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Membrane homeoviscous adaptation in the piezo-hyperthermophilic archaeon Thermococcus barophilus.

Cario A, Grossi V, Schaeffer P, Oger PM - Front Microbiol (2015)

Bottom Line: Reversely, a higher proportion of GDGT-0 is observed under low pressure and high temperature conditions.Whether these apolar lipids insert in the membrane or not remains to be addressed.However, our results raise questions about the structure of the membrane in this archaeon and other Archaea harboring a mixture of di- and tetraether lipids.

View Article: PubMed Central - PubMed

Affiliation: CNRS, Laboratoire de Géologie de Lyon, Ecole Normale Supérieure de Lyon, UMR 5276, Université Claude Bernard Lyon 1 Lyon, France.

ABSTRACT
The archaeon Thermococcus barophilus, one of the most extreme members of hyperthermophilic piezophiles known thus far, is able to grow at temperatures up to 103°C and pressures up to 80 MPa. We analyzed the membrane lipids of T. barophilus by high performance liquid chromatography-mass spectrometry as a function of pressure and temperature. In contrast to previous reports, we show that under optimal growth conditions (40 MPa, 85°C) the membrane spanning tetraether lipid GDGT-0 (sometimes called caldarchaeol) is a major membrane lipid of T. barophilus together with archaeol. Increasing pressure and decreasing temperature lead to an increase of the proportion of archaeol. Reversely, a higher proportion of GDGT-0 is observed under low pressure and high temperature conditions. Noticeably, pressure and temperature fluctuations also impact the level of unsaturation of apolar lipids having an irregular polyisoprenoid carbon skeleton (unsaturated lycopane derivatives), suggesting a structural role for these neutral lipids in the membrane of T. barophilus. Whether these apolar lipids insert in the membrane or not remains to be addressed. However, our results raise questions about the structure of the membrane in this archaeon and other Archaea harboring a mixture of di- and tetraether lipids.

No MeSH data available.


Related in: MedlinePlus

Example of high performance liquid chromatography–mass spectrometry (HPLC–MS) chromatograms of the lipid extract of acid-hydrolyzed cells of T. barophilus. Cells were grown at optimal pressure and temperature (OPT, 40 MPa, 85°C), low temperature (LT, 40 MPa, 75°C), high pressure (HP, 70 MPa, 85°C), low pressure (LP, 0.1 MPa, 85°C), or high temperature (HT, 40 MPa, 90°C). (1) Diphytanyl glycerol diether (archaeol); (2) glycerol trialkyl glycerol tetraether (GTGT); (3) glycerol dibiphytanyl glycerol tetraether (GDGT-0).
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Figure 2: Example of high performance liquid chromatography–mass spectrometry (HPLC–MS) chromatograms of the lipid extract of acid-hydrolyzed cells of T. barophilus. Cells were grown at optimal pressure and temperature (OPT, 40 MPa, 85°C), low temperature (LT, 40 MPa, 75°C), high pressure (HP, 70 MPa, 85°C), low pressure (LP, 0.1 MPa, 85°C), or high temperature (HT, 40 MPa, 90°C). (1) Diphytanyl glycerol diether (archaeol); (2) glycerol trialkyl glycerol tetraether (GTGT); (3) glycerol dibiphytanyl glycerol tetraether (GDGT-0).

Mentions: Acid-hydrolyzed core lipids of T. barophilus grown under optimal growth conditions (OPT) were analyzed by HPLC–APCI–MS. The major core lipids identified were GDGT-0 ([M+H]+ 1302.5; compound 3, Figure 2) and archaeol ([M+H]+ 653.5; compound 1, Figure 2). A third core lipid present in trace amounts showed a protonated [M+H]+ ion at m/z 1304.5 and was identified as a glycerol-trialkyl-glycerol-tetraether (GTGT; compound 2, Figure 2). The latter compound, which contains one biphytanyl and two phytanyl chains, has been formerly proposed to be an intermediate of GDGT-0 biosynthesis (Schouten et al., 2000; Pitcher et al., 2011), although this has been recently subject to debate (Villanueva et al., 2014). H-shaped GDGT-0 derivatives previously reported in several members of the Thermococcales (Sugai et al., 2004), GDGT with 1–4 cyclopentane ring(s) observed in some thermoacidophilic Archaea and sulfur-dependent thermophiles (De Rosa et al., 1980b), and macrocyclic archaeol reported in two species of Methanococcus (Comita et al., 1984; Trincone et al., 1992), were not detected in T. barophilus strain MP. It is noteworthy that the response factors in MS of archaeol and GDGT-0 are not known but that they likely differ due to the higher number of protonable sites present in GDGT-0 compared to archaeol. Thus, the variations of the archaeol/GDGT-0 (D/T) ratio observed between growth conditions (Figure 2) indicate qualitative rather than quantitative changes between both classes of core lipids. Nonetheless, considering exclusively the two predominant compounds (i.e., archaeol and GDGT-0) present in the HPLC chromatogram, the area of the peak corresponding to GDGT-0 represented 84% of the ether lipids vs. 16% for archaeol.


