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Originally published In Press as doi:10.1194/jlr.M700152-JLR200 on May 22, 2007

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Journal of Lipid Research, Vol. 48, 1825-1831, August 2007
Copyright © 2007 by American Society for Biochemistry and Molecular Biology

Structural elucidation of a novel phosphoglycolipid isolated from six species of Halomonas

Assunta Giordano1, Filomena M. Vella, Ida Romano and Agata Gambacorta

Istituto di Chimica Biomolecolare, Consiglio Nazionale delle Ricerche, 34 80078 Pozzuoli, Italy

Published, JLR Papers in Press, May 22, 2007.

1 To whom correspondence should be addressed. e-mail: agiordano{at}icmib.na.cnr.it


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The structure of a new phosphoglycolipid from the halophilic Gram-negative bacteria Halomonas elongata ATCC 33173T, Halomonas eurihalina ATCC 49336T, Halomonas almeriensis CECT 7050T, strain Sharm (AM238662), Halomonas halophila DSM 4770T, and Halomonas salina ATCC 49509T was elucidated by NMR and mass spectroscopy studies. In all of the species examined, the polar lipid composition consisted of 1,2-diacylglycero-3-phosphorylethanolamine, 1,2-diacylglycero-3-phosphoryl-glycerol, bisphosphatidyl glycerol, and the new phosphoglycolipid PGL1. The structure of PGL1 was established to be (2-({alpha}-D-glucopyranosyloxy)-3-hydroxy-propyl)-phosphatidyl diacylglycerol. C16:0;C18:1 and C16:0;C19:cyclopropane are the most abundant acyl chains linked to the phosphatidylglycerol moiety of each isolated PGL1. All of the species presenting the lipid PGL1 belong to Halomonas rRNA group 1, suggesting that the new phosphoglycolipid could be a chemotaxonomic marker of this phylogenetic group.

Supplementary key words Halomonas elongata ATCC 33173T • Halomonas eurihalina ATCC 49336T • Halomonas almeriensis CECT 7050T • strain Sharm (AM238662) • Halomonas halophila DSM 4770T • Halomonas salina ATCC 49509T • nuclear magnetic resonance spectroscopy • tandem mass spectrometry

Abbreviations: CD, circular dichroism; DPG, bisphosphatidyl glycerol; DQF-COSY, double quantum-filtered correlation spectroscopy; FAME, fatty acid methyl ester; HMBC, heteronuclear multiple bond coherence; HSQC, heteronuclear single quantum coherence; PEA, phosphatidylethanolamine; PG, phosphatidylglycerol


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Halophile organisms are able to withstand fluctuations of extracellular salinity using two strategies that can operate simultaneously. The first one involves the cytoplasmic accumulation of small organic compounds, called osmolites or compatible solutes, which enable the cell to reduce the water loss and to maintain the cell pressure by reducing the osmotic potential between the cell and the cytoplasm (1, 2). The second one consists of modifying the membrane structure, generally affecting phospholipids and their fatty acid composition. In halophilic Gram-negative bacteria, the increase in salt concentration usually corresponds to a decrease of the zwitterionic phospholipid phosphatidylethanolamine (PEA) and an increase of the anionic lipids phosphatidylglycerol (PG) and/or bisphosphatidyl glycerol (DPG) as well as the incorporation of cyclopropanic rings and double bonds in fatty acid chains (3, 4). Regulation of the phospholipid composition of the cell membrane is also used by the microorganisms to adjust the proton permeability of the membrane to the growth temperature of the cell (5, 6).

