Metabolomics and Microbiomics Insights into the Differential Surface Fouling of Brown Algae

Marine macroalgae (seaweeds) are key components of marine ecosystems with vital roles in costal habitats. As they release dissolved organic matter and other molecules, seaweeds are under strong settlement pressure by micro- and macro-epibionts. Uncontrolled epibiosis causes surface fouling with detrimental effects on the health and well-being of the organism. Seaweeds control surface epibionts directly by releasing antifouling and antimicrobial metabolites onto their surfaces, and indirectly by recruiting beneficial microorganisms that produce antimicrobial/antifouling metabolites. Three species of the brown algal genus Fucus, F. vesiculosus (FV), F. serratus (FS) and F. distichus subsp. evanescens (FE) form the Fucus belt habitat in the Kiel Fjord, Germany. They often co-occur in the same spot but their blades are fouled differently; we observed FE to be the least fouled, and FV to be the most fouled species. This study was designed to investigate the potential factors underlying different fouling intensities on the surfaces of the three co-occurring Fucus spp. Their surface metabolomes were analysed by comparative untargeted UPLC-MS/MS based metabolomics to identify marker metabolites influencing the surface fouling. The epiphytic microbial communities of the Fucus spp. were also comparatively characterized by high-throughput amplicon sequencing to identify the differences in the surface microbiome of the algae. By employing these omics methods, integrated with multivariate analyses, we identified discriminant metabolites and microbial taxa associated with FE surface, including antimicrobial polar lipids, the fungal genera Mucor, Alternaria, and bacterial genus Yoonia-Loktanella. These taxa have been previously reported to produce antimicrobial and antifouling compounds, suggesting their potential involvement in the fouling resistance (least fouled) observed on the FE surface relative to the co-occurring algae FS and FV. These findings shed light on the surface metabolome and microbiome of Fucus spp. and their influence in different fouling intensities and also have implications for the conservation of coastal habitats.