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Biochimica et Biophysica Acta 1788 (2009) 2101–2106
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Biochimica et Biophysica Acta
j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / b b a m e m
The cardiolipin analogues of Archaea
Angela Corcelli
Dipartimento di Biochimica Medica, Biologia Medica e Fisica Medica, Università degli Studi di Bari, Piazza G. Cesare, 70124 Bari, Italy
a r t i c l e
i n f o
Article history:
Received 2 October 2008
Accepted 14 May 2009
Available online 20 May 2009
Keywords:
Archaea
Diphytanylglycerol diether lipids
Extreme halophiles
Dimeric phospholipids and phosphoglycolipids
Osmotic stress
a b s t r a c t
The present article reviews studies of the structure and functional roles of the cardiolipin analogues of
extremely halophilic prokaryotes belonging to the Archaea domain. Analogies and differences between the
archaeal bisphosphatidylglycerol and the mitochondrial cardiolipin are presented. Furthermore the structure
of archaeal glycophospholipid dimers is illustrated together with the available information on their function.
The studies on the function of cardiolipin analogues in archaebacteria point out the tight interaction
established by these phospholipids with membrane proteins and their role as bioactive lipids in the
adaptation of microorganisms to osmotic stress.
© 2009 Elsevier B.V. All rights reserved.
1. Introduction to the membrane biochemistry of Archaea
Archaea are prokaryotes, which are able to colonize the most
extreme environments on earth. Rift vents in deep sea, hot springs,
extremely alkaline and acid waters, salt lake and coastal salterns represent typical environments where the Archaea flourish. The
biochemistry of Archaea is quite different from other forms of life;
one of the most peculiar aspects of the biochemistry of the third
domain of phylogenetic tree is represented by the structures of cell
membrane lipids.
In contrast with Eukarya and Bacteria containing largely diacylglycerol-derived membrane lipids and some monoacyl-monoalkylglycerol-derived lipids, archaeal membrane lipids are unique in
containing diphytanylglycerol diether lipids [1]. The saturated isopranoid hydrocarbon chains impart stability to peroxidation degradation and the ether linkages are resistant to chemical hydrolysis over a
wide range of pH: these properties appear to be an advantage for
microorganisms growing over a pH range of 5–10, exposed to air and
sunlight at temperature even higher than 100 °C.
The diether core lipid that forms the basis for most polar lipid
structures present in archaeal microorganisms is 2,3-di-O-phytanylsn-glycerol (C20, C20), also called archaeol (Fig. 1). Therefore archaeal
diether phospholipids contain the sn-glycerol-1-phosphate isomer
(S configuration) and not the sn-glycerol-3-phosphate isomer,
(R configuration) typically present in bacterial and eukaryal phospholipids; in other words archaeal phospholipids are the mirror
images of the analogous diester glycerophospholipid found in all other
organisms (Fig. 2).
Information on lipid biosynthesis in Archaea is available thanks to
labeling studies with whole cells [2,3].
E-mail address: a.corcelli@biologia.uniba.it.
0005-2736/$ – see front matter © 2009 Elsevier B.V. All rights reserved.
doi:10.1016/j.bbamem.2009.05.010
Examples of phospholipid structures present in the archaeal microorganisms are archaeol analogues of phosphatidylglycerol, methyl ester
of phosphatidylglycerophosphate, phosphatidylglycerosulfate and
phosphatidic acid (Fig. 3). PA is normally detected only as minor components, probably because present as biosynthetic intermediates.
While the chemical physical properties and aggregation states of
membrane lipids of Bacteria and Eukarya are well known, the knowledge of the physical properties of archaeal lipids is relatively limited.
However even from the limited knowledge of their properties and
characteristics, it is clear that archaeal lipids are well adapted as
membrane components in extreme environmental conditions.
2. The archaeal bisphosphatidylglycerol
An interesting kind of phospholipid belonging to membranes of
Bacteria and Eukarya is cardiolipin, or bisphosphatidylglycerol, a
dimeric phospholipid constituted by phosphatidic acid linked to
phosphatidylglycerol by a phosphoester bond having four chains in
the hydrophobic tail.