Phosphoglycolipids have a relatively limited distribution among Gram-negative bacteria compared with Gram-positive bacteria. Among euryhaline microorganisms, Halomonas species are widely distributed throughout saline environments and constitute a remarkably high percentage of the total microbial community in hydrothermal vent habitats. The polar lipid composition shows a general pattern, because PEA, PG, and DPG are the major lipid components. The presence of unknown lipids was first described in 1990 by Franzmann and Tindall (7), who reported the occurrence of unidentified periodate-Schiff-positive phospholipids in some species of the Halomonas genus. In 1998, Yagi and Maruyama (8) described in a patent the presence of new glucosyl phosphatidyl glycerol derivatives in Halomonas marina. In this study, the structure of a new phosphoglycolipid present in six strains belonging to the genus Halomonas was elucidated by NMR and mass spectroscopy studies.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Isolation and culture conditions
During the summer of 2005, samples of water with mat were collected from the salt lake inside Ras Muhammad Park in Egypt; pH was 8.5 and temperature was 30°C.

Isolation of Sharm strain was carried out on a saline medium (medium 1) containing the following components: 2.0 g/l KCl, 20 g/l MgSO4·7H2O, 150 g/l NaCl, 3.0 g/l sodium citrate, 5.0 g/l yeast extract, 5.0 g/l casamino acids, 0.36 µg/l MnCl2·4H2O, and 50 µg/l FeSO4. The strain was isolated by dilution-plating technique on solid medium 1. Solid medium for purification and maintenance of the strain was prepared by the addition of 1.8% agar to medium 1. Routinely, the strain was grown on liquid and/or solid medium 1. In liquid medium, growth was followed by measuring the absorbance at 540 nm. Halomonas elongata ATCC 33173T (9), Halomonas eurihalina ATCC 49336T (10), Halomonas salina (11), and Halomonas halophila DSM 4770T (12) were obtained from the Deutsche Sammlung von Mikroorganismen und Zellkulturen (Brunschweig, Germany). Halomonas almeriensis CECT 7050T was kindly provided by Martinèz-Checa et al. (13). All of the strains were grown in the media at their optimal growth conditions, as suggested in the literature.

Lipid extraction and characterization
Complex lipid analyses were performed using freshly harvested cells of the strains (5 g) that were lyophilized and extracted. Cells in the stationary phase were collected by centrifugation and lyophilized. Dry cells were extracted with chloroform-methanol-water (65:25:4, v/v) and evaporated under reduced pressure. The lipid extract was analyzed by two-dimensional TLC on silica gel plates cut to 10 cm x 10 cm. The TLC products were developed in chloroform-methanol-water (65:25:4; first dimension) and chloroform-methanol-acetic acid-water (80:12:15:4; second dimension). The lipid extract was then fractionated by flash chromatography on silica gel with methanol-chloroform (1:9, v/v), methanol-chloroform (2:8), methanol-chloroform (3:7), and methanol-chloroform-water (25:75:4). The fraction eluted with chloroform-methanol-water (25:75:4) was purified by preparative TLC eluting with chloroform-methanol-water (25:75:4; retention factor of phosphoglycolipid PGL1, 0.25). Polar lipids were quantified by the weight of the isolated fractions.

13C NMR spectra were acquired on a Bruker DPX-300 operating at 300 MHz using a dual probe. 1H, 1H-1H double quantum-filtered correlation spectroscopy (DQF-COSY), heteronuclear multiple bond coherence (HMBC), and heteronuclear single quantum coherence (HSQC) experiments were recorded on a 600 MHz Bruker instrument. Chemical shifts were given in ppm ({delta}) scale; the methanol signal was used as the internal standard ({delta} 3.34 1H; {delta} 49.0 13C). Mass spectra of the unknown phosphoglycolipid were recorded on a QTof-/micro/mass spectrometer (Waters) equipped with an electrospray ionization source in negative ion mode.

Fatty acid methyl esters (FAMEs) were obtained from complex lipids by acid methanolysis incubating phosphoglycolipids with 0.5 M methanol-HCl at 80°C for 1 h. The solvent was removed under vacuum, and the residue was mixed with chloroform and water. FAMEs partitioned into the organic phase. GC-MS analysis of FAMEs was performed with an HP5890 series II plus-5989B equipped with an HP-V column with a flux of 45 ml/min. The analysis program was 60°C for 1 min, 60–140°C at 25°C/min, 140–200°C at 5°C/min, and 200–300°C at 10°C/min.

