Metabolites Protect Earthworms Against Harmful Plant Compounds In Diets

Earthworms would prefer not to eat a diet high in polyphenols. But they often have no choice. The leaf litter that provides most of their diet is typically high in polyphenols, which can trigger proteins in the worms to precipitate and can disrupt their enzymes. Plants produce these compounds to defend against herbivores.

New research suggests that a metabolite unique to earthworms might help them cope with their high-polyphenol diet.

By using mass spectrometric imaging, Jacob G. Bundy of Imperial College London and coworkers showed that a class of metabolites the researchers call drilodefensins are localized in the earthworm gut (Nat. Commun. 2015, DOI: 10.1038/ncomms8869). Worms that eat more polyphenols produce more drilodefensins, according to the researchers.

Chemically speaking, the drilodefensins are dialkylfuransulfonates. They account for about 1% of the worms’ body mass, Bundy says. The researchers have found them in multiple earthworm species but not in other types of worms, such as leeches or aquatic worms, that don’t consume leaf litter. The researchers think the compounds work as biological surfactants that prevent protein precipitation without reducing enzyme activity.

When Bundy and coworkers first identified the compounds, they thought they were probably on the worms’ surface and helping them move through soil. But mass spec imaging revealed that wasn’t the case.

“Not until we got the mass spec images did we realize that, no, they’re in the gut,” Bundy says. “The mass spec imaging completely changed our understanding about their potential function as biological molecules.”

To obtain the images, the researchers needed to freeze the earthworms and cut them into sections. If they tried to extract the gut components, the drilodefensins simply disappeared. Bundy suspects that enzymes toward the back of the worms’ gut rapidly degrade the metabolites to recycle them—especially the sulfur, he says.

Randy A. Dahlgren, a professor of soil science at the University of California, Davis, says the work is of interest because of potential impacts on terrestrial ecosystems. “Polyphenols play an important role in organic matter quality that affects carbon cycling,” he says. “The earthworm turnover of high-polyphenol, organic matter may affect global carbon cycling.”