Ceramide phosphorylglycerol phosphate. A New Sphingolipid Found in Bacteria. and ceramide phosphorylglycerol
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1 Ceramide Phsphrylglycerl Phsphate A New Sphinglipid Fund in Bacteria DAVD C. WHTE and ANNE N. TUCKER, Department f Bichemistry, University f Kentucky Medical Center, Lexingtn, Kentucky ABSTRACT Ceramide phsphrylglycerl phsphate (CPGP) has been identified in the lipid extract f the anaerbic bacterium Bactericles rnelaningenicus. T ur knwledge this is the first reprt f this lipid in bilgical material. The ceramide derivative cntains tw phsphates, an amide linked fatty acid and a dihydrsphingsine lng chain base. Glycerl diphsphate (PGP) identified by paper and clumn chrmatgraphy can be islated after mild acid hydrlysis f the ceramide derivative. nrganic phsphate is liberated quantitatively n treatment f the PGP frm the ceramide derivative with alkaline phsphatase. The prprtins f the fatty acids fund linked t the amide f the dihydrsphingsine (LCB) differ frm thse esterified t cardilipin in this rganism. The lng chain base appears t cnsist f part f an hmlgus series f branched and nrmal LCB cntaining frm 17 t 21 carbn atms. Previus wrk has indicated that ceramide phsphrylethanlamine and ceramide phsphrylglycerl (CPG) are present in the lipid extracts f B. melaningenicus. By analgy with phsphatidylglycerl synthesis, CPGP is pstulated t be an intermediate in the synthesis f CPG. NTRODUCTON The anaerbic bacterium Bacterides melaningenicus has been shwn t cntain phsphate cntaining sphinglipids which accunt fr half the extractible lipid phsphate (1). Sphinglipids are exceedingly rare in eubacteria (2). Ceramide phsphrylethanlamine (CPE), a rare sphinglipid previusly reprted in insects, prtza and certain snails, and ceramide phsphrylglycerl (CPG), a lipid nt previusly reprted, make up the majr prtin f the sphinglipid f B. melaningenicus (1) A trace f a third phsphate cntaining sphinglipid was detected. n this study the trace ceramide has been identified as ceramide phsphrylglycerl phsphate (CPGP), a lipid nt previusly described in nature. Materials MATERALS AND METHODS The strain f B. m elaningenieus, the cultural cnditins, harvesting prcedures and methds fr insuring cultural purity have been described in previus wrk (1,3). H 332 p 4 was supplied in plastic bttles by Tracerlabs, Waltham, Mass. Clumn Chrmatgraphy Fatty acid methyl esters were separated frm ceramides r LCB n 1 g silicic acid clumns ( 1 X 50 ram, Unisil, mesh). The fatty acid methyl esters were eluted in 5 ml f chlrfrm. The dihydrsphingsine lng chain bases (LCB) r ceramides were eluted with 5 ml f chlrfrm-methanl, (1:1) fllwed by 5 ml f methanl. Glycerl phsphate esters derived frm the lipids were eluted frm 0.4 X 81 cm clumns f Dwex-1 8X ( mesh) in the frmate frm prepared as described (4,5). The esters were eluted with an ammnium frmatesdium brate gradient (4) r with 0.3 M ammnium frmate ph 9.5 (Lester, unpublished methd). The esters were desalted with Dwex-1 ( mesh) as described in the text. Paper Chrmatgraphy Lipids were separated n silica gel laded paper (Whatman SG-81) using slvents f chlrfrm-methanl-diisbutylketne-acetic acidwater (23:10:45:25:4 v/v), Slvent 1 in the first dimensin and chlrfrm-methanl-diisbutylketne-pyridine-0.5 M ammnium acetate ph 10.4 (30:17.5:25:35:6 v/v), Slvent 2. Lipids were eluted frm the silica gei laded paper with a slvent f chlrfrm-methanl- 19 mm ammnium hydrxide (20:20:1) by saking the paper in 3 ml f slvent fr 1 hr. The paper was then rinsed in three 1 ml prtins f slvent. The recvery was quantitative. Glycerl phsphate esters were separated n acid washed amin-cellulse paper (Whatman AE-81) (7). Slvents were 0.4% pyridine in 3 M frmic acid and mdified Wawszkiewicz slvent (5). This slvent cntains 1.15 M ammnium acetate with 11.8 mm ethylenediaminetetra- 56
