Environmental Controls on Crenarchaeol Distributions in Hydrothermal Springs

Thermophilic archaea synthesise cellular membranes composed primarily of isoprenoid glycerol dibiphytanyl glycerol tetraethers (iGDGTs). Cells can adjust the packing of their lipids by increasing cyclopentyl ring production, thereby decreasing membrane permeability and fluidity to maintain cellular function at high temperature, acidic pH, or nutrient limitation. Archaea of the class Nitrososphaeria synthesise crenarchaeol, an iGDGT with four cyclopentyl rings and a cyclohexyl ring, the function of which is unknown. Structural modelling suggests the cyclohexyl ring may increase membrane fluidity, potentially optimising membranes for mesophilic conditions. To investigate the role of crenarchaeol in archaeal membranes in natural settings, we quantify iGDGT compositions of forty-one thermal springs in Yellowstone National Park (YNP), USA, and contextualise these within a global compilation of thermal spring iGDGTs spanning pH values of 1.1-10.1 and temperatures of 16°C-95°C. Spring pH is the strongest predictor of both crenarchaeol relative abundance and the number of cyclopentyl rings per iGDGT. Crenarchaeol relative abundance exhibits a nonlinear relationship with pH and temperature, with highest relative abundances at pH 7.4 and 46°C, decreasing above and below these values. These observations indicate that the cyclohexyl ring of crenarchaeol optimises archaeal cellular membranes for circumneutral and moderate temperature environmental conditions.