Surface chemical defence of the eelgrass Zostera marina against microbial foulers

Stefano Papazian,Delphine Parrot,Florian Weinberger,Deniz Tasdemir,Barbora Burýšková

doi:10.1038/s41598-019-39212-3

Stefano Papazian, Delphine Parrot + Show 3 more

Open Access

https://doi.org/10.1038/s41598-019-39212-3

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Abstract

Plants rely on both mechanical and chemical defence mechanisms to protect their surfaces against microorganisms. The recently completed genome of the eelgrass Zostera marina, a marine angiosperm with fundamental importance for coastal ecosystems, showed that its re-adaptation from land to the sea has led to the loss of essential genes (for chemical communication and defence) and structural features (stomata and thick cuticle) that are typical of terrestrial plants. This study was designed to understand the molecular nature of surface protection and fouling-control strategy of eelgrass against marine epiphytic yeasts. Different surface extraction methods and comparative metabolomics by tandem mass spectrometry (LC-MS/MS) were used for targeted and untargeted identification of the metabolite profiles of the leaf surface and the whole tissue extracts. Desorption electrospray ionization-imaging mass spectrometry (DESI-IMS) coupled with traditional bioassays revealed, for the first time, the unique spatial distribution of the eelgrass surface-associated phenolics and fatty acids, as well as their differential bioactivity against the growth and settlement of epiphytic yeasts. This study provides insights into the complex chemical defence system of the eelgrass leaf surface. It suggests that surface-associated metabolites modulate biotic interactions and provide chemical defence and structural protection to eelgrass in its marine environment.

Highlights

Seagrass meadows are widespread along the coastlines of the world oceans, where they prevent sediment erosion and provide numerous animal species with food and shelter, supporting the stability of marine habitats[1]
These include the classical ‘surface dipping’ method, which involves the brief immersion of the leaves in organic solvents[19], or the solid-phase extraction method, recently developed for studying seaweed surfaces, in which chemicals are first adsorbed onto C18 material and eluted with a solvent[24]
When dose responses of the surface and whole leaf tissue extracts were related to 1-fold concentrations found in Z. marina[19], all models showed selective inhibition against either growth or settlement of the yeasts (Supplementary Figs S22–S24)

Summary

Introduction

Seagrass meadows are widespread along the coastlines of the world oceans, where they prevent sediment erosion and provide numerous animal species with food and shelter, supporting the stability of marine habitats[1]. These include the classical ‘surface dipping’ method, which involves the brief immersion of the leaves in organic solvents[19], or the solid-phase extraction method, recently developed for studying seaweed surfaces, in which chemicals are first adsorbed onto C18 material and eluted with a solvent[24] Both methods are tedious and entail limitations, e.g. poor recovery or reproducibility, potential degradation of the compounds, and the risk of physical or chemical damage to the tissues, which result in the co-extraction of metabolites from the epidermis. DESI-IMS is a versatile tool in chemical ecology for spatial analysis of biological surfaces and for the identification of host-microbe interactions, as demonstrated by pioneering studies on seaweeds and corals[29,30]

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