2 CERAMDES FROM BACTERA 57 B_ MELANNOGENCUS LPD (12/~ MOLES LPD P} PAPER CHROMATOGRAPHY... f.....? TOP HAND MDDLE HAND LOWER HAND (036/~ MOLES LPD P) PG PS CL PE CPE PA CPG C-07[ ] 2D - PAPER CHROMATOGRAPHY CL CPG 3 CPE C-OT NONE NONE (SEE FG 2) (99% OF 32p OF TOP HAND) MLD ALKALNE METHANOLYSS AQUEOUS PHASE LPD (0.16/~ MOLES LPD P) (020p.MOLES LPD P) GPGPG (C-O 71) FATTY ACD METHYL ESTERS SLCC ACiD COLUMN CL FATTY ACD METHYL ESTERS C-0.7 GLC (SEE FG. 3) (SEE TABLE ) ACD HYDROLYSS AQUEOUS PHASE PGP LPD SLCC ACD COLUMN C*O.71 FATTY ACD + METHYL ESTERS LCB~TMS ~ - LOB GLC GLC (SEE TABLE [) FG. 1. Flw sheet fr the purificatin f the unknwn ceramide derivative. acetic acid made t ph 5.0 with acetic acid and diluted 3 t 7 with 95% ethanlic 0.25 M ammnium hydrxide. Schleicher and Schuell 589 acid washed paper was used with ascending paper chrmatgraphy with the mdified Wawszkiewicz slvent. The lipids were detected with the Hanes-sherwd reagent fr phsphate (4) r by peridate treatment fllwed by -tluidine (4). Gas Chrmatgraphy Fatty acid methyl esters were prepared and separated n ethylene glycl succinate r SE-30 clumns under the cnditins described previusly (8). Trimethylsilyl ether derivatives (TMS) f the LCB were prepared and analyzed as in an earlier study (1). Measurement f Radiactivity 32 p was cunted n paper disks in a scintillatin spectrmeter (7). Radiautgrams were prepared with Kdak n-screen x-ray film (7). llustratins f radiautgrams were prepared by drawing the figures, cpying the figure n a mylar sheet with the Xerx cpier, then superimpsing the develped film and the mylar sheet prperly. The sheet and superimpsed film were then phtgraphed n a glw bx. FG. 2. Radiautgram f the chrmatgraphic separatin f the unknwn ceramide derivative and CL frm B. melaningenicus grwn with 32p. See Materials and Methds and Reference 7. Extractin and Analysis f the Lipid Lipids were extracted frm the bacteria by a mdified Bligh and Dyer prcedure (9). A 30 ml suspensin f bacteria in 50 mm phsphate buffer ph 7.6 cntaining abut 200 mg dry weight f cells was mixed with 75 ml f methanl and 37.5 ml f chlrfrm and shaken vigrusly. The ne phase system was allwed t stand vernight. Then 37.5 ml f chlrfrm and 37.5 ml f 1.0 M KCL slutin cntaining glacial acetic acid (0.4% v/v) was added and the mixture shaken. After several hurs the mixture separated int tw phases. The lwer layer cntaining the lipid was filtered thrugh a 4 cm piece f Whatman N. 12 filter paper. Purificatin f the Lipid A flw chart f the purificatin f the unknwn lipid is illustrated in Figure 1. A ttal f 12 #mles f lipid phsphate islated frm cells grwn in the presence f a2p was sptted near the bttm edge f tw silica gel impregnated papers. The lipids were separated int three bands by ascending chrmatgraphy in a slvent f chlrfrm-methanl-diisbutylketne-acetic acid-water (23:10:45:25:4 v/v). The bands were lcated by radiautgraphy LPDS, VOL. 5, NO. 1
