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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.

Glycerol monoalkyl glycerol tetraethers (GMGTs) are a group of membrane spanning lipids produced by some species of archaea and bacteria. They differ from the more commonly studied glycerol dialkyl glycerol tetraethers (GDGTs) in having an additional covalent carbon-carbon bond connecting the two alkyl chain. The relative abundance and distribution of bacterial branched GMGTs (brGMGTs) in surface sediments from a set of East African lakes were studied. The abundance of brGMGTs relative to the brGDGTs is positively correlated to measured mean annual air temperature (MAAT), although with a significant amount of scatter. BrGMGT abundance was not correlated to lake water pH. Seven major brGMGTs that vary in degree of methylation were identified, with m/z 1020, 1034 and 1048. Further, the mass chromatograms of the m/z 1020 and 1034 brGMGTs show an interesting distribution of peaks, which likely relates to the occurrence of distinct brGMGT isomers. This structural complexity is higher than previously observed in peats and marine sediments. Principal component analysis of the fractional abundance of bacterial tetraether lipids revealed the brGMGTs behave similarly to one another but differently from both the 5- or 6-methyl brGDGTs. This suggests the brGMGTs are produced by a common source organism and are methylated at a different position. The distribution of the seven brGMGTs showed considerable correlation with MAAT. This variability was captured in a new proxy index (the brGMGTI), which showed a strong positive linear relationship with MAAT. Lacustrine brGMGTs show potential to be applied to ancient settings to provide information about paleoclimate. © 2019 The Authors

The impact of hydrothermal activity on wider ocean geochemistry and microbial ecology remains a topic of much interest. To explore whether hydrothermal microbial signatures are exported to surrounding marine sediments or if such organisms serve as an important source of sedimentary organic matter, we determined the distributions of glycerol dialkyl glycerol tetraether (GDGT) membrane lipids in surficial normal marine sediments, metalliferous sediments and low-temperature hydrothermal deposits at newly discovered hydrothermal fields and adjacent areas at the Southwest Indian Ridge (SWIR). The GDGTs in those samples varied significantly, evidently representing a variable influence of the hydrothermal activity. GDGT compositions of surficial background sediments in SWIR were similar to those commonly observed in marine sediments, dominated by GDGTs associated with marine planktonic archaea and especially GDGT−0 and crenarchaeol. In contrast, the GDGTs of metalliferous sediments strongly impacted by hydrothermal activity and low-temperature hydrothermal deposits were markedly different, characterized by high relative abundances of isoprenoid GDGTs (iGDGTs) bearing multiple rings (yielding a higher ring index), low relative abundances of crenarchaeol, and the presence of glycerol monoalkyl glycerol tetraether lipids (GMGTs; so called ‘H-tetraethers’) that were absent in the normal marine sediments. Sources for these hydrothermal-specific tetraether lipids likely include methanogens and anaerobic methanotrophic archaea (GDGT−0 and GDGT−1–3, respectively), Thermoprotei and Thermoplasmatales (elevated GDGT−3 and 4), and other thermophilic archaea including Methanobacteriales (GMGTs). Deposits influenced by low-temperature hydrothermal activity also contained higher abundances of branched GDGTs (brGDGTs) typically attributed to soil bacteria. The more distal metalliferous sediments influenced by the neutrally buoyant plume did not contain putative hydrothermal GDGTs, having the same GDGT distribution as the background sediments. This suggests that the neutrally buoyant plume has a limited potential to directly influence the organic matter inputs to surrounding sediments, due to a rapidly waning chemosynthetic microbial contribution relative to normal marine contributions as the plume dispersed and was diluted.

Elucidating the lipidome of Archaea is essential to understand their tolerance to extreme environmental conditions. Previous characterizations of the lipid composition of Pyrococcus species, a model genus of hyperthermophilic archaea belonging to the Thermococcales order, led to conflicting results, which hindered the comprehension of their membrane structure and the putative adaptive role of their lipids. In an effort to clarify the lipid composition data of the Pyrococcus genus, we thoroughly investigated the distribution of both the core lipids (CL) and intact polar lipids (IPL) of the model Pyrococcus furiosus and, for the first time, of Pyrococcus yayanosii, the sole obligate piezophilic hyperthermophilic archaeon known to date. We showed a low diversity of IPL in the lipid extract of P. furiosus, which nonetheless allowed the first report of phosphatidyl inositol-based glycerol mono- and trialkyl glycerol tetraethers. With up to 13 different CL structures identified, the acid methanolysis of Pyrococcus furiosus revealed an unprecedented CL diversity and showed strong discrepancies with the IPL compositions reported here and in previous studies. By contrast, P. yayanosii displayed fewer CL structures but a much wider variety of polar heads. Our results showed severe inconsistencies between IPL and CL relative abundances. Such differences highlight the diversity and complexity of the Pyrococcus plasma membrane composition and demonstrate that a large part of its lipids remains uncharacterized. Reassessing the lipid composition of model archaea should lead to a better understanding of the structural diversity of their lipidome and of their physiological and adaptive functions.