Membrane adaptation in the hyperthermophilic archaeon Pyrococcus furiosus relies upon a novel strategy involving glycerol monoalkyl glycerol tetraether lipids

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 lipid core composition of the hyperthermophilic neutrophilic marine archaeon Pyrococcus furiosus. Every growth parameter tested affected the lipid core 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 tetraethers 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.

Thermophilic archaeon orchestrates temporal expression of GDGT ring synthases in response to temperature and acidity stress

“…Archaea inhabit a wide range of terrestrial and marine environments and possess diverse membrane lipids. To adapt to environment fluctuations, they modulate their membrane lipid composition with different strategies, such as unsaturation, cyclization, hydroxylation, and methylation of biphytanyl moieties (Bale et al, 2019; Cobban et al, 2020; Elling et al, 2014; Elling et al, 2015; Feyhl‐Buska et al, 2016; Matsuno et al, 2009; Pearson et al, 2008; Qin et al, 2015; Tourte et al, 2022; Zhou et al, 2020). But enzymes involved in these modifications and their regulation mechanisms are largely unexplored.…”

“…Recent studies showed GDGTs are synthesized through the condensation of two molecules of archaeols by tetraether synthase (Tes) proteins (Lloyd et al, 2022; Zeng et al, 2022), and the biochemical assays suggest saturated archaeols (Lloyd et al, 2022), hydrogenated from unsaturated archaeols by the geranylgeranyl reductase (GGR) (Xu et al, 2010), are the precursor of GDGTs. The core biphytanyl chains of GDGT‐0 (acyclic GDGT) can be further modified by cyclization, hydroxylation, methylation and cross linking (Bale et al, 2019; Cobban et al, 2020; Elling et al, 2014; Elling et al, 2015; Feyhl‐Buska et al, 2016; Matsuno et al, 2009; Qin et al, 2015; Tourte et al, 2022; Zhou et al, 2020). Cyclization of GDGTs was shown to be catalysed at C‐7 or C‐3 position of each biphytanyl chain forming a cyclopentane ring, or at C‐11 position forming a cyclohexane ring (Jain et al, 2014; Zeng et al, 2019).…”

Membrane Adaptations and Cellular Responses of Sulfolobus acidocaldarius to the Allylamine Terbinafine

“…Inositol-phosphate dialkyl glycerol diether (IP-DGD) is the most abundant bilayer forming dialkyl glycerol diether lipid (DGD) in the Sulfolobus membrane [ 15 ]. The membrane composition of S. acidocaldarius is modulated by environmental factors, such as growth phase, growth rate, temperature, pH, and starvation [ 11 , 15 , 16 , 17 ]. Common adaptations include altering the ratio of DGDs to GDGTs and incorporating cyclopentane rings into tetraether lipids.…”

Membrane Adaptations and Cellular Responses of Sulfolobus acidocaldarius to the allylamine terbinafine

“…Inositol-phosphate dialkyl glycerol diether (IP-DGD) is the most abundant dialkyl glycerol diether lipid (DGD) [10]. The membrane composition of S. acidocaldarius is modulated by environmental factors such as growth phase, growth rate, temperature, pH and starvation [7] [10] [11] [12]. The common adaptations include altering the ratio of DGDs to GDGTs and the incorporation of cyclopentane rings in tetraether lipids.…”