3 5 8 DAVD C. WHTE AND ANNE N. TUCKER TABLE Distributin f Fatty Acids Between the Amide f Ceramide Phsphrylglycerl Phsphate and the Esters f Cardilipin in Bacterides melaningenicus a Fatty acid Amide f CPGP Ester f C1 12: :0, Br :0, Br : :0, Br : :0, Br t6: :0, Br :0, Br :0, Br : :0, Br 20: : afatty acid methyl esters determined frm the areas f respnse after GLC n ethylene glycl succinate clumns. The data are given as the percentage f the ttal fatty acids recvered frm the amide r the ester linkage. FG. 3. Radiautgram f the unknwn ceramide derivative after mild alkaline methanlysis which remves the CL. See Figure 2. and the lipids recvered. The tp band cntained lipids with the chrmatgraphic mbility in ther slvent systems (7) f cardilipin (CL), phsphatidic acid (PA), and the trace ceramide derivative (Rf value 0.71). The middle band cntained lipids with the chrmatgraphic mbility in ther systems f phsphatidylglycerl (PG), CPG and phsphatidyl ethanlamine (PE) (Rf value 0.52) and the lwer band cntained CPE and phsphatidylserine (PS) (Rf value 0.43). The lipids frm the tp band were recvered frm the silica gel impregnated paper and sptted n sheets f this paper again. Twdimensinal chrmatgraphy separated the CL and ceramide derivative frm the phsphatidic acid (Fig. 2). The CL plus ceramide derivative were recvered and accunted fr 99% f the 32p frm the tp band. Mild alkaline methanlysis was perfrmed at 0 C fr 2 hr and the KOH neutralized with Birex 70 (a weakly acidic catin exchange resin (7). The water sluble glycerl phsphate ester derived frm the diacyl lipid was then separated frm the fatty acid methyl esters and the ceramide derivative using a sequence f three extractins with diethyl ether and a final extractin with chlrfrm t minimize emulsin frmatin (1). The mild alkaline methanlysis is cmplete in 2 hr (1). Lipid phsphate was analyzed after digestin f the samples in perchlric acid (4); 0.16 gmles f radiactive phsphate were recvered as a water sluble ester which c-chrmatgraphed with unlabeled authentic diglycerl phsphrylglycerl (GPGPG) in tw dimensins n amincellulse paper (7). The remainder f the 32p (0.20 ~mles lipid phsphate) was recvered in the rganic slvent after the mild alkaline methanlysis. The rganic phase frm the mild alkaline methanlysis cntained fatty acid methyl esters derived frm the CL. The fatty acid esters were separated frm the ceramide derivative by silicic acid chrmatgraphy. The fatty acid esters were then analyzed by gas liquid chrmatgraphy (GLC). The ceramide derivative recvered frm the silicic acid clumn was chrmatgraphed in tw dimensins n silica gel-laded paper (Fig. 3). The ceramide derivative had identical chrmatgraphic mbility befre and after mild alkaline methanlysis (Fig. 2 and 3). This suggests the ceramide derivative cntains n ester linked fatty acids. N fatty acyl esters were detected in ceramide phsphrylethanlamine (CPE) in this rganism (1). The ceramide derivative did nt react with peridate (4) befre r after mild alkaline hydrlysis. The ceramide derivative was hydrlyzed in methanlic 2 N HC1 cntaining water (9.5% v/v) at 100 C fr 2 hr (1,10). This prcedure quantitatively liberates the amide linked fatty LPDS, VOL. 5, NO. 1
