Amenabar, M. J. | bioRxiv Science

bioRxiv2024

Environmental controls on crenarchaeol distributions in hydrothermal springs

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.

microbiology↗

bioRxiv2023

Mode of carbon and energy metabolism shifts lipid composition in the thermoacidophile Acidianus

The degree of cyclization, or ring index (RI), in archaeal glycerol dibiphytanyl glycerol tetraether (GDGT) lipids was long thought to reflect homeoviscous adaptation to temperature. However, more recent experiments show that other factors (e.g., pH, growth phase, and energy flux) can also affect membrane composition. The main objective of this study was to investigate the effect of carbon and energy metabolism on membrane cyclization. To do so we cultivated Acidianus sp. DS80, a metabolically flexible and thermoacidophilic archaeon, on different electron donor, acceptor and carbon source combinations (S0/Fe3+/CO2, H2/Fe3+/CO2, H2/S0/CO2, or H2/S0/glucose). We show that differences in energy and carbon metabolism can result in over a full unit of change in RI in the thermoacidophile Acidianus sp. DS80. The patterns in RI correlated with the normalized electron transfer rate between electron donor and acceptor and did not always align with thermodynamic predictions of energy yield. In light of this, we discuss other factors that may affect the kinetics of cellular energy metabolism: electron transfer chain (ETC) efficiency, location of ETC reaction components (cytoplasmic vs. extracellular), and the physical state of electron donors and acceptors (gas vs. solid). Furthermore, assimilation of a more reduced form of carbon during heterotrophy appears to decrease the demand for reducing equivalents during lipid biosynthesis, resulting in lower RI. Together, these results point to the fundamental role of the cellular energy state in dictating GDGT cyclization, with those cells experiencing greater energy limitation synthesizing more cyclized GDGTs. ImportanceSome archaea make unique membrane-spanning lipids with different numbers of five or six membered rings in the core structure that modulate membrane fluidity and permeability. Changes in membrane core lipid composition reflect fundamental adaptation strategies of archaea in response to stress, but multiple environmental and physiological factors may affect the needs for membrane fluidity and permeability. In this study, we tested how Acidianus sp. DS80 changed its core lipid composition when grown with different electron donor/acceptor pairs. We show that changes in energy and carbon metabolisms significantly affected the relative abundance of rings in the core lipids of DS80. These observations highlight the need to better constrain metabolic parameters, in addition to environmental factors, that may influence changes in membrane physiology in Archaea. Such consideration would be particularly important for studying archaeal lipids from habitats that experience frequent environmental fluctuations and/or where metabolically diverse archaea thrive.

microbiology↗