Transcriptomic and metabolomic analysis of copper stress acclimation in Ectocarpus siliculosus highlights signaling and tolerance mechanisms in brown algae.

Andrés Ritter,Philippe Potin,Simon M Dittami,Catherine Boyen,Thierry Tonon,Juan A Correa,Sophie Goulitquer

doi:10.1186/1471-2229-14-116

Abstract

BackgroundBrown algae are sessile macro-organisms of great ecological relevance in coastal ecosystems. They evolved independently from land plants and other multicellular lineages, and therefore hold several original ontogenic and metabolic features. Most brown algae grow along the coastal zone where they face frequent environmental changes, including exposure to toxic levels of heavy metals such as copper (Cu).ResultsWe carried out large-scale transcriptomic and metabolomic analyses to decipher the short-term acclimation of the brown algal model E. siliculosus to Cu stress, and compared these data to results known for other abiotic stressors. This comparison demonstrates that Cu induces oxidative stress in E. siliculosus as illustrated by the transcriptomic overlap between Cu and H2O2 treatments. The common response to Cu and H2O2 consisted in the activation of the oxylipin and the repression of inositol signaling pathways, together with the regulation of genes coding for several transcription-associated proteins. Concomitantly, Cu stress specifically activated a set of genes coding for orthologs of ABC transporters, a P1B-type ATPase, ROS detoxification systems such as a vanadium-dependent bromoperoxidase, and induced an increase of free fatty acid contents. Finally we observed, as a common abiotic stress mechanism, the activation of autophagic processes on one hand and the repression of genes involved in nitrogen assimilation on the other hand.ConclusionsComparisons with data from green plants indicate that some processes involved in Cu and oxidative stress response are conserved across these two distant lineages. At the same time the high number of yet uncharacterized brown alga-specific genes induced in response to copper stress underlines the potential to discover new components and molecular interactions unique to these organisms. Of particular interest for future research is the potential cross-talk between reactive oxygen species (ROS)-, myo-inositol-, and oxylipin signaling.

Highlights

Brown algae are sessile macro-organisms of great ecological relevance in coastal ecosystems
Brown algae (Kingdom Chromalveolata, Division Heterokontophyta, Class Phaeophyceae) are sessile macro-organisms of great ecological relevance in coastal ecosystems, and belong to an evolutionary lineage that has diverged from land plants and other multicellular organisms more than one billion years ago through secondary endosymbiosis [1]
Algae were incubated in presence of Cu(II) during 8 h at final concentrations of 250 μg L−1 and at 500 μg L−1. These concentrations are comparable to those registered in Cu polluted marine sites where E. siliculosus has been observed [27,28], and correspond to an approximately 400-fold enrichment of the total dissolved Cu content in the natural seawater used to set-up the experiments

Summary

Introduction

Brown algae are sessile macro-organisms of great ecological relevance in coastal ecosystems. Free Cu is found only in traces in eukaryotic cells, where it is tightly controlled by a set of specific transporters and cytosolic chaperones that deliver it to their respective target proteins or organelles [5] At high concentrations, both cupric and cuprous (Cu(II)/Cu(I), E0 = +0.15 V) ions can participate in redox reactions affecting organisms at the cellular level mainly by three well-established processes: (i) direct protein inactivation by undesired amino acid-metal interactions due to the affinity of Cu(II) for thiol-, imidazole-, and carboxyl- groups; (ii) in presence of superoxide or reducing agents Cu(II) can be reduced to Cu(I), which is capable of catalyzing the formation of hydroxyl radicals via the non-enzymatic Fenton’s reaction [6]; (iii) displacement of essential cations from specific binding sites. This metal has been extensively utilized as antifouling agent to prevent the proliferation of algal flora on immersed surfaces

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