PGL1 (2 mg) was incubated in 1 M methanol-HCl (1 ml) at 60°C for 12 h. The reaction mixture was dried and partitioned between chloroform and water-methanol (8:2). The aqueous layer containing the sugar was concentrated, filtered on a Sep-Pak cartridge, and dried. Benzoyl chloride (0.5 ml) and dry pyridine (0.5 ml) were added to the methanolysis products. After 12 h at room temperature, the mixture was dried and purified on silica gel (hexane/diethyl ether gradient) to give 0.7 mg and 0.4 mg of pure {alpha}- and ß-tetra-benzoate. The absolute stereochemistry of the sugar was determined by comparison of the circular dichroism (CD) spectra of the benzoate derivatives with samples prepared from commercial {alpha}- and ß-methyl-D-glucopyranose, respectively. For CD (n-hexane), [{theta}]248 1640 for {alpha} derivative and [{theta}]235 613 for the ß derivative.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The strain Sharm was isolated from samples of water with mat collected from a saline lake inside Ras Muhammad Park in the promontory of Sinai Peninsula in Egypt. The Gram-negative microorganism grew aerobically in enrichment medium containing up to 30% NaCl, with an optimum at 5–15% NaCl. The 16S rRNA gene sequence (EMBL database accession number AM238662) was determined (data not shown) and compared with all sequences currently available for members of the genus Halomonas and related taxa. The results are presented as a phylogenetic dendrogram (Fig. 1 ) showing that strain Sharm is a member of the genus Halomonas. The strain clustered together with the species H. elongata and H. eurihalina and other species of the rRNA group 1, according to the phylogenetic classification of Halomonas (14).


Figure 1
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  		Fig. 1. Neighbor-joining tree based on 16S rRNA gene sequences showing the phylogenetic relationships of strain Sharm and other Halomonas species. The bar indicates 0.01 substitutions per nucleotide position. Strains belonging to rRNA group 1 of Halomonas are marked with a bracket.

 
The total lipid compositions of strain Sharm and the five related species, H. elongata, H. eurihalina, H. salina, H. almeriensis, and H. halophila, are reported in Table 1 . The isolate Sharm possessed three phospholipids, PEA (13%), PG (51.4%), and DPG (0.7%), and the new phosphoglycolipid PGL1 (33.0%), identified by NMR studies. Polar lipid analysis of the other Halomonas strains showed that these species contain the same lipid pattern but with different distribution (Table 1).


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  		TABLE 1. Polar lipid pattern and FAME composition of PGL1 in the examined Halomonas species

 
The structure of phosphoglycolipid PGL1 and NMR assignments are reported in Fig. 2 and Table 2 . The presence of spin systems corresponding to one sugar unit (H1-H6), two glycerols (H1'-H3' and H1''-H3''), and fatty acids was suggested from 1H, 13C, and 1H-1H DQF-COSY spectra. The HSQC spectrum gave the assignment of carbons directly bonded to protons. The 1H and 13C NMR spectra contained methyls ({delta}H 0.88), methylene chains ({delta}H 1.25–2.42), double bonds ({delta}H 5.33, {delta}C 130.0) in methylene chains, and carbonyl carbons ({delta}C 173.2, 173.4), suggesting the presence of fatty acid moieties. Moreover, the presence of 1H signals at ~–0.4 ppm indicated the presence of a cyclopropanic ring.


Figure 2
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  		Fig. 2. Structure of phosphoglycolipid PGL1 [(2-({alpha}-D-glucopyranosyloxy)-3-hydroxy-propyl)-phosphatidyl diacylglycerol].

