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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.

Abstract: We have investigated the distributions and carbon isotopic compositions of archaeal membrane lipids in gas-hydrate-bearing sediments collected from the northern Cascadia Margin offshore from Vancouver Island (Sites U1327 and U1328) by the R/V JOIDES Resolution during IODP Expedition 311. Archaeal lipid biomarkers, including glycerol dialkyl glycerol tetraethers (GDGTs), tend to become abundant below 100mbsf (meters below sea floor). Tricyclic biphytane (BP[3]; which is a robust biomarker derived from GDGT), crenarchaeol, and other BPs exhibit δ13C values of ca. −20‰, and become abundant between 130 and 230mbsf at Site U1328. In this depth range, concentrations of ammonium and phosphate in interstitial waters also increase, suggesting that a larger population and higher activity of heterotrophic community consisting of crenarchaeota and other archaea decompose the sedimentary organic matter, thereby liberating ammonium and phosphate. Such crenarchaeotic activity can produce other metabolic products such as molecular hydrogen by fermentation of organic matter during diagenesis. Furthermore, near the organic matter decomposition zone (130 to 230mbsf), a probable methanogen biomarker (13C-depleted BP[1] with δ13C values as low as −48.8‰) becomes abundant, indicating that methanogens utilize these diagenetic products. The molecular and isotopic distributions of archaeal lipid biomarkers indicate that the archaeal community plays an important role in the biogeochemical cycles of deep-sea sediments, including both methanogenesis and nutrient recycling. [Copyright &y& Elsevier]

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. [ABSTRACT FROM AUTHOR]