First evidence of the presence of cardiolipin analogues in the
Archaea domain has been obtained in my laboratory. In collaboration
with Morris Kates, we showed that the bisphosphatidylglycerol
(archaeal BPG), sn-2,3-di-O-phytanyl-1-phosphoglycerol-3-phosphosn-di-O-phytanylglycerol is present in the extremely halophilic
archaeon, Halobacterium salinarum [4].
Structure, proton NMR spectrum and the ESI-MS of the archaeal
BPG are shown in Fig. 4a–c, respectively. The proton NMR spectrum
(Fig. 4b) shows a group of resonances in the region 4.0–3.5 ppm
arising from glycerol C-1, C-2 and C-3, while phytanyl chain CH3,
CH2 and CH proton resonances are in the region 1.7–0.8 ppm. ESI-MS
in Fig. 4c shows a monocharged molecular ion [M-H]− at m/z 1521.3
and a bischarged molecular ion [M-2H] 2− at m/z 760, in
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Fig. 1. Chemical structure of 2,3-di-O-phytanyl-sn-glycerol (C20, C20), the basic unit of
archaeabacterial phospholipids.
good agreement with the molecular mass 1521.3 calculated for
C89H182O13P2. The fragmentation ions at 731.7 and 805.9 correspond
to PA and PG, which are compatible with a BPG structure.
The archaeal bisphosphatidylglycerol, being a dimeric phospholipid, with a bridge structure and four chains in the hydrophobic tail, can be considered an analogue of eukaryal and bacterial
cardiolipin.
As the stereochemistry of archaeal and bacterial membrane lipids
is different, it can be predicted that archaeal bisphosphatidylglycerol
is in the S/S configuration, whereas bacterial or mitochondrial cardiolipin is in the R/R configuration. In both R/R and S/S configurations the two phosphate groups are not chemically equivalent.
Two distinct 31P-NMR resonances have been reported for natural
cardiolipin [5]; on the contrary in the case archaeal bisphosphatidylglycerol only one phosphorus resonance was detected by phosphorus NMR analysis [4,6]. Differently from NMR analyses of mitochondrial cardiolipin carried out at high concentrations [5], the
available phosphorus NMR analyses of archaeal phospholipids
have been performed with relatively low amount of lipid material,
isolated and purified from lipid extracts of archaeons in culture with
time consuming laboratory procedures [4,6]. Further parallel NMR
studies on cardiolipin and archaeal BPG are required to clarify this
discrepancy.
The question arises if, as in the case of cardiolipin [7], the formation of a stable intramolecular hydrogen bond with the central
hydroxyl group of the bridging glycerol is possible, determining a
different level of acidity of the two phosphate residues in bisphopshatidylglycerol. Unfortunately data on pKa values of the two phosphate groups in the polar head of archaeal bisphosphatidylglycerol
are not yet available.
Information on the presence and distribution of bisphosphatidylglycerol among the halophilic Archaea, both in their natural habitat
and in culture, was obtained by analyzing with electrospray ionization
mass spectrometry the lipids extracted from the crystallizer ponds of
two different salterns in the Mediterranean Sea (Margherita di Savoia
in southern Italy and Eilat in Israel) and from cultures of various
species of halophiles. Lipid analyses revealed the presence of the
archaeal bisphosphatidylglycerol in the biomass of salterns, as well as
in all species of archaeal halophiles examined [8].
In the various species of archaeal extreme halophilic microorganisms analyzed in our laboratory, it is invariably present the archaeal
BPG carrying four identical C20 phytanyl chains; on the contrary many
molecular species of bacterial and mitochondrial cardiolipin, deriving
from difference in tail length, unsaturation and permutations of the
four acyl chains, have been described [9].
One of the most important biochemical features of cardiolipin is
its ability to tightly bind different protein complexes of the inner
mitochondrial and bacterial membranes, which have bioenergetic
functions.
