Coping with phenol-rich foodstuffs

We rightly salute fungi and bacteria as being indispensable to the decomposition processes that breaks down dead organic matter into inorganic components that can then be recycled through the biosphere in those all-important biogeochemical cycles.

Formation of Vegetable Mould

However, those microbes benefit from the activity of other organisms that break down larger biological units into smaller, more manageable chunks. One of nature’s most important – though largely unsung – heroes in this respect is the earthworm. A measure of the worm’s importance is the realisation that it is largely by dint of their industry that we aren’t knee-deep in rotting leaves at this time of the year in temperate zones with large populations of deciduous angiosperm trees having recently shed their pigmented mantle.

Given how important leaves’ photosynthetic services are to the growth and very survival of the plant that bears them, it’s not too surprising that plants go to great lengths to protect them with a range of chemical ‘deterrants’. However, after abscission and leaf-fall, those formerly life-sustaining compounds continue to work and help prevent the decay and break-down of the leaf’s structures in death. One such group of compounds, the polyphenols, has potent anti-herbivory properties* by inhibiting the action of digestive enzymes in the would-be consumer’s gut.

Faced with such a formidable defence, how do earthworms manage to digest such well-defended leaves? A good question, and one which Manuel Liebeke et al. appear to have solved. The team discovered that the earthworm (Lumbricus rubellus, whose eminently apt international common name in English is the ‘leaf worm’), contains metabolites in their gut,** which counteract the inhibitory effects of polyphenols on their gut enzymes. These dialkylfuransulfonate compounds, whose proposed name is drilodefensins, increase in concentration in response to diets high in polyphenols – both in the laboratory and in field populations. The importance of drilodefensins – and of the polyphenol-rich leaf diet – in earthworm biology is underlined by the fact that these compounds constitute 1% or more of the earthworm’s total dry biomass, and 20% of the organism’s total sulphur budget(!) As they conclude, “We have identified the key mechanism for adaptation to a dietary challenge in an animal group that has a major role in organic matter recycling in soils worldwide.”

As so often in science, it’s not enough just to accept that something happens, knowing why/how is so much more satisfying. And maybe as satisfying as a belly-filling meal of leaves is for a vegetarian… In any event it’s research that quite literally breaks the mould.

*These compounds also have anti-fungal potency (e.g. Vincenzo Lattanzio et al., Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects. Phytochemistry: Advances in Research, 23-67). Quite how fungi overcome this dietary-deterrence is another story…

** For those of you keen to see the intralumbrical distribution of drilodefensin (compound 1), the paper includes a very impressive schematic multi-modal three-dimensional model (Fig. 3e) based on micro-computed tomography integrated with imaging mass spectrometry (IMS) techniques to explore metabolite distributions in snap-frozen and cryosectioned earthworms (!).

*** If you are now all excited by earthworm biology/ecology, and would like a pedagogic dimension, there are some interesting activities at Can’t get enough earthworm imagery? Then check out Rosa Fernández et al.Sine Systemate Chaos? A Versatile Tool for Earthworm Taxonomy: Non-Destructive Imaging of Freshly Fixed and Museum Specimens Using Micro-Computed Tomography”.

[Ed. – but surely one of the most surprising aspects of this story is that the article makes no mention of the work of Charles Darwin in the whole importance of earthworm’s biology issue. After all, the Great Man worked for >40 years on his last book, “The Formation of Vegetable Mould Through the Action of Worms, with Observations on Their Habits”. A book which interestingly outsold one of his better-known, previous literary forays – “On the origin of species” – in his lifetime. Oh well, arguably better to be remembered for contribution to biological evolution than biogeochemical revolution..?]