4 CERAMDES FROM BACTERA 59 O-PE Methyl GP Pi egp k " PGP O-PS GPGP W "7 E W,_ 0.65' J~ 17 / l f ; b i ] A v to O B X ta tm r c.) ) ib TUBE NUMBER ) 8b FG. 4. Clumn chrmatgraphy f the water sluble prducts f the mild acid hydrlysis f the ceramides f Bacterides melaningenicus grwn in the presence f 32p. Fractins f 2.65 ml were cllected, a prtin remved t assay the 32p and the remainder digested fr the phsphate determinatin. The elutin vlumes f authentic cmpunds are illustrated at the tp f the Figure. The recvery f 32p was quantitative. acid, the LCB and water sluble phsphate derivative (1). The fatty acids derived frm the amide f the LCB were separated frm the LCB by silicic acid chrmatgraphy f the rganic phase f the hydrlysis mixture. These fatty acids were methylated (8) and separated by GLC. A cmparisn f the prprtins f fatty acid cmpnents frm the amide f the LCB and the fatty acids in ester linkage t CL is given in Table. The fatty acids derived frm the amide cntain less 15:0, Br and mre f the lnger branched fatty acids than are fund in the ester linkage. The LCB fractin was recvered frm the silicic acid clumn and TMS derivatives prepared (1,11). TMS derivatives f the LCB had retentin times crrespnding t 16:0 (1.5%), 17:0,Br (39%), 18:0 (18%), 20:0, BR (4%), 20:0 (20%) and 21:0 (15%). The ttal detectr respnse crrespnded t 0.10 #mles f TMS-dihydrsphingsine. This indicates that the mlar rati f LCB t phsphate in the ceramide was 1.00 t The ttal respnse f the amide-linked fatty acid crrespnded t 0.09 #mles f methyl palmitate fr an amide fatty acid t phsphate mlar rati f 0.92 t dentificatin f the Water Sluble Prduct f Acid Hydrlysis T cllect a large amunt f the water sluble hydrlysis prduct f the unknwn ceramide derivative fr identificatin, the ttal lipid was deacylated by mild alkaline methanlysis and the fatty acids separated frm the ceramide derivatives n a silicic acid clumn. The ceramide derivatives were hydrlyzed in 1 ml methanlic 2 N HC1 cntaining 6.5 M water fr 1 hr at 100 C. After cling, 1 ml f water was added and the mixture extracted with tw 2 ml prtins f petrleum ether. The aqueus phase was then made t ph 10 with KOH and the petrleum ether extractin repeated twice. The aqueus phase was desalted by passing thrugh a 5 X 300 mm clumn f Dwex 50-8X, mesh, in the acid frm and the 32p recvered quantitatively. The HC1 was remved in a stream f nitrgen. The 32p labeled hydrlysis prducts were cmbined wit h au t hen tic -phsphrylethanlamine (-pe), L-a-glycerl phsphate (agp), inrganic phsphate (Pi), glycerl diphsphate (PGP) and -phsphrylserine (-ps) in 20 mm sdium brate ph 9.5 and laded n a Dwex-1 clumn. The esters were then eluted frm the clumn with an ammnium frmate-sdium brate gradient (4). Esters cntaining 32p were detected at the elutin vlumes f -pe (43.3% f the 32p), methyl-gp (4.5%), agp (43.6%) and GPGP r PGP (8.5%). This is illustrated in Figure 4. The fractins crrespnding t PGP r GPGP were cmbined and diluted t eight times their vlume with distilled water. The sample was then pumped nt a 0.4 X 15 cm clumn f Dwex-1-8X ( )mesh in the LPDS, VOL. 5, NO. 1
5 60 DAVD C. WHTE AND ANNE N. TUCKER (5). n this system the Rf values were glycerl, 0.80; glycerl phsphrylglycerl (GPG), 0.64; GPGP, 0.18; Pi, 0.15; and PGP, A radiautgram f the 32P-cntaining ester and its hydrlysis prduct tgether with a chrmatgram f authentic standards is illustrated in Figure 5. The 32p-cntaining ester had the chrmatgraphic mbility f PGP. Only 32p i culd be detected after alkaline phsphatase treatment. As a further identificatin the ester crrespnding t the 32p spt in Figure 5 was eluted frm the paper with water, mixed with authentic Pi, GPGP and PGP and applied t a Dwex-1 8X ( mesh) clumn. The esters were eluted with 0.3 M ammnium frmate ph 9.5 as illustrated in Figure 6. The 32p cntaining ester is clearly nt GPGP. RESULTS FG. 5. Radiautgram f the separatin f the water sluble glycerl phsphate esters derived frm the trace ceramide f