Nat. Commun. 6, 7869 (2015)

Credit: NAT. COMMUN.

Polyphenols, known to cause protein precipitation, are produced in abundance by plants, meaning that earthworms are likely to be subjected to particularly high concentrations of these compounds due to plant decomposition. Previous research has shown that earthworms prefer plant material with low amounts of polyphenols, suggesting the compounds do affect the worms. But how do they contend with these molecules to prevent their deleterious effects? Liebeke et al. used metabolomics to search for small molecules that might be involved. The authors performed imaging mass spectrometry of cryosectioned worms looking for highly abundant molecules that might interact directly with the polyphenols. They identified a peak corresponding to 2-hexyl-5-ethylfuran-3-sulfonate and several variants present in the earthworm gut. Though this molecule has been identified in worms before, its biological role had not been established. The authors found the molecule in the anterior part of the gut lumen, well positioned to interact with material eaten by the worm. The suite of compounds are unique to earthworms as compared to other species and were also found in all earthworms tested (14 species across three families), and their abundance varied across life stages, consistent with a physiological role unique to the earthworm habitat. In vitro studies established that the compounds are surfactants and can solubilize lipids in addition to protecting proteins from polyphenols. However, in vivo experiments showed that the compounds are produced in greater quantities in response to a high-polyphenol diet than to a control or high-fat diet, and are present in higher quantities in earthworms collected from sites with larger amounts of leaf litter, suggesting that their primary function is linked to polyphenols. The discovery of these 'drilodefensins' sets the stage for further research into their biosynthesis and the mechanism by which complexed polyphenols are removed from the gut.