Apolar Polyisoprenoids Located in the Midplane of the Bilayer Regulate the Response of an Archaeal-Like Membrane to High Temperature and Pressure

LoRicco, Josephine G; Salvador-Castell, Marta; Demé, Bruno; Peters, Judith; Oger, Philippe

doi:10.3389/fchem.2020.594039

Cited by 7 publications

(8 citation statements)

References 63 publications

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“…This is representative of a general phenomenon as other studies have shown that isoprenoid compounds, e.g., squalene or hydrocarbons such as hexadecane, also localize in the midplane. 25,92,94,95 The assembly of MK8 and MKOL8 are found to mix well, with head−head pair distribution function showing the first interaction shell located at a distance around 6 Å.…”

Section: ■ Conclusionmentioning

confidence: 94%

Location and Conformational Ensemble of Menaquinone and Menaquinol, and Protein–Lipid Modulations in Archaeal Membranes

et al. 2021

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Halobacteria, a type of archaea in high salt environments, have phytanyl ether phospholipid membranes containing up to 50% menaquinone. It is not understood why a high concentration of menaquinone is required and how it influences membrane properties. In this study, menaquinone-8 headgroup and torsion parameters of isoprenoid tail are optimized in the CHARMM36 force field. Molecular dynamics simulations of archaeal bilayers containing 0 to 50% menaquinone characterize the distribution of menaquinone-8 and menaquinol-8, as well as their effects on mechanical properties and permeability. Menaquinone-8 segregates to the membrane midplane above concentrations of 10%, favoring an extended conformation in a fluid state. Menaquinone-8 increases the bilayer thickness but does not significantly alter the area compressibility modulus and lipid chain ordering. Counterintuitively, menaquinone-8 increases water permeability because it lowers the free energy barrier in the midplane. The thickness increase due to menaquinone-8 may help halobacteria ameliorate hyper-osmotic pressure by increasing the membrane bending constant. Simulations of the archaeal membranes with archaerhodopsin-3 show that the local membrane surface adjusts to accommodate the thick membranes. Overall, this study delineates the biophysical landscape of 50% menaquinone in the archaeal bilayer, demonstrates the mixing of menaquinone and menaquinol, and provides atomistic details about menaquinone configurations.

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Section: ■ Conclusionmentioning

confidence: 94%

Location and Conformational Ensemble of Menaquinone and Menaquinol, and Protein–Lipid Modulations in Archaeal Membranes

et al. 2021

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“…Those diether-exclusive extremophiles (e.g., A pernix ) also contain apolar polyisoprenoids such as lycopanes (major component) and squalenes (minor components). Using synthetic diether lipids, i.e., 1,2-di- O -phytanyl- sn -glycero-3-phosphocholine (DoPhPC) and 1,2-di- O -phytanyl- sn -glycero-3-phosphoethanolamine (DoPhPE) and neutron diffraction, as well as other physical techniques, Oger’s group and his collaborators showed that the apolar molecules (squalane) can intercalate into the diether bilayer mid-plane space in parallel with the membrane surface (illustrated in Figure 2 ), reducing proton permeability, inducing negative membrane curvature, and creating non-lamellar structures at high temperatures and high pressures [ 22 , 33 ]. This unusual membrane structure (right panel, Figure 2 ) has been proposed as an adaptation strategy of those hyperthermophiles, with only diether lipids, to cope with extremely harsh environments such as high growth temperatures [ 21 , 22 , 33 ].…”

Section: Vesicular Archaea Lipid Membranes (Archaeosomes)mentioning

confidence: 99%

“…Using synthetic diether lipids, i.e., 1,2-di- O -phytanyl- sn -glycero-3-phosphocholine (DoPhPC) and 1,2-di- O -phytanyl- sn -glycero-3-phosphoethanolamine (DoPhPE) and neutron diffraction, as well as other physical techniques, Oger’s group and his collaborators showed that the apolar molecules (squalane) can intercalate into the diether bilayer mid-plane space in parallel with the membrane surface (illustrated in Figure 2 ), reducing proton permeability, inducing negative membrane curvature, and creating non-lamellar structures at high temperatures and high pressures [ 22 , 33 ]. This unusual membrane structure (right panel, Figure 2 ) has been proposed as an adaptation strategy of those hyperthermophiles, with only diether lipids, to cope with extremely harsh environments such as high growth temperatures [ 21 , 22 , 33 ]. At present, it is not clear whether this unusual membrane structure (e.g., right panel, Figure 2 ) can occur in PLFM archaeosomes made of C 25,25 -archaeols and whether archaea diether bilayers with intercalated apolar isoprenoids are better nano-carriers of therapeutics than those without an apolar isoprenoid.…”