Although in last years considerable information accumulates in the
literature on archaeal respiratory chains, very few data are available
regarding the association of specific archaeal lipids with enzymes
participating to oxidative phosphorylation and on the functional role
of lipids in the bioenergetic functions of Archaea.
It has been recently shown that membranes highly enriched
in bisphosphatidylglycerol, isolated from an extremely halophilic
archaeal microorganism Halorubrum sp., exhibit cytochrome c oxidase
activity. Non denaturing gel electrophoresis revealed only one fraction
having TMPD-oxidase activity in which archaeal BPG is the major lipid
component. The cytochrome c oxidase activity of the archaeal BPG
rich membranes was inhibited by the fluorescent dye 10-N-nonyl
acridine orange (NAO) in a dose dependent manner (Fig. 5), indicating
that bisphosphatidylglycerol is required for its functioning [10]. The
tight association between cardiolipin and cytochrome c oxidase in
mitochondria and bacteria is paralled in Archaea, attesting the
universality of this specific lipid–protein interaction. Specific cardiolipins appear to be involved in the function of the respiratory chain
complexes regardless of the phylogenetic background in which it
occurs. The presence of dimeric phospholipids in Archaea can be
considered as an example of convergent molecular evolution since in
spite of the similarity of the lipid backbone, the chemical nature of the
hydrophobic chain is distinct (fatty acids for bacteria and mitochondrion, phytanyl for Archaea) and consistent with the wide phylogenetic distance separating Bacteria from Archaea.
Recently the possibility to specifically label archaeal bisphopshatidylglycerol with the fluorescent dye NAO in vivo has been
examined. Both absorption and fluorescence spectroscopy studies
have indicated that the interaction of archaeal bisphosphatidylglycerol with NAO is similar to that of cardiolipin. However, it has also
been shown that other non dimeric phospholipids carrying two acid
residues in the polar head and sulfoglycolipids present in the
membrane of Archaea may mimic the interaction of mitochondrial
cardiolipin with NAO [11]. These findings imply that it is not easy to
explain NAO staining of archaebacteria, but also that NAO staining of
bacterial species containing sulfoglycolipids should be interpreted
with caution.
3. Dimeric archaeal glycophospholipids
Hbt. salinarum can be considered as a model organism of archaeal
world. One of the most interesting characteristics of Hbt. salinarum is
represented by its ability to convert light in chemical energy for the
metabolic requirements. This feature is due to the presence of a
specialized membrane domain, containing the purple protein bacteriorhodopsin, a photoactivated proton pump, which sustains the ATP
synthesis.
One of the main lipid components in the lipid extract of the purple
membrane of Hbt. salinarum is a complex phosphosulfoglycolipid, called
in laboratory jargon glycocardiolipin or GlyC, (3-HSO3-Galp-β-1,6Manp-α-1,2-Glcp-α-1,1-[sn-2,3-di-O-phytanylglycerol]-6-[phospho-sn2,3-di-O-phytanylglycerol]. Having two diphytanylglycerol moieties
(and four chains) in its molecule, the structure is analogous to that of
cardiolipin. As said before, the purple membrane also contains minor
amounts of archaeal BPG.
Interestingly GlyC consists of a sulfo-triglycosyl diphytanylglycerol
esterified to the phosphate group of phosphatidic acid; in addition
NMR analysis shows that its polar head group is composed of the
same sugars in the same sequence and anomeric configuration as in
S-TGD-1, the major membrane glycolipid of Halobacterium, namely:
Fig. 2. The different glycerol phosphate isomers used in the stereospecific biosynthesis
of (a) archaeal and (b) bacterial and eukaryal phospholipids.
A. Corcelli / Biochimica et Biophysica Acta 1788 (2009) 2101–2106
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Fig. 3. Phospholipids of archaeal microorganisms.
(βGalp→αMan→αGlc) [4]. The sulfate group is also located on C-3 of
the galactose residue, as in S-TGD-1 [12]. Therefore the novel
phosphosulfoglycolipid has been named S-TGD1-PA (Fig. 6).
