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Functionalized Membrane Domains: an Ancestral Feature of Archaea? Maxime Tourte, Philippe Schaeffer, Vincent Grossi, Phil Oger

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Functionalized Membrane Domains: an Ancestral Feature of Archaea? Maxime Tourte, Philippe Schaeffer, Vincent Grossi, Phil Oger Functionalized Membrane Domains: An Ancestral Feature of Archaea? Maxime Tourte, Philippe Schaeffer, Vincent Grossi, Phil Oger To cite this version: Maxime Tourte, Philippe Schaeffer, Vincent Grossi, Phil Oger. Functionalized Membrane Domains: An Ancestral Feature of Archaea?. Frontiers in Microbiology, Frontiers Media, 2020, 11, pp.526. 10.3389/fmicb.2020.00526. hal-02553764 HAL Id: hal-02553764 https://hal.archives-ouvertes.fr/hal-02553764 Submitted on 20 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. fmicb-11-00526 March 30, 2020 Time: 21:44 # 1 ORIGINAL RESEARCH published: 31 March 2020 doi: 10.3389/fmicb.2020.00526 Functionalized Membrane Domains: An Ancestral Feature of Archaea? Maxime Tourte1†, Philippe Schaeffer2†, Vincent Grossi3† and Phil M. Oger1*† 1 Université de Lyon, INSA Lyon, CNRS, MAP UMR 5240, Villeurbanne, France, 2 Université de Strasbourg-CNRS, UMR 7177, Laboratoire de Biogéochimie Moléculaire, Strasbourg, France, 3 Université de Lyon, ENS Lyon, CNRS, Laboratoire de Géologie de Lyon, UMR 5276, Villeurbanne, France 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 Edited by: Mark Alexander Lever, archaeon Thermococcus barophilus. With very different physico-chemical parameters ETH Zürich, Switzerland of the mono- and bilayer, each domain type would thus allow the docking of different Reviewed by: membrane proteins and express different biological functions in the membrane. To Laura Villanueva, estimate the ubiquity of this putative membrane ultrastructure in and out of the order Royal Netherlands Institute for Sea Research (NIOZ), Netherlands Thermococcales, we re-analyzed the core lipid composition of all the Thermococcales Marcus Elvert, type species and collected all the literature data available for isolated archaea. We University of Bremen, Germany show that all species of Thermococcales synthesize a mixture of diether bilayer *Correspondence: Phil M. Oger forming and tetraether monolayer forming lipids, in various ratio from 10 to 80% [email protected] diether in Pyrococcus horikoshii and Thermococcus gorgonarius, respectively. Since †ORCID: the domain formation prediction rests only on the coexistence of di- and tetraether Maxime Tourte lipids, we show that all Thermococcales have the ability for domain formation, i.e., orcid.org/0000-0001-5089-7416 Philippe Schaeffer differential functionalization of their membrane. Extrapolating this view to the whole orcid.org/0000-0003-0618-0834 Archaea domain, we show that almost all archaea also have the ability to synthesize Vincent Grossi orcid.org/0000-0001-6263-3813 di- and tetraether lipids, which supports the view that functionalized membrane Phil M. Oger domains may be shared between all Archaea. Hence domain formation and membrane orcid.org/0000-0001-6298-6870 compartmentalization may have predated the separation of the three domains of life and Specialty section: be essential for the cell cycle. This article was submitted to Keywords: Archaea, Thermococcales, membrane domains, archaeal lipids, membrane architecture, membrane Extreme Microbiology, function, evolution, adaptation a section of the journal Frontiers in Microbiology Received: 04 November 2019 INTRODUCTION Accepted: 11 March 2020 Published: 31 March 2020 Archaea are the main inhabitants of the harshest environments, regardless of whether the extreme Citation: conditions are temperature, salinity, hydrostatic pressure, pH, or scarce nutrients. This tolerance Tourte M, Schaeffer P, Grossi V to extreme physical and chemical conditions has been associated with three specific characteristics and Oger PM (2020) Functionalized Membrane Domains: An Ancestral of their membrane lipids, which greatly differ from their eukaryotic and bacterial counterparts (De Feature of Archaea? Rosa et al., 1986a; Albers and Meyer, 2011): (1) archaeal ether bonds that are more chemically Front. Microbiol. 