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In Search for the Membrane Regulators of Archaea

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In Search for the Membrane Regulators of Archaea International Journal of Molecular Sciences Review In Search for the Membrane Regulators of Archaea Marta Salvador-Castell 1,2 , Maxime Tourte 1,2 and Philippe M. Oger 1,2,* 1 Université de Lyon, CNRS, UMR 5240, F-69621 Villeurbanne, France 2 Université de Lyon, INSA de Lyon, UMR 5240, F-69621 Villeurbanne, France * Correspondence: [email protected] Received: 7 August 2019; Accepted: 6 September 2019; Published: 9 September 2019 Abstract: Membrane regulators such as sterols and hopanoids play a major role in the physiological and physicochemical adaptation of the different plasmic membranes in Eukarya and Bacteria. They are key to the functionalization and the spatialization of the membrane, and therefore indispensable for the cell cycle. No archaeon has been found to be able to synthesize sterols or hopanoids to date. They also lack homologs of the genes responsible for the synthesis of these membrane regulators. Due to their divergent membrane lipid composition, the question whether archaea require membrane regulators, and if so, what is their nature, remains open. In this review, we review evidence for the existence of membrane regulators in Archaea, and propose tentative location and biological functions. It is likely that no membrane regulator is shared by all archaea, but that they may use different polyterpenes, such as carotenoids, polyprenols, quinones and apolar polyisoprenoids, in response to specific stressors or physiological needs. Keywords: archaea; membrane organization; membrane modulators; polyterpenes; carotenoids; polyprenols; quinones; polyisoprenoids; adaptation 1. Introduction In 1972, Singer and Nicolson reconciled the numerous observations about cell membranes to construct the now well-established fluid mosaic model [1]. Since then, the ultrastructure of cell membranes has further evolved to accommodate the lipid phases, i.e., gel or liquid crystalline, lipid phase partition, membrane curvature and the presence of lipid membrane regulators, which are currently gaining much attention in membrane structuration, function and regulation [2–4]. Lipid membrane regulators allow to expand the functional state of the lipid membrane to broader environmental conditions. The best studied membrane regulator is cholesterol, a sterol derivative present in animal cell membranes [3,5–10]. Although Bacteria do not synthesize sterols, their hopanoids have been accepted as “sterol surrogates” [11,12]. Sterols or hopanoids are absent in Archaea, and whether Archaea have membrane regulators remains a hotly debated question. The current review sums up the data available on putative archaeal membrane regulators and poses the groundwork for their identification in Archaea. 2. Structure of Bacterial and Eukaryal Membrane Regulators Sterols are the most well-known lipid membrane regulators. The term sterols covers a variety of compounds synthesized from 2,3-epoxide-squalene and consisting of an aliphatic chain with 7–10 carbons and four flat fused rings, the outermost one exhibiting an sn-3 hydroxyl group [6]. The three major kingdoms of the Eukarya, e.g., mammals, fungi and plants, synthesize different types of sterols, cholesterol, ergosterol and sitosterols and stigmasterols respectively. Hopanoids are pentacyclic triterpenoids synthesized from squalene. Such term regroups C30 derivatives such as diploptene, a hydrophobic molecule, and C35 molecules such as bacteriohopane, and their Int. J. Mol. Sci. 2019, 20, 4434; doi:10.3390/ijms20184434 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2019, 20, 4434 2 of 26 derivatives [13]. In hydrophilic hopanoids, hydroxyl groups are bound to the branched aliphatic chain, whichresults therefore in an “inverted” results in polarity an “inverted” in comparison polarity to in sterols. comparison Sterols to and sterols. hopanoids Sterols belong and hopanoids to a much belonglarger togroup a much of natural larger groupcompounds of natural called compounds polyterpenes, called i.e., polyterpenes, hydrocarbon i.e., oligomers hydrocarbon resulting oligomers from resultingsuccessive from condensations successive condensations of isoprene precursors of isoprene, precursors,namely, isopentenyl namely, isopentenyl pyrophosphate pyrophosphate (IPP) and (IPP)dimethyallyl and dimethyallyl diphosphate diphosphate (DMAP) (DMAP) (Figure (Figure 1). Poly1).terpenes Polyterpenes represent represent one oneof the of thelargest largest class class of ofnaturally naturally occurring occurring compounds compounds and and are are widely widely distributed distributed in Eukaryotes, Bacteria asas wellwell asas Archaea.Archaea. AlthoughAlthough all all polyterpenes polyterpenes of theof threethe three domains domain of lifes of originate life originate from IPP from and DMAP,IPP and these DMAP, precursors these areprecursors synthesized are synthesized via two independent, via two independent, non-homologous non-homologous pathways: thepathways: methylerythritol the methylerythritol 4-phosphate 4- pathwayphosphate in pathway Bacteria andin Bacteria the mevalonate and the mevalonate pathway in Eukaryotespathway in andEukaryotes Archaea and [14 ,Archaea15]. [14,15]. FigureFigure 1. 