Ecological lipidology

Abstract

Dietary lipids (DLs), particularly sterols and fatty acids, are precursors for endogenous lipids that, unusually for macronutrients, shape cellular and organismal function long after ingestion. These functions - cell membrane structure, intracellular signalling, and hormonal activity - vary with the identity of DLs, and scale up to influence health, survival, and reproductive fitness, thereby affecting evolutionary change. Our Ecological Lipidology approach integrates biochemical mechanisms and molecular cell biology into evolution and nutritional ecology. It exposes our need to understand environmental impacts on lipidomes, the lipid specificity of cell functions, and predicts the evolution of lipid-based diet choices. Broad interdisciplinary implications of Ecological Lipidology include food web alterations, species responses to environmental change, as well as sex differences and lifestyle impacts on human nutrition, and opportunities for DL-based therapies.

Keywords: cell biology; diet choice; ecology; fatty acids; fitness; food web; membrane; sterols.

Figure 1.. Lipids influence cell membrane properties.

Dietary lipids (DLs) integrate into cell membranes where they have vital cellular functions that ultimately influence reproductive fitness (see Table 1). Phosphoglycerolipids are polar, with a hydrophilic ‘head’ and hydrophobic ‘tail’. In cell membranes, they are oriented with heads on the outside to the extracellular environment, the tails on the inside towards the cell interior. Sterols are also incorporated, and can be locally enriched to affect membrane properties in specific areas. The lipid profile differs between the inner and outer leaflets, reflecting their different biological functions. The lipid profile of a membrane determines its diffusion properties, fluidity, curvature, and width (Harayama and Riezman, 2018). The quantity of membrane sterols, as well as the amount, chain length, and saturation, of fatty acids that form phospholipids and sphingolipids influence the amount of water interspersed in the membrane leaflets. For example, cis unsaturation in the tails of fatty acids change the angle between neighbouring carbons and generate a kink, creating space for water molecules to intersperse, which in turn increases membrane fluidity. Similarly, the unequal distribution of sterols in the leaflets can result in asymmetries (Steck and Lange, 2018), and facilitate membrane curvature. Curvature determines molecular transport and endocytosis but reduces stiffness and integrity, and its maintenance likely incurs energetic costs (Stachowiak et al., 2013). Membrane width is mostly defined by fatty acid chain length, however, their saturation type and abundance is also important. Membrane width influences the insertion of transmembrane proteins and is thus a critical variable for the protein sorting machinery in the cellular organelles, including the Golgi apparatus or the endoplasmatic reticulum.

Figure 2.. Specific lipid requirements may alter lipid flux through food webs.

Producer dietary lipids (DLs) (e.g., plant lipids A to C, left panel, lower section) are the source that consumers use in tailoring their lipid profiles to meet lipid-mediated body functions (black solid lines and icons) other than mere energy provision. For instance, a herbivorous invertebrate acquires three types of DL from plants (Lipids A to C) and produces one itself (Lipid D, middle panel, lower section). The lipid identity may change if, as in some herbivorous insects, dietary plant sterols are converted to cholesterol (reviewed in Behmer and Nes, 2003; Jing and Behmer, 2020). A consumer that feeds on the herbivore and/or the plant acquires three lipids (A, B, and D) but is either unable to take up lipid C, or lipid C is available in insufficient concentration (right panel, lower section). Quantitative DL availability changes throughout food webs; in this example, the concentration of all lipids (x-axis, lower section) decreases up the food chain. Qualitative DL availability also changes because Lipids C, D, and E are only found in some species. Variation in quantitative and qualitative DL demand is driven by ecological changes – any resulting deficiencies must be countered by alternative sources of DLs (red arrows and icons). In this example, the low concentration of lipid A in the consumer suffices to enable its role in signalling and no additional uptake is needed (Lavrynenko et al., 2015). Lipid D is a hormone precursor in the consumer but requires structural change to function as a hormone. Under changing environment, such as temperatures, Lipid E, substitutes for the lack of Lipid C due to absorption problems, is needed by the consumer to enable thermal resistance (qualitative limitation). If the quantity of Lipid B is insufficient in the herbivore under an ecological change, an alternative source for Lipid B must be found (quantitative limitation). In nature, many example of such changes in food webs exist, such as scavenging on animal corpses or feeding on pollen by otherwise herbivorous insects (see photographs top section). Ecological Lipidology predicts that acquiring the same lipid from different sources (Lipid B from mouse carcass) or different but functionally similar lipids (Lipid E replacing Lipid C in the chicken) will mainly occur when the environment changes.