Coral color morphs exhibit distinct microbial and proteomic profiles linked to stress and immune mechanisms in a changing ocean.
BACKGROUND: Coral phenotypic plasticity facilitates acclimation and adaptation to environmental variability. Coral species often display a variety of color morphs, yet key biological and ecological implications of such phenotypic variation remain underexplored. Here, we present the first proteomic and untargeted lipidomic and metabolomic survey to explore the biological characteristics and potential ecological significance of different color morphs (pink and brown) of healthy Pocillopora verrucosa sampled along a latitudinal gradient. RESULTS: Our multi-omic approach elucidated distinct mechanisms associated with these dominant color morphs. We discovered bacterial indicators specific to each morph: putative pathogens such as Salmonella, Escherichia-Shigella, and carotenoid-producing Gemmatimonas were notably associated with the pink morph, whereas the brown morph was associated with potentially beneficial bacteria, such as Lysobacter, Acinetobacter, and Endozoicomonas. Despite these microbiome differences, the lipidome and metabolome of P. verrucosa were surprisingly homogeneous across colors and locations, suggesting similar metabolic performances during summer conditions. Key polar and apolar lipid classes, such as fatty acids, glycerophosphocholines, and retinoids, were prevalent. Notably, our proteomic analysis revealed morph-specific expressions, with pink morphs exhibiting enhanced levels of GFP-like proteins, Ankyrin, and the enzyme pullulanase, suggesting novel putative protective roles. In contrast, the brown morphs showed a higher abundance of heat shock proteins, indicating putative differential stress response capabilities. CONCLUSION: This comprehensive study provides the first proteomic survey of P. verrucosa and identifies key physiological pathways and trade-offs linked to color morphs, which can further contribute to enhancing our understanding of coral resilience in the face of climate change. SIGNIFICANCE STATEMENT: Understanding the phenotypic plasticity of corals is crucial for uncovering mechanisms of resilience in warming oceans, yet the biological significance of coral color morphs still needs to be explored. Using an innovative multi-omic approach (proteomics, lipidomics, and metabolomics), we provide the first comprehensive analysis of differences between pink and brown morphs of Pocillopora verrucosa. Our data reveal key taxa, potentially pathogenic or beneficial, associated with each morph, and suggest different strategies for each color morph to cope with heat stress, either expressing proteins involved in UV protection and heterotrophic activity or enhanced levels of heat stress resilience and DNA repair. These findings offer insights into the phenotypic plasticity of coral color morphs and their differential responses to climate change. Video Abstract.