Differential impact of copper stress in two Ectocarpales: metabolic disruption and defensive signaling in the free-living Ectocarpus sp7 and the endophytic Laminarionema elsbetiae

Abstract

Algae are photosynthetic organisms, responsible for the primary production in oceans and lakes. Brown algae have evolved independently from other major eukaryotic lineages, such as the Opistokonts (animals, fungi) or Archaeplastida (land plants, green and red algae). Within this lineage, there is considerable variation between species, which differ in ecology, diversity, and evolutionary features, suggesting specific adaptations in their changing marine environment. In this context, several questions remain regarding the evolution of brown algal metabolism, particularly in response to oxidative stress. This study explored the consequences of copper stress on two brown algae from the Ectocarpales order: the free-living Ectocarpus sp7 and the endophytic Laminarionema elsbetiae. Using PAM-based fluorescence measurements, we revealed that high copper exposure reduces the photosynthetic capacity and activity of the endophyte. Through a cutting-edge untargeted metabolomic approach using UHPLC-HRMS profiling, we detected metabolic alterations induced by short-term exposure to moderate copper concentration in both free-living and endophytic Ectocarpales. The metabolite-regulated response appears to be substantial in Ectocarpus sp7 compared to L. elsbetiae, as a greater number of up- and down-regulated features were detected. Among the discriminant ions identified by tandem mass spectrometry, our results confirmed that copper exposure triggers the metabolism of algal defense signaling, primarily through the upregulation of oxylipins, but mainly in Ectocarpus sp 7. Altogether, our findings suggest that in Ectocarpales, fine metabolic adaptation may have altered the metabolism linked to defense signaling, such as the oxylipin pathway, particularly in ecological niches like endophytic life.