Evolution of Wax Esters as Storage Lipids in Microbial Mats

Lakes in Warner Valley, Oregon, experience significant changes in water balance caused by seasonality to decadal scale droughts. Throughout the system, microbial mats in the lakes, playas, and springs are controlled by temperature and water chemistry, augmented by seasonally dynamic microbial populations that respond to profound shifts in temperature, pH and ion and metal concentrations. The compositions and distributions of wax esters (WE) are unprecedented, and vary among the different hydration states of equivalent microbial mats. WE are low in abundance among the lipids from the non-saponified toluene eluate fraction of live mats (submerged and emergent) whereas they dominate analogous desiccated mats and mats from other evaporatively concentrated lakes within the basin. WE in desiccated mats range from C₂₆ to C₅₀ and are comprised of a simpler range of carboxylic acid moieties than those found in marine and hot spring environments, except that they include isoprenoid components previously observed among the lipids of marine bacteria fed phytol and the plant genus Arabidopsis. The longer chain length of the WE from the Warner Valley is consistent with lower solubilities and greater resistance to degradation and oxidation with desiccation. Moreover, aeolian transport of desiccated mat-rip-ups between lake flats allows for migration of microbial communities within and between lake flats and basins during arid conditions. Seasonal rehydration of this environment can then be considered a natural saponification step where initial hydration allows for regeneration of acids and alcohols. Breakdown of WE thereby provides storage lipids and the resulting high molecular weight materials for cell walls for the next viable microbial generation. This represents a significant evolutionary pathway in lipid biosynthesis and usage. Production of WE may have facilitated microbial migration to the lake environments that represented the earliest terrestrial ecosystems, and survival through the Great Oxygenation Event.