Pressure effects on the composition and thermal behavior of lipids from the deep-sea thermophile Methanococcus jannaschii

Abstract

The deep-sea archaeon Methanococcus jannaschii was grown at 86؇C and under 8, 250, and 500 atm (1 atm ‫؍‬ 101.29 kPa) of hyperbaric pressure in a high-pressure, high-temperature bioreactor. The core lipid composition of cultures grown at 250 or 500 atm, as analyzed by supercritical fluid chromatography, exhibited an increased proportion of macrocyclic archaeol and corresponding reductions in archaeol and caldarchaeol compared with the 8-atm cultures. Thermal analysis of a model core-lipid system (23% archaeol, 37% macrocyclic archaeol, and 40% caldarchaeol) using differential scanning calorimetry revealed no well-defined phase transition in the temperature range of 20 to 120؇C. Complementary studies of spin-labeled samples under 10 and 500 atm in a special high-pressure, high-temperature electron paramagnetic resonance spectroscopy cell supported the differential scanning calorimetry phase transition data and established that pressure has a lipid-ordering effect over the full range of M. jannaschii's growth temperatures. Specifically, pressure shifted the temperature dependence of lipid fluidity by ca. 10؇C/500 atm.For archaea to flourish in the extreme environments that many inhabit, normal membrane structure and function must be preserved. Preservation of membrane function may derive partly from the unique physical structures of archaeal lipids, which differ greatly from those of their eubacterial counterparts (7,(16)(17)(18). In contrast to the straight or minimally branched, mostly unsaturated fatty acids of variable lengths found in eubacteria, archaeal apolar chains are based on saturated isopranoid alcohols typically containing 20 or 40 carbon atoms. These isopranyl chains are connected to a glycerol (or more rarely, a complex polyol) head group by ether bonds, not the fatty acid ester bonds common to eubacteria. Moreover, the stereochemistry of these ether lipids (D or sn-2,3) is opposite to that seen in eubacteria (L or sn-1,2). Some archaea also possess bilayer-spanning tetraether lipids, in which a pair of biphytanyl-based chains are linked to two glycerol moieties via ether bonds. In total, the structural differences are pronounced enough to raise the question of whether archaeal lipids respond differently to temperature and pressure than do eubacterial lipids, thus contributing to microbial viability under extreme conditions.Given that eubacterial thermophiles and barophiles do exist (6), the unique structural features of archaeal lipids are not necessarily required for retention of membrane structure and function at elevated temperatures and pressures. However, considering the abundance of archaea and relative scarcity of eubacteria at the outer regions of the pressure-temperature envelope at which life is known to exist, many archaea appear to possess an intrinsic capacity for thermophilic and barophilic behavior.To adapt to moderate fluctuations in temperature, virtually all eubacteria can maintain optimal membrane fluidity by modulating their lipid composition in a process termed homeoviscous ad...

High‐pressure systems for gas‐phase free continuous incubation of enriched marine microbial communities performing anaerobic oxidation of methane

“…For the study and isolation of piezophilic microorganisms also sampling and incubation devices were developed and applied which allow processing of microbiological samples without depressurization (Kato, 2006 andreferences therein, Parkes et al, 2009). Two-phase batch incubation techniques with gas enrichment resulting from free-gas have also been described (Berberich et al, 2000;Boonyaratanakornkit et al, 2007;Kaneshiro and Clark, 1995;Knutson et al, 1999;Malahoff et al, 2002;Miller et al, 1989;Nelson et al, 1992). Further, several systems for high-pressure fed-batch or continuous incubation were designed and described (Houghton et al, 2007;Jannasch et al, 1996;Wirsen and Molyneaux, 1999).…”

Differential Effects of Permeating and Nonpermeating Solutes on the Fatty Acid Composition of Pseudomonas putida

“…We cannot state conclusively that these observations represent homeoviscous adaptation of membrane fluidity until physical measurements of membrane viscosity are made. However, studies of other organisms have shown a strong correlation between temperature-and pressure-induced changes in lipid composition and maintenance of membrane fluidity (27,43). Additional studies will allow us to determine whether membrane fluidity is altered by matric water stress, whether other physiological strategies are employed to counter the membrane destabilizing effects of cellular dehydration, and whether the same enzyme is responsible for the cis-to-trans and trans-to-cis isomerization activities.…”

“…Sucrose and trehalose can depress the phase transition temperature during desiccation and may contribute to the ability of many microorganisms to survive desiccation by maintaining the fluidity of the membrane (9,15,40). Bacteria that are exposed to low matric water potentials may adjust membrane fatty acid composition or make other adaptations to offset the lipidsolidifying effects of dehydration in a fashion that is analogous to the homeoviscous adaptation of membrane fluidity to changes in temperature (30,43) or hyperbaric pressure (12,27). The phospholipid fatty acid (PLFA) profiles of subsurface bacteria have been previously shown to change during starvation and desiccation in a porous medium, although it is difficult to separate desiccation effects from starvation effects, since both stresses can occur simultaneously during air drying of a porous medium (28).…”

Temperature resistance studies on the deep-sea vent shrimpMirocaris fortunata

“…Pressure is another possible factor that may cause differences in thermal biology of a given species. Pressure-dependant thermal characteristics have been reported for various biological systems, from isolated biomolecules to whole organisms (Summit et al, 1998;Kaneshiro and Clark, 1995;Holden and Baross, 1995;Kaneko et al, 2000). Temperature resistance properties of M. fortunata do not appear to be influenced by depth of occurrence, at least in the 800-1700·m depth range.…”