Another archaeal glycosylated dimeric phospholipid was recently
found in a membrane fraction isolated from an extreme halophilic
archaeon, Halorubrum sp., isolated from the salt ponds in Margherita di
Savoia, Italy [13]. By means of NMR and ESI-MS analyses it was shown
that this cardiolipin analogue of Halorubrum also has the structure of a
sulfo-glyco-diether-phosphatidic acid, i.e. a phospholipid dimer consisting of the glycolipid S-DGD-5 esterified to phosphatidic acid,
namely S-DGD-5-PA, 2-HSO3-Manp-α-1,2-Glcp-α-1,1-[sn-2,3-di-Ophytanylglycerol]-6-[phospho-sn-2,3-di-O-phytanylglycerol] (see
structure in Fig. 6). Again, NMR analysis shows that the sugars in the
novel phospholipid are the same and in the same order as the
glycolipid S-DGD-5 isolated from the Halorubrum membranes, in
which the sulfatated mannose is linked to glucose[13]. Clearly the
glycolipids S-TGD-1 and S-DGD-5 are precursor of S-TGD-1-PA and SDGD-5-PA, respectively [13,14]. Finally the glycosyl cardiolipin analogue S-GL-2, 6′-HSO3-D-Manp-α-1,2-D-Glcp-α-1,1-[sn-2,3-di-O-phytanylglycerol]-6-[phospho-sn-2,3-di-O-phytanylglycerol] was found in
the membranes of Haloferax volcanii (Fig. 6) [15].
Dimeric phospholipids constituted by a glycolipid linked to
phosphatidic acid have been previously found in pathogenic bacteria.
Glycosylated cardiolipin was first detected in several strains of Streptococcus and identified as glucopyranosyl cardiolipin (Fig. 7) [16].
Later, in both the Gram-positive bacteria Lactococcus and Streptococcus, several complex glycolipids deriving from the kojibiosyl diacylglycerol structure were identified [17]. The function of these complex
bacterial glycophospholipids has not yet been elucidated.
4. Functional roles: protein interactions and osmoadaptation
Most information on the organization of archaeal lipids in the
lipid bilayer, as well as on lipid–protein interactions, has
been obtained from morphological, biophysical and biochemical
studies on the specialized purple membrane patches of Hbt.
salinarum [18–20]. The purple membrane contains the only protein
bacteriorhodopsin and a small number of phospholipids and
glycolipids. By electron microscopy and specific labeling, the
glycolipids have been found exclusively in the outer leaflet of the
membrane bilayer [21]. Localization of archaeal glycolipids in the
purple membranes of Hbt. salinarum has also been achieved by in
vivo labeling and neutron diffraction [22]. It has been suggested
that the specific hydrophobic interactions between the tryptophan
aromatic residues in the protein and carbohydrates in the lipids
may play an important role in the stabilization and assembly of
bacteriorhodopsin in the purple membrane [22]. It is not clear
whether both glycolipids S-TGD-1 and S-TGD-1-PA interact directly
with bacteriorhodopsin. The available biochemical data indicate
that the interactions of bacteriorhodopsin with S-TGD-1-PA are
stronger than those with S-TGD-1. It is extremely difficult to
remove S-TGD-1-PA from the annulus of bacteriorhodopsin in the
course of solubilization with detergents and even after lipid extraction with denaturing organic solvents a residual amount of
S-TGD-1-PA still remains associated with denatured bacteriorhodopsin [23]. Furthermore the S-TGD-1-PA seems to play an important role in stability and maintaining the trimeric structure of
bacteriorhodopsin [24].
The S-TGD-1-PA/bacteriorhodopsin stoichiometry in the purple
membrane has been determined by analyzing an unprocessed
lipid extract of the purple membrane with both of 31P-NMR and
1
H-NMR spectroscopy [6]. The molar ratio of S-TGD-1-PA to BR, in
standard purple membrane preparation, is one and appears to be
consistent with its possible location in the intra-trimer space [6].
