Functionalized Membrane Domains: An Ancestral Feature of Archaea?

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.

Novel Intact Polar and Core Lipid Compositions in the Pyrococcus Model Species, P. furiosus and P. yayanosii, Reveal the Largest Lipid Diversity Amongst Thermococcales

“…This IPL composition contrasts with those previously reported for this species, although PI-DGD II was systematically the most abundant IPL detected [ 21 , 22 ]. GMGT-based CL [ 4 , 25 , 26 ] and IPL [ 33 ] have been identified in numerous archaea, including some Thermococcales but, to the best of our knowledge, our study constitutes the first identification of GMGT-based lipids in P. furiosus and the first report of PI-GMGT0-PI XXIV and PI-GTGT0-PI XX as archaeal IPL. By contrast, Sprott et al [ 21 ] tentatively identified PG-based IPL, such as PG-DGD VIII and dihexose(2Hex)-GDGT0-PG XII ( Figure 1 ), in addition to PI-DGD II and PHexNAc-DGD III.…”

“…However, a variety of cyclopentane ring-containing tetraethers, including GTGT with 1 and 2 rings (GTGT1 and 2, XXI and XXII, respectively), GDGT with 1 to 4 rings (GDGT1 to 4, XIII, XV, XVII and XVIII, respectively) and GMGT with 1 to 4 rings (GMGT1 to 4, XXV to XXIIIV, respectively), was obtained upon acidic methanolysis of P. furiosus lipid extract, pre-extracted cells and biomass ( Figure 3 A–C). Correcting for the response factor for diethers relative to tetraethers [ 26 ], we determined that the most abundant CL in the three different methanolysates of P. furiosus were DGD I (ca. 44%, 45% and 36%, respectively) and GMGT0 XXIII (ca.…”

“…The solvent of the resulting CL extracts was removed under reduced pressure, and the extracts were resolubilized in n -hexane/isopropanol (99:1, v/v ). CL analysis was conducted using HPLC coupled with atmospheric-pressure chemical ionization MS (HPLC-APCI-MS) as described in Tourte et al [ 26 ]. Under our analytical conditions, DGD was the only form of diether CL detected, whereas numerous tetraether structures were identified, namely GDGT, GTGT and GMGT and their cyclopentane ring-containing derivatives.…”

“…In order to exhaustively analyze the CL composition of the strains, polar head groups were removed using acid methanolysis (1.2 N HCl in MeOH at 110 • C for 3 h) of ( 1) the total lipid extracts, (2) the cell residue obtained after lipid extraction and (3) the intact cell pellets (26). Because of the low biomass of P. yayanosii, the CL preparation was conducted only on the total lipid extract and the cell residue for this species.…”

“…Additionally, the core lipid compositions of P. furiosus and P. woesei differ greatly from that of other Pyrococcus members, such as P. abyssi, which synthesizes 15% of DGD and 85% of GDGT, including ca. 9% with two cyclopentane rings [23], P. horikoshii, which mostly produces tetraether lipids (>90%) with more than 15% in the GMGT monoalkyl form [24][25][26], and P. kukulkanii, which seemingly produces only diether lipids [27].…”