Environmentally induced lipidome adaptation in the bacterial model organism M. extorquens

Abstract

Cells, from microbes to man, adapt their membranes in response to the environment to maintain their properties and functions. To adapt, lipid composition is homeostatically regulated to conserve optimal membrane properties. Global patterns of lipidome remodelling are poorly understood, particularly in model organisms with simple lipid compositions that can provide insight into fundamental principles underlying membrane adaptation. Using shotgun lipidomics, we examined the simple yet adaptive lipidome of the plant-associated Gram-negative bacterium Methylobacterium extorquens over varying temperature, hyperosmotic and detergent stress, carbon sources, and cell density. We observed that as few as ten lipids account for 90% of the total changes, thus constraining the upper limit of variable lipids required for an adaptive living membrane. Across all conditions, the highest degree of lipidomic variability was observed for changing growth temperature. We also revealed that variations in lipid structural features are not monotonic over a given range of conditions and are heterogeneous across lipid classes. Interestingly, phosphotidylcholine showed the most extreme acyl chain remodeling among all lipid classes, suggesting a new link to its importance in bacterial-host interactions and pathogenicity. These patterns in lipidomic remodeling suggest a highly adaptive mechanism with many degrees of freedom and constrain the lipidomic requirements for an adaptive membrane.