Abstract
Bacteria and Eukarya organize their plasma membrane spatially into domains of distinct functions. Due to the uniqueness of their lipids, membrane functionalization in Archaea remains a debated area. A novel membrane ultrastructure predicts that monolayer and bilayer domains would be laterally segregated in the hyperthermophilic archaeon Thermococcus barophilus. With very different physico-chemical parameters of the mono- and bilayer, each domain type would thus allow the docking of different membrane proteins and express different biological functions in the membrane. To estimate the ubiquity of this putative membrane ultrastructure in and out of the order Thermococcales, we re-analyzed the core lipid composition of all the Thermococcales type species and collected all the literature data available for isolated archaea. We show that all species of Thermococcales synthesize a mixture of diether bilayer forming and tetraether monolayer forming lipids, in various ratio from 10 to 80% diether in Pyrococcus horikoshii and Thermococcus gorgonarius, respectively. Since the domain formation prediction rests only on the coexistence of di- and tetraether lipids, we show that all Thermococcales have the ability for domain formation, i.e., differential functionalization of their membrane. Extrapolating this view to the whole Archaea domain, we show that almost all archaea also have the ability to synthesize di- and tetraether lipids, which supports the view that functionalized membrane domains may be shared between all Archaea. Hence domain formation and membrane compartmentalization may have predated the separation of the three domains of life and be essential for the cell cycle.
Highlights
Archaea are the main inhabitants of the harshest environments, regardless of whether the extreme conditions are temperature, salinity, hydrostatic pressure, pH, or scarce nutrients
We looked at the ability of Archaea to harbor a differentially functionalized membrane, by focalizing on the diether/tetraether domain formation, which is the easiest to assess at the phylum level since it can be inferred from the sole analysis of membrane core lipid compositions
It confirmed the synthesis of previously undetected tetraether lipids, showing that all Thermococcales are able to synthesize both di- and tetraethers. These findings show that the membrane organization proposed for T. barophilus could be extended to the whole Thermococcales order and suggest that the ability to synthesize diethers and/or tetraethers could be inferred from taxonomically related species
Summary
Archaea are the main inhabitants of the harshest environments, regardless of whether the extreme conditions are temperature, salinity, hydrostatic pressure, pH, or scarce nutrients. No strong correlation have been highlighted for other extremes, nor for mesophilic conditions, which raises questions as to how archaea thriving in such habitats adapt to their specific lifestyles. This suggests that some environmental stress factors are not strong enough to drive measurable compositional shifts in membrane lipids or may involve adaptive routes not requiring an alteration of the diether/tetraether ratio, or that unknown alternative adaptive routes exist in Archaea
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