The cuticle lamellae responsible for structural coloration in red algae display common features with the metazoan extracellular matrix

Structural coloration is a physical phenomenon observed in many living organisms, including seaweeds, via the formation of highly organized nanostructures. Although the deposition of multilayer thin-film in the extracellular matrix (ECM) is a widespread characterized system, enabling light interference, to date such lamellae have only been described in the cuticle of red algae belonging to the Gigartinaceae family within macroalgae. Here, we determine the composition of the multilayered cuticle components in the model species Chondrus crispus (Rhodophyta), using genomic, transcriptomic, proteomic, metabolomic and analytical profiling of carbohydrates. The complex structural assembly revealed common features with the ECM of animals. The carbohydrate fraction consists of a complex mixture of ECM carrageenans and glycosaminoglycan-like structures. A major von Willerbrand factor A domain (VWA) protein plays a critical role for the adhesion of macromolecules, including protein-protein interactions and to sulfated polysaccharides. We propose the name of Lamellae Cohesive Protein (LCP) regarding the alternate distribution of chemically distinct constituents within the cuticle. For the first time, we identified major proteins of the algal cuticle, providing a framework for addressing the evolutionary origins of the algal cuticle biosynthesis and raise important questions regarding its role, particularly across the life cycle marked by major structural ECM modifications.