Section: Vesicular Archaea Lipid Membranes (Archaeosomes)mentioning

confidence: 99%

“… ( Left ) Structures of diether lipids in the polar lipid methanol fraction (PLMF) extracted from the hyperthermophile Aeropyrum pernix . ( Right ) Putative membrane structure containing AI (blue circles), AGI (red circles), and the apolar molecule squalane, which resides in the mid-plane space of diether bilayers, similar to the case of squalane in DoPhPC as revealed by neutron diffraction [ 21 , 22 , 23 , 24 , 25 ]. …”

Section: Figurementioning

confidence: 99%

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Vesicular and Planar Membranes of Archaea Lipids: Unusual Physical Properties and Biomedical Applications

Chong

Chang

et al. 2022

IJMS

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Liposomes and planar membranes made of archaea or archaea-like lipids exhibit many unusual physical properties compared to model membranes composed of conventional diester lipids. Here, we review several recent findings in this research area, which include (1) thermosensitive archaeosomes with the capability to drastically change the membrane surface charge, (2) MthK channel’s capability to insert into tightly packed tetraether black lipid membranes and exhibit channel activity with surprisingly high calcium sensitivity, and (3) the intercalation of apolar squalane into the midplane space of diether bilayers to impede proton permeation. We also review the usage of tetraether archaeosomes as nanocarriers of therapeutics and vaccine adjuvants, as well as the biomedical applications of planar archaea lipid membranes. The discussion on archaeosomal therapeutics is focused on partially purified tetraether lipid fractions such as the polar lipid fraction E (PLFE) and glyceryl caldityl tetraether (GCTE), which are the main components of PLFE with the sugar and phosphate removed.

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“…Because of their non-bilayer-forming property, neutral lipids pose a unique challenge to experimental characterizations. Studies have indicated that “fluid lamellar phases” exist for squalane in the archaea-mimicking membrane . Triacylglycerol blisters in the bilayer have long been proposed on the basis of 1 H NMR measurements and optical microscopy and thin-layer chromatography results .…”

Section: Introductionmentioning

confidence: 99%

Molecular Condensate in a Membrane: A Tugging Game between Hydrophobicity and Polarity with Its Biological Significance

et al. 2022

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Lipid self-organization and lipid−water interfaces have been an increasingly important topic positioned at the crossroads of physical chemistry and biology. Some neutral lipids can partition into the biomembrane and play an important biological role. In this study, we have used all-atom molecular dynamics simulations to dissect the partition, aggregation, flip-flop, and modulation of neutral lipids including (i) menaquinone/menaquinol, (ii) ubiquinone/ubiquinol, and (iii) triacylglycerol. The partitioning of these molecules is driven by the balancing force between headgroup hydrophilicity and acyl chain hydrophobicity as well as the lipid shapes. We then discuss the emerging questions in this area, share our own perspectives, and mention the development of the CHARMM-GUI membrane modeling platform, which enables further computational investigations into those questions.

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Apolar Polyisoprenoids Located in the Midplane of the Bilayer Regulate the Response of an Archaeal-Like Membrane to High Temperature and Pressure

Cited by 7 publications

References 63 publications

Location and Conformational Ensemble of Menaquinone and Menaquinol, and Protein–Lipid Modulations in Archaeal Membranes

Location and Conformational Ensemble of Menaquinone and Menaquinol, and Protein–Lipid Modulations in Archaeal Membranes

Vesicular and Planar Membranes of Archaea Lipids: Unusual Physical Properties and Biomedical Applications

Molecular Condensate in a Membrane: A Tugging Game between Hydrophobicity and Polarity with Its Biological Significance

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