 

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  		TABLE 2. NMR data of PGL1 in CDCl3/CD3OD

 
The HSQC spectrum (Fig. 3 ) also revealed one anomeric methine ({delta}H 4.99, {delta}C 98.8), suggesting the presence of one sugar unit with {alpha}-configuration (J1-2 = 3.6). Starting from the anomeric proton H1, interpretation of COSY correlations (Fig. 4 ) allowed us to assign the {delta}H of the protons of the sugar ring (Fig. 4). The high values of the coupling constants J2-3 (9.90 Hz), J3-4 (9.0 Hz), and J4-5 (9.2 Hz) indicated the axial orientation of H2, H3, H4, and H5; thus, the sugar was assigned as a glucopyranose ring in the 4C1 conformation.


Figure 3
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  		Fig. 3. Sections of heteronuclear single quantum coherence and 1H NMR spectra of PGL1. 1H-13C correlations relative to glucose and the phosphatidylglycerol (PG) moiety are visible.

 

Figure 4
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  		Fig. 4. Double quantum-filtered correlation spectroscopy spectrum of PGL1. 1H-1H correlations of the glucose ring and the PG moiety are visible.

 
Four oxymethylenes and two oxymethines were assigned as two glycerol units on the basis of the spin system from 1H-1H COSY and their directly bonded carbons (Fig. 4). Coupling constants of the carbon signals indicated the presence of a phosphate unit linking the two glycerols. In particular, the small values of JC3'-P and JC1''-P are diagnostic for the presence of a phosphate group directly linked to these carbons. HMBC cross-peak H2'/C1 (3.90/98.8) showed that the glucose molecule is attached to the C2 of the first glycerol moiety (Fig. 5 ). Furthermore, long-range correlations of the H2'' and H3'' with the carbonyl carbons demonstrated that the two acyl groups were located on C-2'' and C-3'' oxydryls (5.25 and 4.42–4.19/169.2).


Figure 5
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  		Fig. 5. 1H-13C heteronuclear multiple bond coherence correlations between H2'' and H3'' and the carbonyl carbons of acyl chains (4.42–4.19/169.2) and between the secondary oxymethine proton of PG and the anomeric carbon (3.90/98.8).

 
The stereochemistry of the glucose unit was determined by comparison of the CD spectra of the purified benzoylated {alpha}- and ß-methyl glucopyranoses. The CD curves of the benzoyl derivatives were identical to those of the corresponding compounds obtained from benzoylation of commercial {alpha}- and ß-methyl-D-glucopyranoses, indicating the D absolute stereochemistry of the sugar unit.

The fatty acid moieties were determined by tandem MS spectra and GC-MS analysis (Table 1). The mass spectra contained several molecular ion peaks indicating differences in the type and distribution of the acyl chains on the PG backbone. For Sharm strain, the most abundant were determined to be C16:0 and C19:cyclopropane, corresponding to the highest peak of m/z 923 in the MS spectrum (Fig. 6A ). In tandem MS spectra using negative ion electrospray ionization (Fig. 6B), fragmentation of the molecular ion m/z 923 (M-H) led to fragment ions 295 (C19:cyc-H) and 255 (C16-H). Mass spectrometry analysis of phosphoglycolipids isolated from the other Halomonas species allowed us to establish the identity of acyl chains linked to the glyceryl moiety. It was shown that all lipids carry two acyl chains, the most abundant being C16:0;C18:1. The fatty acid composition was also confirmed by GC-MS analysis of methyl esters obtained by acid methanolysis of the phosphoglycolipids. The structure of the phosphoglycolipid present in Sharm strain, H. elongata, H. eurihalina, H. salina, H. almeriensis, and H. halophila was established to be 2-({alpha}-D-glucopyranosyloxy)-3-hydroxy-propyl)-phosphatidyl diacylglycerol.


