An international team of researchers has identified molecules in the earthworm gut that enable digestion of polyphenol-rich plant material, such as fallen leaves.

Earthworms are responsible for returning the carbon locked inside dead plant material back into the ground. They drag fallen leaves and other plant material down from the surface and eat them, enriching the soil, and they do this in spite of toxic chemicals produced by plants to deter herbivores.

The team, directed by Dr Jake Bundy from Imperial College London, UK, and Dr Manuel Liebeke of the Max Planck Institute for Marine Microbiology in Germany, has now identified molecules in earthworms that counteract the plant’s natural defenses.

“These molecules, named drilodefensins, are very abundant. Their abundance is not, however, an excess – drilodefensins are so precious that earthworms recycle the molecules in order to harness their effects again. A world without drilodefensins would be a very different world,” said Dr Bundy, senior author of a paper published in Nature Communications.

“Without drilodefensins, fallen leaves would remain on the surface of the ground for a very long time, building up to a thick layer. Our countryside would be unrecognizable, and the whole system of carbon cycling would be disrupted,” he said.

“We have established that earthworms, referred to as ‘nature’s ploughs’ by Charles Darwin, have a metabolic coping mechanism to deal with a range of leaf litter diets. In this role, drilodefensin support the role of earthworm as key ecosystem engineers within the carbon cycle,” said co-author Dr Dave Spurgeon of the Centre for Ecology and Hydrology in Wallingford, UK.

Plants make polyphenols, which act as antioxidants and give the plants their color; they also inhibit the digestion of many herbivores. Earthworms, however, are able to digest fallen leaves and other plant material, thanks to the ability of drilodefensins to counteract polyphenols.

The researchers found that the more polyphenols present in the earthworm diet, the more drilodefensins they produce in their guts.

The finding that the molecules are abundant in the gut of earthworms was made possible by using modern visualization techniques based on mass spectrometry.

“Using these molecular microscopes is changing how we understand complex biochemistry of living beings,” Dr Liebeke said.

“We are now able to locate every molecule in, for example, an earthworm to a specific location. Knowing the location of a molecule can help us to figure out what it actually does.”

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Manuel Liebeke et al. 2015. Unique metabolites protect earthworms against plant polyphenols. Nature Communications 6, article number: 7869; doi: 10.1038/ncomms8869