Abstract
Elucidating the lipidome of Archaea is essential to understand their tolerance to extreme environmental conditions. Previous characterizations of the lipid composition of Pyrococcus species, a model genus of hyperthermophilic archaea belonging to the Thermococcales order, led to conflicting results, which hindered the comprehension of their membrane structure and the putative adaptive role of their lipids. In an effort to clarify the lipid composition data of the Pyrococcus genus, we thoroughly investigated the distribution of both the core lipids (CL) and intact polar lipids (IPL) of the model Pyrococcus furiosus and, for the first time, of Pyrococcus yayanosii, the sole obligate piezophilic hyperthermophilic archaeon known to date. We showed a low diversity of IPL in the lipid extract of P. furiosus, which nonetheless allowed the first report of phosphatidyl inositol-based glycerol mono- and trialkyl glycerol tetraethers. With up to 13 different CL structures identified, the acid methanolysis of Pyrococcus furiosus revealed an unprecedented CL diversity and showed strong discrepancies with the IPL compositions reported here and in previous studies. By contrast, P. yayanosii displayed fewer CL structures but a much wider variety of polar heads. Our results showed severe inconsistencies between IPL and CL relative abundances. Such differences highlight the diversity and complexity of the Pyrococcus plasma membrane composition and demonstrate that a large part of its lipids remains uncharacterized. Reassessing the lipid composition of model archaea should lead to a better understanding of the structural diversity of their lipidome and of their physiological and adaptive functions.
Highlights
Archaea are ubiquitous in all Earth ecosystems due to peculiar physiological features that allow them to withstand environmental conditions ranging from the mildest to the harshest
We show that P. yayanosii synthesizes phosphatidylinositol-based intact polar lipids (IPL) with typical DGD and GDGT cores, while several novel IPL and core lipids (CL) could be identified in P. furiosus, notably GMGT and GDGT with up to four cyclopentane rings
The analysis of the total lipid extracts from Pyrococcus furiosus, P. yayanosii and Thermococcus kodakarensis obtained with our modified Bligh and Dyer (B&D) extraction procedure showed various IPL structures and distinct lipid compositions in these three closely related hyperthermophilic archaea (Figure 2)
Summary
Archaea are ubiquitous in all Earth ecosystems due to peculiar physiological features that allow them to withstand environmental conditions ranging from the mildest to the harshest. One of these peculiarities lies in the structure of their cell membranes, which are composed of lipids of divergent structures and properties from the typical fatty-acyl phospho- and glyco-lipids found in Bacteria and Eukarya. The hydrophobic core of archaeal lipids is made of C20, C25 and C40 isoprenoid hydrocarbon chains linked to a glycerol backbone in an sn-2,3 configuration by ether bonds, creating cell membranes with enhanced impermeability and stability compared to that of Bacteria and Eukarya [1,2]. The polar head group diversity of archaea mostly resembles that typical for bacterial/eukaryal lipids, with the existence of phospho- and glyco-lipids deriving from sugars [8], aminoacids [9] or combinations of both [9]
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