Unravelling Plankton Adaptation in Global Oceans through the Analysis of Lipidomes

A recent global survey of planktonic lipids showed a fundamental temperature-mediated regulation of lipid unsaturation in the global oceans [Holm H, et al. (2022) Science 376:1487-1491]. We expand the analysis of this dataset, both spatially and methodologically, to examine diverse environmental stressors across the ocean. Utilizing weighted correlation network analysis, we analyzed 3,164 lipid features in the dataset comprising 930 samples of suspended particulate matter, taken across a broad range of oceanographic conditions and water depths up to 600 meters. A total of 16 lipid clusters being co-expressed across diverse environments were identified. This analysis reveals universal relationships between environmental factors and the lipidome of the planktonic community. The largest lipid cluster, comprising 481 lipid features, including glycerolipids with polyunsaturated fatty acids, exhibited a significant enrichment in polar oceans, suggesting the highest lipid diversity in these ocean regions. Remarkably, marine plankton in these regions employ both desaturation and chain shortening for cold acclimation. Additionally, one lipid cluster strongly linked to the plankton residing in the surface of tropical and subtropical oceans was enriched with non-phosphorus lipids. We suggest this adaptive response enables the plankton to cope with phosphorous scarcity and heat stress. Notably, in the subsurface of these regions, a co-expressed cluster of highly unsaturated lipids is consistent with an enhanced production of polyunsaturated fatty acids by phytoplankton, possibly for low light adaptation. This adaptation is important as it may represent a source of essential fatty acids below the warm sea surface where such vital compounds may be diminished in the warmer future. SignificanceMarine plankton is vital for marine ecosystems and climate regulation. We analyzed a large lipidomics dataset of 930 samples collected from global oceans. This allowed us to explore how plankton adapt their lipidomes across different environments. Our findings show distinct lipid clusters correlating with specific environmental conditions, revealing mechanisms like chain shortening to cope with cold stress, enrichment of non-phosphorus lipids in tropical surface waters, and increased polyunsaturated fatty acids in low-light tropical subsurface areas. These adaptations are crucial for understanding how climate change will impact marine ecosystems.