1.Most Most representative representative polyterpenes polyterpenes and theirand biosynthetictheir biosynthetic link. Carbon link. Carbon nomenclature nomenclature and isoprene and conformationsisoprene conformations are indicated are as indicated mentioned as hereafter.mentioned hereafter. 3. Mechanisms of Membrane Regulation in Eukarya and Bacteria 3. Mechanisms of Membrane Regulation in Eukarya and Bacteria TheThe impact impact of of sterols, sterols, and and particularly particularly of cholesterol, of cholesterol, on lipid on membraneslipid membranes has been has largely been studied. largely Sterolsstudied. are Sterols oriented are perpendicular oriented perpendicular to the membrane to the surfacemembrane with surface the hydroxyl with facingthe hydroxyl the phospholipid facing the esterphospholipid carbonyl ester and carbonyl stabilize and the stabilize functional the phospholipid functional phospholipid liquid-crystalline liquid-crystalline phase, i.e., phase, decrease i.e., gel-to-liquid lipid phase transition temperature (Tm). Sterols modulate membrane parameters decrease gel-to-liquid lipid phase transition temperature (Tm). Sterols modulate membrane byparameters tightening by and tightening reducing and the averagereducing tilt the of phospholipidaverage tilt of acyl phospholipid chains [16], acyl therefore chains decreasing [16], therefore acyl chains’decreasing motion acyl [17 chains’] while motion increasing [17] the while viscosity increasi andng the the order viscosity of lipid and membranes the order [of18 lipid]. They membranes also limit lipid[18]. membraneThey also passivelimit lipid permeability membrane to passive ions and perm smalleability molecules to ions [17]. and Last, small cholesterol molecules is the [17]. essential Last, componentcholesterol ofis thethe thickeressential liquid-ordered component of phase the thicker present liquid-ordered in eukaryotic cell phase membranes, present previouslyin eukaryotic called cell “lipidmembranes, raft”, which previously is essential called for “lipid membrane raft”, which functional is essential differentiation. for membrane This functional cholesterol-induced differentiation. lipid phaseThis leadscholesterol-induced to a discontinuity lipid of thephase membrane leads boundaryto a discontinuity and, therefore, of the to amembrane line-tension boundary between bothand, phasestherefore, [19 ].to This a line-tension tension may between facilitate both cell membranephases [19]. bending This tension and, consequently, may facilitate cell cell processes membrane as fusionbending and and, fission, consequently, which are essentialcell processes for numerous as fusion physiological and fission, mechanisms which are essential including for cell numerous division, cellphysiological compartmentalization mechanisms or including vesicle formation. cell division, cell compartmentalization or vesicle formation. The hydrophobic hopanoid, diploptene, is placed in the midplane of the lipid bilayer with an average tilt angle of about 51° to the membrane plane, whereas bacteriohopanetetrol presents an Int. J. Mol. Sci. 2019, 20, x; doi: FOR PEER REVIEW www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2019, 20, 4434 3 of 26 The hydrophobic hopanoid, diploptene, is placed in the midplane of the lipid bilayer with an average tilt angle of about 51◦ to the membrane plane, whereas bacteriohopanetetrol presents an orientation similar to that of cholesterol with an average tilt angle of 14◦ [20]. Hopanoids, although with different efficiencies, can induce order and decrease fluidity and permeability of model membranes, even though they do not show a significant effect on bilayer elasticity [12,13,20,21]. Similarly to cholesterol, hopanoids can induce the formation of more ordered phases at physiological concentrations [20]. Whether they are involved in membrane domain formation in Bacteria remains to be demonstrated. 4. Candidate Surrogates for Sterol and Hopanoid Membrane Regulators in Archaea As Archaea apparently lack both sterols and hopanoids and considering the physiological importance of membrane regulators in bacterial and eukaryal membranes, we can suppose the existence of membranes regulators in Archaea as well. However, one has to keep in mind that archaeal and bacterial/eukaryal lipids strongly differ in their structure. The former ones being based on ether-linked isoprenoid chains,
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