Until now S-TGD-1-PA or glycocardiolipin has been found only in
the extreme halophiles and in association with bacteriorhodopsin,
while the archaeal bisphosphatidylglycerol is widespread in all
genera of the family Halobacteriaceae [8].
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Fig. 4. Structure, NMR spectrum and ESI-MS profile of isolated and purified archaeal bisphosphatidylglycerol.
Recently novel aspects regarding the regulation of the lipid
biosynthesis in the archaeal extreme halophiles have been described
[13,14]. When archaeal extreme halophiles are exposed to low salt
conditions, relevant changes in the cell membrane lipid composition
occur; during the adaptation of extreme halophilic microorganisms to
hypo-osmolarity the membrane undergoes significant biochemical
and structural changes, especially in terms of an increase in the
content of cardiolipin analogues.
Fig. 5. Inhibition of archaeal cytochrome c oxidase activity by NAO in bisphopshatidylglycerol rich membranes, isolated from an extreme halophilic microorganism.
Oxidation kinetics of reduced horse heart cytochrome c (10 μM) by the archaeal
membranes (protein concentration 9.4 μM). The reaction was followed at 550–540 nm;
reported traces are the average of five independent experiments.
As stated above, Hbt. salinarum cells possess a phospholipid dimer
consisting of a glycolipid sulfo-triglycosyl-diether (S-TGD-1) esterified to the phosphatidic acid (PA), i.e. S-TGD-1-PA. S-TGD-1-PA is
almost absent in the lipid extract of cells of Hbt. salinarum, while it is
abundant in the purple membrane (PM), which is typically isolated
after cell disruption by osmotic shock. It has been shown that osmotic
stress specifically induces S-TGD-1-PA increase at the expenses of
S-TGD-1 in Hbt. salinarum cells [14]. The membrane content of the
archaeal cardiolipin analogue S-TGD-1-PA appears to be modulated by
the extent of the incubation time and of osmotic unbalance across the
membrane. Therefore, it is possible to isolate purple membrane at
variable S-TGD-1-PA content to study the effect of subtle variation in
the protein lipid annulus composition, avoiding the use of detergents
and exogenous lipids [25]. Recently, osmotic shock has been also used
as tool to modulate the cardiolipin content in native membrane of
chromatophores of Rhodobacter sphaeroides [26]. Another example of
the osmoregulated neosynthesis of phospholipid dimers in extremely
halophilic Archaea has been described in an archaeon of the Halorubrum genus; membranes isolated after cell disruption by osmotic
shock from Halorubrum sp. are highly enriched in archaeal bisphosphatidylglycerol (BPG) and reveal the presence of the cardiolipin
analogue (or phospholipid dimmer) having the structure of a sulfodiglycosyl-diether-phosphatidic acid (S-DGD-5-PA). It has been
clearly demonstrated that hyposmotic shock induces a specific
increase in the content of archaeal BPG and S-DGD-5-PA in Halorubrum sp., at the expense of phosphatidylglycerol and the glycolipid SDGD-5, respectively [13]. Fig. 8 illustrates the conversion of PG in BPG
in Halorubrum sp cells under osmotic shock. The evidence that
osmotic shock stimulates the de novo synthesis of phospholipid
dimers, i.e. cardiolipin analogues, in extreme halophilic Archaea,
together with similar literature reports on bacterial organisms [for
A. Corcelli / Biochimica et Biophysica Acta 1788 (2009) 2101–2106
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Fig. 6. Dimeric glycophospholipids of extremely halophilic archeons.
example as in refs 26–30], suggests a general role for “cardiolipin” in
osmoadaptation.
A higher archaeal cardiolipin cell content could protect the cell
from lysis. The increase in archaeal cardiolipin occurring in cells
undergoing osmotic shock may represent the physiological response
of the extremely halophilic archaeal microorganisms to the dilution of
the salt saturated water occurring during rainfalls. The modifications
in lipid composition could affect the physical–chemical properties of
the membrane, such as bilayer thickness, membrane fluidity and
transport properties.
