Environmental controls on crenarchaeol distributions in hydrothermal springs

Abstract

AbstractThermophilic archaea synthesize cellular membranes composed primarily of isoprenoid glycerol dibiphytanyl glycerol tetraethers (iGDGTs). Cells can adjust the structure of iGDGTs by increasing the number of cyclopentyl rings to enhance lipid packing, thereby decreasing membrane permeability and fluidity to maintain cellular function at high temperature and/or acidic pH. Certain archaea synthesize an iGDGT, crenarchaeol, with four cyclopentyl rings and a unique cyclohexyl ring, the function of which is unknown. Structural modeling suggests the cyclohexyl ring may increase membrane fluidity, potentially representing an adaptation that allowed thermophiles to radiate into cooler environments. To begin to investigate this hypothesis, iGDGT abundance was quantified in forty-one hydrothermal springs in Yellowstone National Park (YNP), USA, and contextualized within a compilation of global hydrothermal spring iGDGTs with pH values of 1.1 to 10.1 and temperatures of 16.3 to 95 °C. pH most strongly correlated with both crenarchaeol abundance and the number of cyclopentyl rings per iGDGT. Crenarchaeol abundance exhibited a nonlinear relationship with both pH and temperature, with highest abundances at pH 7.4 and 46 °C, then decreasing in abundance above and below these values. These observations support the hypothesis that crenarchaeol’s cyclohexyl ring facilitated the adaptation of thermophilic and acidophilic archaea to lower temperature and higher pH niches, enabling their radiation into the marine realm.ImportanceArchaea change the composition of their membrane lipids to alter the fluidity of their membranes to protect cellular functions from environmental stressors. Some archaea 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 hot springs. In addition, the lipid distributions we find support the hypothesis that crenarchaeol facilitated the archaeal evolutionary transition from hot and acidic to cool and neutral waters. We contextualize these findings in a literature compilation that spans the globe.