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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: 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.

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

Stylized schematic representation of lipid organization in putative archaeal membrane models. Homogenous lipid mix of di- and tetraether lipids (A), coexistence of monolayer and bilayer domains (B). As proposed by Lanyi et al. (1974) or Gilmore et al. (2013), lycopane-derivatives in the hydrophobic region of the membrane in parallel to the isoprenoid chains in a homogenous (C) or bilayer domain-containing (D) membrane. In contrast, lycopane-derivatives could be inserted in the hydrophobic midplane of bilayer microdomains in parallel to the surface of the membrane (E), as also suggested by Haines (2001) for squalane in membranes of halophiles.
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Figure 5: Stylized schematic representation of lipid organization in putative archaeal membrane models. Homogenous lipid mix of di- and tetraether lipids (A), coexistence of monolayer and bilayer domains (B). As proposed by Lanyi et al. (1974) or Gilmore et al. (2013), lycopane-derivatives in the hydrophobic region of the membrane in parallel to the isoprenoid chains in a homogenous (C) or bilayer domain-containing (D) membrane. In contrast, lycopane-derivatives could be inserted in the hydrophobic midplane of bilayer microdomains in parallel to the surface of the membrane (E), as also suggested by Haines (2001) for squalane in membranes of halophiles.

Mentions: The cellular function of apolar lipids in Archaea, Eukarya, and Bacteria remains unclear. Cellular lipids can fulfill three general functions. First, they are used to form the matrix of cellular membranes. Second, because of their reduced state, they can serve as efficient storage of caloric reserves and stocks of fatty acid components that are needed for membrane biogenesis. Third, lipids can act as first and second messengers in signal transduction and molecular recognition processes (Fernandis and Wenk, 2007; van Meer et al., 2008). The latter function can be ruled out, since there is no evidence of lipid signaling in Bacteria or Archaea. Furthermore, we show that apolar lipids are accumulated in very low concentrations in T. barophilus cells, ca. 1–2% of total lipids, which does not support a major role for these lipids as energy storage. It is also unlikely that apolar isoprenoid hydrocarbons of T. barophilus could serve as building blocks for archaeal polar lipid biosynthesis or could be derived from polar lipid degradation, since lycopane-type isoprenoid chains are derived from a tail-to-tail condensation of two phytanyl isoprenoid chains, as opposed to the head-to-head condensation of the biphytane isoprenoid chains observed in GDGTs from archaea. The regulation of the level of unsaturation of the lycopane derivatives as a function of pressure and temperature in T. barophilus may support a role of these apolar lipids in homeoviscous adaptation and, thus, their presence in membranes. In addition to this species and Thermococcus litoralis (Lattuati et al., 1998), irregular polyunsaturated isoprenoid lipids have been observed in methanogens, halophiles and alkaliphiles, but have never been detected in thermoacidophiles (Langworthy, 1982). Experiments performed on archaeal lipids in the presence or absence of apolar lipids revealed that the domain structure in monolayered membranes is strongly influenced by the apolar components (Gilmore et al., 2013). These experiments demonstrated that in these archaeal membrane analogs, squalene plays a function similar to that of cholesterol in eukaryotic membranes, helping to orient the lipid tails away from the interface. This allows the lipid tails to pack more closely together, lowering the average area per molecule. The enhanced order leads to the formation of domains in the membrane in the presence of squalene (Gilmore et al., 2013), and to an increased impermeability of the membrane (Lanyi et al., 1974). In the absence of a midplane interface, squalane derivatives could insert within the hydrophobic domain in parallel to the isoprenoid chains. The location of squalene in bilayered membranes remains a subject of debate. Indeed, Haines (2001) and Hauß et al. (2002) have demonstrated that squalane molecules could sit at the midplane of the lipid bilayers, in parallel to the surface of the membrane. By crowding the inner space of the bilayer, the presence of isoprenoid hydrocarbons in the midplane would explain two specific properties of the halophilic membrane: first the decreased proton and water permeability and second the increased membrane rigidity (Haines, 2001). This proposed ultrastructure is yet to be confirmed in membranes of extreme halophiles. In T. barophilus, membrane lipids consist of a majority of tetraether and diether lipids and ca. 1–2% of apolar lipids, which raises questions about the spatial arrangements of these molecules in the membrane. The membrane could be composed of a monolayer matrix constituted by a homogenous mix of tetraether and diether lipids (Figure 5A). Alternatively, the membrane could be constituted of coexisting domains of bilayers and monolayers (Figure 5B). Polyunsaturated lycopane-derivatives could insert similarly to cholesterol in eukaryotic membranes as proposed by Lanyi et al. (1974) and Gilmore et al. (2013; Figures 5C,D). Alternatively, these apolar lipids may insert in the midplane of the bilayer domains formed by diether lipids, parallel to the plane of the membrane as proposed for extreme halophiles by Haines (2001) and Hauß et al. (2002; Figure 5E). The presence of a significant proportion of archaeol in T. barophilus makes the existence of such bilayer membrane domains plausible. Whether models C, D, or E are valid remains to be addressed. As mentioned above, membrane structures based on models C or D would yield increased membrane rigidity and impermeability under high temperature. In contrast, benefits associated with model E would combine the increased membrane fluidity of the archaeol-based membrane and the increased rigidity and reduced permeability brought by the unsaturated lycopane derivatives present in the midplane of the bilayer. Thus, altering the degree of unsaturation of lycopane derivatives and promoting a bilayer-type membrane could strongly modify the melting transition temperatures and lead to more fluid membrane domains under low temperature or high pressure conditions (Smeller, 2002), and represent a possible adaptation strategy in T. barophilus.


