Spatial metabolomics shows contrasting phosphonolipid distributions in tissues of marine bivalves

Lipids are an integral part of cellular membranes that allow cells to alter stiffness, permeability, and curvature. Among the diversity of lipids, phosphonolipids uniquely contain a phosphonate bond between carbon and phosphorous. Despite this distinctive biochemical characteristic, few studies have explored the biological role of phosphonolipids, although a protective function has been inferred based on chemical and biological stability. We analyzed two species of marine mollusks, the blue mussel Mytilus edulis and pacific oyster Crassostrea gigas, and determined the diversity of phosphonolipids and their distribution in different organs. High-resolution spatial metabolomics revealed that the lipidome varies significantly between tissues within one organ. Despite their chemical similarity, we observed a high heterogeneity of phosphonolipid distributions that originated from minor structural differences. Some phosphonolipids are ubiquitously distributed, while others are present almost exclusively in the layer of ciliated epithelial cells. This distinct localization of certain phosphonolipids in tissues exposed to the environment could support the hypothesis of a protective function in mollusks. This study highlights that the tissue specific distribution of an individual metabolite can be a valuable tool for inferring its function and guiding functional analyses.