Much remains to be learned concerning the precise asymmetric
arrangement of the archaeal cardiolipins in the membrane bilayer, the
precise mode of interaction of the cardiolipins with the membrane
proteins, the transmembrane distribution with respect to ion transport, permeability to nutrients, proton transport and conductance,
and energy transduction.
Fig. 7. Structure of a bacterial dimeric glycophospholipid.
Fig. 8. Conversion of phosphatidylglycerol (PG) in bisphosphatidylglycerol (BPG) in an
extremely halophilic archeon under osmotic stress.
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A. Corcelli / Biochimica et Biophysica Acta 1788 (2009) 2101–2106
Acknowledgements
With the financial support of MIUR (Minister of School, University
and Research) and the Italian Minister of Defense.
References
[1] M. Kates, Membrane lipids of Archaea, in: M. Kates, D.J. Kushner, A.T. Matheson
(Eds.), The Biochemistry of Archaea (Archaebacteria), Elsevier, Amsterdam, 1993,
pp. 261–295.
[2] M. Kates, M.K. Wassef, D.J. Kushner, Radioisotopic studies on the biosynthesis of
the glyceryl diether lipids of Halobacterium cutirubrum, Can. J. Biochem. 46 (1968)
971–977.
[3] Y. Boucher, M. Kamekura, W.F. Doolittle, Origins and evolution of isoprenoid lipid
biosynthesis in archaea, Mol. Microbiol. 52 (2) (2004) 515–527.
[4] A. Corcelli, M. Colella, G. Mascolo, F.P. Fanizzi, M. Kates, A novel glycolipid and
phospholipid in the purple membrane, Biochemistry 39 (2000) 3318–3326.
[5] G.L. Powell, J. Jacobus, Nonequivalence of the phosphorus atoms in cardiolipin,
Biochemistry 13 (1974) 4024–4026.
[6] A. Corcelli, V.M.T. Lattanzio, P. Papadia, F.P. Fanizzi, Lipid/protein stoichiometries
in a crystalline biological membrane: NMR quantitative analysis of the lipid
extract of the purple membrane, J. Lipid Res. 43 (1) (2002) 132–140.
[7] M. Kates, J.Y. Syz, D. Gosser, T.H. Haines, pH-dissociation characteristics of
cardiolipin and its 2′-deoxy analogue, Lipids 28 (1993) 877–882.
[8] V.M.T. Lattanzio, A. Corcelli, G. Mascolo, A. Oren, Presence of two novel
cardiolipins in the halophilic archaeal community in the crystallizer brines from
the salterns of Margherita di Savoia (Italy) and Eilat (Israel), Extremophiles 6
(2002) 437–444.
[9] M. Schlame, M. Ren, Y. Xu, M.L. Greenberg, I. Haller, Molecular symmetry in
mitochondrial cardiolipin, Chem. Phys. Lipids 138 (2005) 38–49.
[10] A. Corcelli, S. Lobasso, L.L. Palese, M. Sublimi Saponetti, S. Papa, Cardiolipin is
associated with the terminal oxidase of an extremely halophilic archaeon, BBRC
354 (2007) 795–801.
[11] S. Lobasso, M. Sublimi Saponetti, F. Polidoro, P. Lopalco, J. Urbanija, V. Kralj-Iglic, A.
Corcelli, Archaebacterial lipid membranes as models to study the interaction of 10n-nonyl acridine orange with phospholipids, Chem. Phys. Lipids 157 (2009) 12–20.
[12] M. Kates, P.W. Deroo, Structure determination of the glycolipid sulfate from the
extreme halophile Halobacterium cutirubrum, J. Lipid Res. 14 (1973) 438–445.
[13] P. Lopalco, S. Lobasso, F. Babudri, A. Corcelli, Osmotic shock stimulates de novo
synthesis of two cardiolipins in an extreme halophilic archaeon, J. Lipid Res. 45
(2004) 194–201.
