fellowship, the Cole-Ocean Ventures Fund (WHOI), a
Tropical Research Initiative grant from the Ocean Life Institute
(WHOI), and grants from SeaSpace and Conchologists of America.This article was written during a science writing course for
graduate students at WHOI, supported by funds from The Henry L. and
Grace Doherty Professor of Oceanography.
Posted: August 26, 2008 [top] |
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