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

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

Stylized schematic representation of lipid organization in putative archaeal membrane models. Homogenous lipid mix of di- and tetraether lipids (A), coexistence of monolayer and bilayer domains (B). As proposed by Lanyi et al. (1974) or Gilmore et al. (2013), lycopane-derivatives in the hydrophobic region of the membrane in parallel to the isoprenoid chains in a homogenous (C) or bilayer domain-containing (D) membrane. In contrast, lycopane-derivatives could be inserted in the hydrophobic midplane of bilayer microdomains in parallel to the surface of the membrane (E), as also suggested by Haines (2001) for squalane in membranes of halophiles.
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Related In: Results  -  Collection

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Figure 5: Stylized schematic representation of lipid organization in putative archaeal membrane models. Homogenous lipid mix of di- and tetraether lipids (A), coexistence of monolayer and bilayer domains (B). As proposed by Lanyi et al. (1974) or Gilmore et al. (2013), lycopane-derivatives in the hydrophobic region of the membrane in parallel to the isoprenoid chains in a homogenous (C) or bilayer domain-containing (D) membrane. In contrast, lycopane-derivatives could be inserted in the hydrophobic midplane of bilayer microdomains in parallel to the surface of the membrane (E), as also suggested by Haines (2001) for squalane in membranes of halophiles.
Mentions: The cellular function of apolar lipids in Archaea, Eukarya, and Bacteria remains unclear. Cellular lipids can fulfill three general functions. First, they are used to form the matrix of cellular membranes. Second, because of their reduced state, they can serve as efficient storage of caloric reserves and stocks of fatty acid components that are needed for membrane biogenesis. Third, lipids can act as first and second messengers in signal transduction and molecular recognition processes (Fernandis and Wenk, 2007; van Meer et al., 2008). The latter function can be ruled out, since there is no evidence of lipid signaling in Bacteria or Archaea. Furthermore, we show that apolar lipids are accumulated in very low concentrations in T. barophilus cells, ca. 1–2% of total lipids, which does not support a major role for these lipids as energy storage. It is also unlikely that apolar isoprenoid hydrocarbons of T. barophilus could serve as building blocks for archaeal polar lipid biosynthesis or could be derived from polar lipid degradation, since lycopane-type isoprenoid chains are derived from a tail-to-tail condensation of two phytanyl isoprenoid chains, as opposed to the head-to-head condensation of the biphytane isoprenoid chains observed in GDGTs from archaea. The regulation of the level of unsaturation of the lycopane derivatives as a function of pressure and temperature in T. barophilus may support a role of these apolar lipids in homeoviscous adaptation and, thus, their presence in membranes. In addition to this species and Thermococcus litoralis (Lattuati et al., 1998), irregular polyunsaturated isoprenoid lipids have been observed in methanogens, halophiles and alkaliphiles, but have never been detected in thermoacidophiles (Langworthy, 1982). Experiments performed on archaeal lipids in the presence or absence of apolar lipids revealed that the domain structure in monolayered membranes is strongly influenced by the apolar components (Gilmore et al., 2013). These experiments demonstrated that in these archaeal membrane analogs, squalene plays a function similar to that of cholesterol in eukaryotic membranes, helping to orient the lipid tails away from the interface. This allows the lipid tails to pack more closely together, lowering the average area per molecule. The enhanced order leads to the formation of domains in the membrane in the presence of squalene (Gilmore et al., 2013), and to an increased impermeability of the membrane (Lanyi et al., 1974). In the absence of a midplane interface, squalane derivatives could insert within the hydrophobic domain in parallel to the isoprenoid chains. The location of squalene in bilayered membranes remains a subject of debate. Indeed, Haines (2001) and Hauß et al. (2002) have demonstrated that squalane molecules could sit at the midplane of the lipid bilayers, in parallel to the surface of the membrane. By crowding the inner space of the bilayer, the presence of isoprenoid hydrocarbons in the midplane would explain two specific properties of the halophilic membrane: first the decreased proton and water permeability and second the increased membrane rigidity (Haines, 2001). This proposed ultrastructure is yet to be confirmed in membranes of extreme halophiles. In T. barophilus, membrane lipids consist of a majority of tetraether and diether lipids and ca. 1–2% of apolar lipids, which raises questions about the spatial arrangements of these molecules in the membrane. The membrane could be composed of a monolayer matrix constituted by a homogenous mix of tetraether and diether lipids (Figure 5A). Alternatively, the membrane could be constituted of coexisting domains of bilayers and monolayers (Figure 5B). Polyunsaturated lycopane-derivatives could insert similarly to cholesterol in eukaryotic membranes as proposed by Lanyi et al. (1974) and Gilmore et al. (2013; Figures 5C,D). Alternatively, these apolar lipids may insert in the midplane of the bilayer domains formed by diether lipids, parallel to the plane of the membrane as proposed for extreme halophiles by Haines (2001) and Hauß et al. (2002; Figure 5E). The presence of a significant proportion of archaeol in T. barophilus makes the existence of such bilayer membrane domains plausible. Whether models C, D, or E are valid remains to be addressed. As mentioned above, membrane structures based on models C or D would yield increased membrane rigidity and impermeability under high temperature. In contrast, benefits associated with model E would combine the increased membrane fluidity of the archaeol-based membrane and the increased rigidity and reduced permeability brought by the unsaturated lycopane derivatives present in the midplane of the bilayer. Thus, altering the degree of unsaturation of lycopane derivatives and promoting a bilayer-type membrane could strongly modify the melting transition temperatures and lead to more fluid membrane domains under low temperature or high pressure conditions (Smeller, 2002), and represent a possible adaptation strategy in T. barophilus.

Bottom Line: 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.

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