Figure 6
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  		Fig. 6. Negative-ion electrospray ionization-MS spectra of PGL1 from Sharm strain. A: Ion peaks of m/z 909, 923, and 963 correspond to a different distribution of acyl chains (C16:0;C18:1, C16:0;C19cyc, and C19cyc;C19cyc, respectively). B: Tandem MS-QTof spectrum of precursor ion m/z 923.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Polar lipids and their fatty acids can be used as biochemical markers because many of them have unique structures. Lipid structures related to that described for Sharm strain were found in microorganisms classified in genera not related to Halomonas, such as Mycoplasma, Acholeplasma, and Streptococcus (15–19). The presence of phosphoglycolipids in several strains belonging to the Halomonas genus was detected by Franzmann and Tindall (7), who analyzed the general composition of polar lipids of many members of the family Halomonadaceae. In 1998, Yagi and Maruyama (8) described in a patent new glucosyl phosphatidyl glycerol derivatives in H. marina.

In connection with our ongoing search for new halophilic and alkalohalophilic phenotypes on different continents (20–23), we isolated a new halophilic strain from a salt lake inside Ras Muhammad Park in Egypt. Phylogenetic analysis of Sharm strain indicated that the strain clustered together with the species H. elongata and H. eurihalina, suggesting that it could belong to the rRNA group 1, according to the Arahal et al. (14) classification of Halomonas. Chemotaxonomic characterization of this strain showed the presence of a large amount of an unidentified compound in the polar lipid extract, positive to sugar and phosphate reaction on TLC.

Interestingly, lipid analysis of the species most related to Sharm strain shows that this new lipid is present in five other members of Halomonas rRNA group 1, confirming a relationship between these species. H. elongata, H. eurihalina, H. salina, H. almeriensis, and H. halophila, grown at their optimal growth conditions, possess the same polar lipids of the Egyptian isolate, although in different proportions. PEA is the major lipid in all of the species with the exception of the Egyptian isolate. Phosphoglycolipid PGL1 accounts for 35% of the total lipid composition of Sharm strain but is present in lower amounts (between 2% and 11%) in the other Halomonas species.

NMR and mass spectroscopic analyses allowed us to establish the structure of PGL1. The chemical shifts and the coupling constants of 1H NMR and 13C spectra indicate the presence of one residue of glucopyranose in {alpha} configuration. The anomeric carbon is directly linked to a diacylated PG molecule. An interesting feature of PGL1 is its unusual linkage of the sugar to the secondary oxydryl group of PG, a structure resembling that of glycosylated teichoic acids of Gram-positive bacteria. Halomonas species are usually rich in C18:1 and C16:0 acyl chains, whereas an increment of cyclopropanic rings is a common response to higher salinity. The FAME composition of each purified phosphoglycolipid agrees with this general rule and is quite superimposable on that of the total lipid fraction. In all of the species, C16:0;C18:1 and C16:0;C19:cyclopropane are the most abundant acyl chains linked to the PG moiety.

To survive in harsh environments, microorganisms modify their membrane structures to modulate the chemical composition of lipids. One of the possible biological roles of phosphoglycolipids in halophilic bacteria is to ensure the osmotic stability of the cellular membrane. Bulky head groups would enhance steric protection through hydrogen bonding via glycosyl head groups (24). This study elucidates the structure of a new phosphoglycolipid that is present in all of the species of Halomonas rRNA group 1. It would be interesting to extend detailed lipid characterization to all Halomonas species to determine whether the new phosphoglycolipid is a chemotaxonomic marker of group 1 or whether it is a common feature of Halomonas.


   ACKNOWLEDGMENTS
 
This work was supported by the Centro Regionale di Competenza in Applicazioni Tecnologiche-Industriali di Biomolecole e Biosistemi. The authors thank Eduardo Pagnotta for technical assistance, Vincenzo Mirra, Salvatore Zambardino, and Dominique Melck for NMR-Istituto di Chimica Biomolecolare service, Maurizio Zampa for MS analyses, and Emilio P. Castelluccio for computer system maintenance.

Submitted on March 29, 2007
Revised on May 11, 2007


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TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
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