[14] S. Lobasso, P. Lopalco, V.M.T. Lattanzio, A. Corcelli, Osmotic shock induces the
presence of glycocardiolipin in the purple membrane of Halobacterium salinarum,
J. Lipid Res. 44 (2003) 2120–2126.
[15] G.D. Sprott, S. Laroque, N. Cadotte, C.J. Dicaire, M. McGee, J.I. Brisson, Novel polar
lipids of halophilic eubacterium Planococcus H8 and archaeon Haloferax volcanii,
Biochim. Biophys. Acta 1633 (2003) 179–188.
[16] W. Fischer, The polar lipids of group B Streptococci. I. Glucosylated diphosphatidylglycerol, a novel glycophospholipid, Biochim. Biophys. Acta 487 (1) (1977)
74–88.
[17] W.M. O'Leary, S.G. Wilkinson, Gram positive bacteria, Chapter 5, in: C. Ratledge, C.
May, et al., (Eds.), Microbial Lipids, 1, Acad Press, 1988, pp. 117–201.
[18] D. Oesterhelt, W. Stoeckenius, Isolation of cell membrane of Halobacterium
halobium and its fractionation into red and purple membrane, Methods Enzymol.
31 (1974) 667–678.
[19] N. Grigorieff, T.A. Ceska, K.H. Dowing, J.M. Baldwin, R. Henderson, Electroncrystallographic refinement of the structure of bacteriorhodopsin, J. Mol. Biol. 259
(1996) 393–421.
[20] M.P. Krebs, T.A. Isenbarger, Structural determinants of purple membrane
assembly, Biochem. Biophys. Acta 1460 (2000) 15–26.
[21] R. Henderson, J.S. Jubb, S. Whytock, Specific labelling on the protein and lipid
on the extracellular surface of purple membrane, J. Mol. Biol. 123 (1978)
259–274.
[22] M. Weik, H. Patzelt, G. Zaccai, D. Oesterhelt, Localization of glycolipids in membrane by in vivo labeling and neutronal diffraction, Mol. Cell 1 (1998) 411–419.
[23] L. Catucci, V.M.T. Lattanzio, S. Lobasso, A. Agostiano, A. Corcelli, Role of
endogenous lipids in the chromophore regeneration of bacteriorhodopsin,
Bioelectrochemistry 63 (2004) 111–115.
[24] F. Lopez, S. Lobasso, M. Colella, A. Agostano, A. Corcelli, Light-dependent and
biochemical properties of two different bands of bacteriorhodopsin isolated on
phenyl-sepharose CL-4B, Photochem. Photobiol. 69 (1999) 599–604.
[25] A. Corcelli, S. Lobasso, M. Sublimi Saponetti, A. Leopold, N.A. Dencher, Glycocardiolipin modulates the surface interaction of the proton pumped by bacteriorhodopsin in purple membrane preparations, BBA-Biomembranes (2007)
2157–2163.
[26] V. De Leo, L. Catucci, A. Ventrella, F. Milano, A. Agostiano, A. Corcelli, Cardiolipin
increases in chromatophores isolated from Rhodobacter sphaeroides after osmotic
stress: structural and functional roles, J. Lipid Res. 50 (2) (2009) 256–264.
[27] A. Okabe, Y. Hirai, H. Hayashi, Y. Kanemasa, Alteration in phospholipid composition of Staphilococcus aureus during formation of autoplast, Biochim. Biophys.
Acta 617 (1) (1980) 28–35.
[28] L. Catucci, N. Depalo, V. Lattanzio, A. Agostiano, A. Corcelli, Neo-synthesis of
cardiolipin in Rhodobacter sphaeroides under osmotic stress, Biochemistry 43 (47)
(2004) 15066–15072.
[29] T. Romantsov, S. Helbig, D.E. Culham, C. Gill, L. Stalker, J.M. Wood, Cardiolipin
promotes polar localization of osmosensory transporter ProP in E. coli, Mol.
Microbiol. 64 (6) (2007) 1455–1465.
[30] E. Mileykovskaya, Subcellular localization of Escherichia coli osmosensor transporter ProP: focus on cardiolipin membrane domains, Mol. Microbiol. 64 (6)
(2007) 1419–1422.

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