BacterMes melaningenicus grwn in the presence f 32p. The PGP fractin frm the clumn illustrated in Figure 4 as desalted and chrmatgraphed befre and after treatment with alkaline phsphatase as described in Materials and Methds. frmate frm. The clumn was washed with 3 clumn vl f 10 mm frmic acid t remve the brate. The glycerl phsphate ester was then eluted with 0.3 M ammnium carbnate ph 8.0. The 32p was quantitatively recvered. The ammnium carbnate was remved frm the fractin cntaining the 32p by biling t dryness in a stream f nitrgen. A prtin f the 32p cntaining ester was disslved in 25 ~1 f 20 mm ammnium acetate ph 8.0. This was treated with 25 btl f alkaline phsphatase (1 mg/ml) frdm Escherichia cli (Wrthingtn) fr 3 hr at 25 C (5). The prducts f enzymatic hydrlysis and unhydrlyzed ester were applied t paper and subjected t ascending chrmatgraphy n acid washed paper with the mdified Wawszkiewicz slvent Separatin f the Unknwn Ceramide Derivative The lipid islated by the prcedure illustrated in Figure 1 was separated frm CL. This is cnfirmed by the different prprtins f fatty acids frm the ceramide derivative and CL (Table ). Chrmatgraphy f the water sluble prtin frm the mild alkaline methanlysis perfrmed n amincellulse paper (7) indicated that there was n ceramide derivative in the GPGPG. The radiautgrams illustrated in Figures 2 and 3 indicate that n CPE r CPG cntaminate the unknwn ceramide derivative. After mild alkaline methanlysis fr 2 hr at 0 C the unknwn ceramide derivative migrates as a single cmpnent in tw dimensinal paper chrmatgraphy (Fig. 3). Authentic CL is cmpletely deacylated in 1.5 hr at 0 C and the phsphate can be quantitatively recvered in the aqueus phase (4,7). Separatin f the Ceramide Derivatives A secnd purificatin prcedure was used t cnfirm the results derived frm the lipid islated as in Figure 1. The ttal lipid extract frm B. melaningenicus grwn with H332PO 4 was subjected t mild alkaline methanlysis, the ceramide derivatives and fatty acid methyl esters frm the diacyl,lipids were recvered in the rganic phase. The fatty acid methyl esters and ceramide derivatives were separated with a silicic acid clumn. The ceramide derivatives were then separated by chrmatgraphy n silica gel-laded paper. The ceramide derivatives in the lipid sample accunted fr 48% f the lipid phsphate. A radiautgram f the separated ceramide derivatives is illustrated in Figure 7. The tw majr ceramide derivatives crrespnd t CPE and CPG which have been identified previusly (1). The distributin f LPDS, VOL. 5, NO. 1
6 CERAMDES FROM BACTERA 61 GPG PiaGP GPGPG GPGP PGP "400 hl bj k- "- O a. O3 W d :L TUBE NUMBER /- r300 bj rn / \\ D A 1 F-,'/,A'~ x ~ a_ ~ :~ FG. 6. Chrmatgraphy f the PGP islated frm the trace ceramide f Bacterides melaningenicus grwn with 32p. PGP was eluted frm the paper chrmatgram used fr Figure 5 and chrmatgraphed n Dwex-1 as described in Materials and Methds. See Figure 4. Each fractin cntained 5.0 ml. The recvery f the 32p was quantitative. The elutin vlumes f authentic glycerl phsphate esters are given at the tp f the Figure. 