Environmental controls on crenarchaeol distributions in hydrothermal springs

Abstract

Thermophilic archaea synthesize cellular membranes composed primarily of isoprenoid glycerol dibiphytanyl glycerol tetraethers (iGDGTs). Cells can adjust the packing of their lipids by increasing the number of cyclopentyl rings during lipid synthesis, thereby decreasing membrane permeability and fluidity to maintain cellular function at high temperature, acidic pH, or nutrient limitation. Archaea of the class Nitrososphaeria synthesize an iGDGT, crenarchaeol, with four cyclopentyl rings and a cyclohexyl ring, the function of which is unknown. Structural modeling suggests the cyclohexyl ring may increase membrane fluidity, potentially optimizing membranes for mesophilic conditions. To begin to investigate this hypothesis, iGDGT composition was quantified in forty-one thermal springs in Yellowstone National Park (YNP), USA, and contextualized within a global thermal spring iGDGT compilation with pH values of 1.1 to 10.1 and temperatures of 16 to 95{degrees}C. pH was the strongest predictor of both crenarchaeol relative abundance and the number of cyclopentyl rings per iGDGT. Crenarchaeol relative abundance exhibited a nonlinear relationship with pH and temperature, with highest relative abundances at pH 7.4 and 46{degrees}C, then decreasing above and below these values. These observations are consistent with the hypothesis that the cyclohexyl ring of crenarchaeol optimizes archaeal cellular membranes for circumneutral and moderate temperature environmental conditions. ImportanceArchaea change the composition of their membrane lipids to alter the fluidity of their membranes to maintain cell homeostasis when confronted with environmental stress. Some archaea of the class Nitrososphaeria produce a lipid, crenarchaeol, with a unique six-membered ring, the effect of which on archaeal membrane dynamics remains unknown. In this study, we identify pH as the most important geochemical variable for archaeal membrane response in Yellowstone National Park thermal springs. In addition, the lipid distributions indicate that crenarchaeol production is highest in circumneutral and mesophilic environments. The YNP results are supported by similar trends across global thermal springs.