Physiological and proteomic responses of Posidonia oceanica to phytotoxins of invasive Caulerpa species

The invasive green algae Caulerpa taxifolia (M. Vahl) C. Agardh, 1817 and Caulerpa cylindracea Sonder, 1845 are widely diffused in the Mediterranean Sea, where they compete for space with the endemic seagrass Posidonia oceanica (Linnaeus) Delile, 1813, a keystone species in Mediterranean marine biodiversity. The present study aims to explore the possible effects of bioactive metabolites from the invasive algae on the seagrass, which may imply an allelopathic action. In particular, the study focuses on the effects of the algal alkaloid caulerpin and the sesquiterpene caulerpenyne. Changes in leaf growth, chlorophyll content, and leaf protein expression of P. oceanica genets under treatments were evaluated after 28 days of cultivation in mesocosms. Caulerpenyne strongly inhibited the growth of adult leaves and the formation of new ones, while inducing the elongation of the intermediate leaves and increased total chlorophyll content; on the contrary, caulerpin did not significantly influence leaf growth and the formation of new ones. A total of 107 differentially accumulated proteins common to the two treatments were also identified using the proteomic approach. Both molecules induced cells to maintain homeostasis, enhancing the amino acid metabolism or fatty acid biosynthesis. Despite these disruptions, P. oceanica demonstrated a more efficient response to stress induced by caulerpin, stimulating the biosynthesis of essential amino acids to maintain cellular homeostasis and mitigate damage caused by reactive oxygen species (ROS). Overall, obtained results supports the possible role of caulerpenyne, and not caulerpin, as an effector in allelopathic interactions among invasive Caulerpa species and P. oceanica in the Mediterranean. • CAU metabolite influenced leaf renewal and longevity in P. oceanica genets, in mesocosm • CYN exerted a strong phytotoxic effects, hindered leaf formation, damaged adult leaves, and stressed leaf meristems. • P. oceanica effectively showed resilence to CAU-induced stress by boosting essential amino acid biosynthesis. • The mesocosm trial results were consistent with observed allelopathic interactions between P. oceanica and Caulerpa species in natural environments.