Which Specialized Metabolites Does the Native Subantarctic Gastropod Notodiscus hookeri Extract from the Consumption of the Lichens Usnea taylorii and Pseudocyphellaria crocata?

Alice Gadea,Maryvonne Charrier,Grichka Biver,Françoise Le Dévéhat,Anne-Cécile Le Lamer,Joël Boustie,Pierre Le Pogam

doi:10.3390/molecules22030425

Abstract

Notodiscus hookeri is the only representative of terrestrial gastropods on Possession Island and exclusively feeds on lichens. The known toxicity of various lichen metabolites to plant-eating invertebrates led us to propose that N. hookeri evolved means to protect itself from their adverse effects. To validate this assumption, the current study focused on the consumption of two lichen species: Usnea taylorii and Pseudocyphellaria crocata. A controlled feeding experiment was designed to understand how the snail copes with the unpalatable and/or toxic compounds produced by these lichen species. The occurrence of two snail ecophenotypes, represented by a mineral shell and an organic shell, led to address the question of a metabolic response specific to the phenotype. Snails were fed for two months with one of these lichens and the chemical profiles of biological samples of N. hookeri (i.e., crop, digestive gland, intestine, and feces) were established by HPLC-DAD-MS and compared to that of the lichens. N. hookeri appears as a generalist lichen feeder able to consume toxic metabolite-containing lichens, independently of the ecophenotype. The digestive gland did not sequester lichen metabolites. The snail metabolism might be based on four non-exclusive processes according to the concerned metabolites (avoidance, passive transport, hydrolysis, and excretion).

Highlights

Lichens are fascinating self-sustaining partnerships consisting of a fungus and a photobiont partner
The diverse strategies implemented by N. hookeri to circumvent the toxicity of their lichen metabolites are discussed
As an exclusive lichen-feeder, Notodiscus hookeri depends on a trophic resource containing several series of toxic metabolites, especially towards invertebrates

Summary

Introduction

Lichens are fascinating self-sustaining partnerships consisting of a fungus and a photobiont partner (in most cases, green algae are sometimes replaced or accompanied by cyanobacteria) Owing to their nutritional autonomy, lichens tend to dominate nutrient-poor, cold and/or dry environments. Due to the extracellular distribution of lichen specialized metabolites, these substances can be non-destructively extracted with acetone through the so-called acetone-rinsing technique without harming the lichen symbionts, offering a powerful experimental setup to evaluate the deterrent functions of lichen metabolites against plant-eating species [7] Using such experimental design, several authors emphasized deterrence and/or toxicity of either pure substances of various structural classes or crude lichen extracts towards insect larvae, moth larvae, bank voles, slugs, and snails (for review, see [3])

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