11:526. resistant than bacterial/eukaryal ester bonds, allow a tighter compaction of the lipids (Baba et al., doi: 10.3389/fmicb.2020.00526 1999); (2) archaeal isoprenoid hydrocarbon chains that enhance membrane packing relative to Frontiers in Microbiology| www.frontiersin.org 1 March 2020| Volume 11| Article 526 fmicb-11-00526 March 30, 2020 Time: 21:44 # 2 Tourte et al. Membrane Domains in Archaea linear acyl chains of bacterial/eukaryal lipids, create cell behavior, e.g., monolayer and bilayer domains, could allow the membranes with enhanced stability and impermeability anchoring of different proteins and confer these domains peculiar (Komatsu and Chong, 1998); and (3) archaeal tetraether physiological and adaptive functions. lipids can form monolayer membranes that are more rigid The formation of membrane domains in archaeal lipids has and impermeable than bacterial/eukaryal bilayer membranes been directly observed in artificial mixtures of either tetraether classically made of diacylglycerols (Chong, 2010). The presence (Bagatolli et al., 2000) or diether lipids (Salvador-Castell et al., of bipolar tetraether lipids is supportive of hyperthermophilic 2020), and has been suggested to occur in natural mixtures (de Rosa et al., 1977) and acidophilic growth (Macalady et al., of both diether and tetraether lipids to explain the extreme 2004) in Archaea. This view was further supported by the tolerance of the membrane of T. barophilus (Cario et al., observation that the most extremophilic bacterium, Thermotoga 2015). In the evolution of Archaea and archaeal membranes, we ◦ maritima (Tmax = 90 C), also produces tetraether membrane- hypothesize that this particular adaptive route might have played spanning lipids (Sinninghe Damsté et al., 2007). All works to a major role. To test this hypothesis, we looked at the ability of date demonstrate a strong correlation between the proportion Archaea to harbor a differentially functionalized membrane, by of tetraether lipids and the adaptation to extreme acidity in focalizing on the diether/tetraether domain formation, which is thermoacidophiles (Boyd et al., 2013), and between the absence the easiest to assess at the phylum level since it can be inferred of tetraether lipids and the adaptation to extreme salinity or from the sole analysis of membrane core lipid compositions. the adaptation to high pH (Kates, 1993). In contrast, no strong However, one bottleneck of this approach is the heterogeneous correlation have been highlighted for other extremes, nor for quality of the lipid data available in the literature. For instance, mesophilic conditions, which raises questions as to how archaea the reassessment of membrane lipid compositions using more thriving in such habitats adapt to their specific lifestyles. This adequate analytical approaches (Nishihara and Koga, 1991; suggests that some environmental stress factors are not strong Sugai et al., 2004; Cario et al., 2015) have highlighted strong enough to drive measurable compositional shifts in membrane discrepancies with those originally reported (De Rosa et al., lipids or may involve adaptive routes not requiring an alteration 1986b, 1987; Marteinsson et al., 1999). To obtain a complete set of the diether/tetraether ratio, or that unknown alternative of comparable membrane lipid compositions and constrain the adaptive routes exist in Archaea. level of trust we could have in published lipid compositions of Hence, the existence of neutrophilic hyperthermophiles, such Archaea, we reassessed the lipid compositions of the whole order as Methanopyrus kandleri, which is incapable of synthesizing Thermococcales, to which T. barophilus belongs. tetraethers but grows optimally at 110◦C(Hafenbradl et al., 1996), We show here that most of the Thermococcales lipid questions the need for these tetraether lipids for growth at high compositions are significantly different from previously temperatures. Furthermore, a large number of hyperthermophilic published work. In some instances, it confirmed the synthesis archaea produce a mixture of tetra- and diether lipids while of previously undetected tetraether lipids, showing that all growing at temperatures near or above 100◦C(Trincone et al., Thermococcales are able to synthesize both di- and tetraethers. 1992). In these organisms, diether lipids often represent a These findings show that the membrane organization proposed large part of the membrane lipids, which implies that the for T. barophilus could be extended to the whole Thermococcales membrane may contain domains of monolayer and domains order and suggest that the ability to synthesize diethers and/or of bilayer. Increasing temperature increases molecular motion tetraethers could be inferred from taxonomically related species. in lipids. Hence, at high temperature, bilayers become more We can thus propose the coexistence of monolayer and bilayer fluid, which
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