Membrane homeoviscous adaptation in the piezo-hyperthermophilic archaeon Thermococcus barophilus.

Cario A, Grossi V, Schaeffer P, Oger PM - Front Microbiol (2015)

Example of high performance liquid chromatography–mass spectrometry (HPLC–MS) chromatograms of the lipid extract of acid-hydrolyzed cells of T. barophilus. Cells were grown at optimal pressure and temperature (OPT, 40 MPa, 85°C), low temperature (LT, 40 MPa, 75°C), high pressure (HP, 70 MPa, 85°C), low pressure (LP, 0.1 MPa, 85°C), or high temperature (HT, 40 MPa, 90°C). (1) Diphytanyl glycerol diether (archaeol); (2) glycerol trialkyl glycerol tetraether (GTGT); (3) glycerol dibiphytanyl glycerol tetraether (GDGT-0).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4612709&req=5

Figure 2: Example of high performance liquid chromatography–mass spectrometry (HPLC–MS) chromatograms of the lipid extract of acid-hydrolyzed cells of T. barophilus. Cells were grown at optimal pressure and temperature (OPT, 40 MPa, 85°C), low temperature (LT, 40 MPa, 75°C), high pressure (HP, 70 MPa, 85°C), low pressure (LP, 0.1 MPa, 85°C), or high temperature (HT, 40 MPa, 90°C). (1) Diphytanyl glycerol diether (archaeol); (2) glycerol trialkyl glycerol tetraether (GTGT); (3) glycerol dibiphytanyl glycerol tetraether (GDGT-0).
Mentions: Acid-hydrolyzed core lipids of T. barophilus grown under optimal growth conditions (OPT) were analyzed by HPLC–APCI–MS. The major core lipids identified were GDGT-0 ([M+H]+ 1302.5; compound 3, Figure 2) and archaeol ([M+H]+ 653.5; compound 1, Figure 2). A third core lipid present in trace amounts showed a protonated [M+H]+ ion at m/z 1304.5 and was identified as a glycerol-trialkyl-glycerol-tetraether (GTGT; compound 2, Figure 2). The latter compound, which contains one biphytanyl and two phytanyl chains, has been formerly proposed to be an intermediate of GDGT-0 biosynthesis (Schouten et al., 2000; Pitcher et al., 2011), although this has been recently subject to debate (Villanueva et al., 2014). H-shaped GDGT-0 derivatives previously reported in several members of the Thermococcales (Sugai et al., 2004), GDGT with 1–4 cyclopentane ring(s) observed in some thermoacidophilic Archaea and sulfur-dependent thermophiles (De Rosa et al., 1980b), and macrocyclic archaeol reported in two species of Methanococcus (Comita et al., 1984; Trincone et al., 1992), were not detected in T. barophilus strain MP. It is noteworthy that the response factors in MS of archaeol and GDGT-0 are not known but that they likely differ due to the higher number of protonable sites present in GDGT-0 compared to archaeol. Thus, the variations of the archaeol/GDGT-0 (D/T) ratio observed between growth conditions (Figure 2) indicate qualitative rather than quantitative changes between both classes of core lipids. Nonetheless, considering exclusively the two predominant compounds (i.e., archaeol and GDGT-0) present in the HPLC chromatogram, the area of the peak corresponding to GDGT-0 represented 84% of the ether lipids vs. 16% for archaeol.

Bottom Line: Reversely, a higher proportion of GDGT-0 is observed under low pressure and high temperature conditions.Whether these apolar lipids insert in the membrane or not remains to be addressed.However, our results raise questions about the structure of the membrane in this archaeon and other Archaea harboring a mixture of di- and tetraether lipids.

View Article: PubMed Central - PubMed

Affiliation: CNRS, Laboratoire de Géologie de Lyon, Ecole Normale Supérieure de Lyon, UMR 5276, Université Claude Bernard Lyon 1 Lyon, France.

ABSTRACT
The archaeon Thermococcus barophilus, one of the most extreme members of hyperthermophilic piezophiles known thus far, is able to grow at temperatures up to 103°C and pressures up to 80 MPa. We analyzed the membrane lipids of T. barophilus by high performance liquid chromatography-mass spectrometry as a function of pressure and temperature. In contrast to previous reports, we show that under optimal growth conditions (40 MPa, 85°C) the membrane spanning tetraether lipid GDGT-0 (sometimes called caldarchaeol) is a major membrane lipid of T. barophilus together with archaeol. Increasing pressure and decreasing temperature lead to an increase of the proportion of archaeol. Reversely, a higher proportion of GDGT-0 is observed under low pressure and high temperature conditions. Noticeably, pressure and temperature fluctuations also impact the level of unsaturation of apolar lipids having an irregular polyisoprenoid carbon skeleton (unsaturated lycopane derivatives), suggesting a structural role for these neutral lipids in the membrane of T. barophilus. Whether these apolar lipids insert in the membrane or not remains to be addressed. However, our results raise questions about the structure of the membrane in this archaeon and other Archaea harboring a mixture of di- and tetraether lipids.

No MeSH data available.


Related in: MedlinePlus