1. Membrane adaptation in the hyperthermophilic archaeon Pyrococcus furiosus relies upon a novel strategy involving glycerol monoalkyl glycerol tetraether lipids
- Author
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Maxime Tourte, Vincent Grossi, Philippe Schaeffer, Philippe Oger, Microbiologie, adaptation et pathogénie (MAP), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS), Institut de Chimie de Strasbourg, Université de Strasbourg (UNISTRA)-Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS), Laboratoire de Géologie de Lyon - Terre, Planètes, Environnement (LGL-TPE), École normale supérieure de Lyon (ENS de Lyon)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut national des sciences de l'Univers (INSU - CNRS)-Université Jean Monnet - Saint-Étienne (UJM)-Centre National de la Recherche Scientifique (CNRS), ANR-17-CE11-0012,ArchaeoMembranes,Des bicouches lipidiques stables au delà du point d'ébullition de l'eau(2017), Microbiology of Extreme Environments (M2E), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Strasbourg (UNISTRA)-Centre National de la Recherche Scientifique (CNRS)-Institut de Chimie du CNRS (INC), Laboratoire de Géologie de Lyon - Terre, Planètes, Environnement [Lyon] (LGL-TPE), Centre National de la Recherche Scientifique (CNRS)-Institut national des sciences de l'Univers (INSU - CNRS)-Université Claude Bernard Lyon 1 (UCBL), and Université de Lyon-Université de Lyon-École normale supérieure - Lyon (ENS Lyon)
- Subjects
Glycerol ,Pyrococcus ,H-shaped lipids ,[SDV]Life Sciences [q-bio] ,chemistry.chemical_element ,Microbiology ,03 medical and health sciences ,chemistry.chemical_compound ,Membrane Lipids ,[CHIM.ANAL]Chemical Sciences/Analytical chemistry ,tetraethers ,Carbon source ,Ecology, Evolution, Behavior and Systematics ,extremophiles ,030304 developmental biology ,0303 health sciences ,Archaeal membrane lipids ,biology ,030306 microbiology ,[SDV.BBM.BM]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Molecular biology ,stress response ,biology.organism_classification ,Sulfur ,Archaea ,Carbon ,Salinity ,Pyrococcus furiosus ,Membrane ,[SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology ,chemistry ,Biochemistry ,Adaptation - Abstract
Microbes preserve membrane functionality under fluctuating environmental conditions by modulating their membrane lipid composition. Although several studies have documented membrane adaptations in Archaea, the influence of most biotic and abiotic factors on archaeal lipid compositions remains underexplored. Here, we studied the influence of temperature, pH, salinity, the presence/absence of elemental sulfur, the carbon source, and the genetic background on the core lipid composition of the hyperthermophilic neutrophilic marine archaeon Pyrococcus furiosus. Every growth parameter tested affected the core lipid composition to some extent, the carbon source and the genetic background having the greatest influence. Surprisingly, P. furiosus appeared to only marginally rely on the two major responses implemented by Archaea, i.e., the regulation of the ratio of diether to tetraether lipids and that of the number of cyclopentane rings in tetraethers. Instead, this species increased the ratio of glycerol monoalkyl glycerol tetraethers (GMGT, aka. H-shaped tetraethers) to glycerol dialkyl glycerol tetrathers (GDGT) in response to decreasing temperature and pH and increasing salinity, thus providing for the first time evidence of adaptive functions for GMGT. Besides P. furiosus, numerous other species synthesize significant proportions of GMGT, which suggests that this unprecedented adaptive strategy might be common in Archaea.Significance statementWe describe here the membrane adaptive strategies the hyperthermophilic, neutrophilic, and marine model archaeon Pyrococcus furiosus implements in response to one of the largest sets of environmental stressors tested to date, including temperature, pH, salinity, presence/absence of elemental sulfur, carbon source, and genetic background. In contrast to the other archaea investigated so far, which response mainly involves the modulation of their diether/tetraether ratio and/or of their average number of cyclopentane rings, P. furiosus regulates its monoalkyl (so called H-shaped) to dialkyl tetraether ratio. Our study thus provides for the first time evidence of adaptive functions of archaeal monoalkyl tetraethers towards low temperature and pH and high salinity.
- Published
- 2022
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