32p in the three ceramide derivatives was CPE, 45%, CPG, 51% and unknwn 4%. The unknwn ceramide derivative has the same chrmatgraphic mbility when recvered and the chrmatgraphy repeated as that illustrated in Figure 3. Water Sluble Prduct f Acid-Hydrlysis f the Unknwn Ceramide Derivative The 32P-cntaining derivative btained after hydrlysis f the unknwn ceramide derivative cchrmatgraphed with PGP in the paper chrmatgraphic system illustrated in Figure 4 and the clumn chrmatgraphic system illustrated in Figure 5. This was true with the unknwn ceramide separated frm ther lipids chrmatgraphically and then frm CL by mild alkaline methanlysis as in Figure 1, frm the unknwn ceramide derivative separated frm the ther ceramide derivatives after mild alkaline methanlysis f the ttal lipid extract as in Figure 7, r frm the hydrlysis prduct f the ceramide derivative mixture separated as in Figure 4. The elutin frm a Dwex-1 clumn f the 32p-glycerl ester recvered frm the hydrlysis f the ceramide derivative is nt exactly cincident with authentic PGP (Fig. 6). Perhaps there are tw glycerl diphsphate esters in the lipid r ne is an artifact f the hydrlysis. The clumn des indicate that the ester is nt GPGP. The absence f reactivity with peridate befre r after mild alkaline methanlysis (Fig. 2, 3 and 7), the chrmatgraphic mbility n paper (Fig. 5) and clumns (Fig. 4,6) and the release f 32p i and nly 32p i by alkaline phsphatase indicate that PGP is the ester liberated after acid hydrlysis f the minr cmpnent f the ceramide derivatives. FG. 7. Radiautgram f the chrmatgraphic separatin f the ceramides f Bacterides melaningenicus grwn in the presence f 32p as in Figure 2. The paper was then dipped in peridate slutin fllwed by -tluidine (4). A secnd paper was dipped in ninhydrin reagent (4). LPDS, VOL 5, NO. 1
7 62 DAVD C. WHTE AND ANNE N. TUCKER DSCUSSON The ceramide derivative described in this study cntains tw phsphates, an amide-linked fatty acid and ne dihydrsphingsine hmlgue per mlecule. The phsphate is prbably linked t the 1 psitin f the LCB as in the ther lipids in this rganism (1). This ceramide derivative cannt be separated frm cardilipin by chrmatgraphy in tw dimensins and its chrmatgraphic mbility n silica gel-laded paper is nt affected by deacylatin. N vicinyl hydrxyl grups can be detected befre r after deacylatin f the ceramide by mild alkaline methanlysis. After mild acid methanlysis PGP was recvered in the aqueus phase. The PGP was identified chrmatgraphically. All the 32p in 32PG32p was liberated as inrganic 32p after treatment with alkaline phsphatase. t wuld appear that the structure f this ceramide derivative is ceramide--phsphryll'-sn-glycerl-3'-phsphate. T ur knwledge this lipid has nt been described previusly. The ceramide derivative described in this study is hmlgus with phsphatidyl glycerl phsphate. A ceramide derivative hmlgus with phsphatidyl glycerl has als been detected in this rganism (1). The presence f these tw lipids suggests that the bisynthesis might als parallel the synthesis f phsphatidyl glycerl as described in E. cli (12). The CPG is present in abut 10 times the cncentratin f the CPGP in B. melaningenicus. ACKNOWLEDGMENT This research was supprted by Grant GM f The nstitute f General Medical Sciences, U.S. Public Health Service and Cntract (73)with the Agricultural Research Service, USDA administered by the E. Utiliz. Res. Dev. Div., Philadelphia, Penna. V. Rizza prvided the rganisms used in this study and Bernice Cke assisted in the experiments. REFERENCES 1. LaBach, J. P., and D. C. White, J. Lipid Res. 10:528 (1969). 2. Asselineau, J., in "The Bacterial Lipids," Hlden- Day, nc., Califrnia, 1966, p Rizza, V., P. R. Sinclair, D. C. White and P. R. Curant, J. Bacterii. 96:665 (1968). 4. White, D. C., and F. E. Frerman, bid. 94: Lester, R. L., and M. R. Steiner, J. Bil. Chem. 243:4889 (1968). 6. Wuthier, R. E., J. Lipid Res. 7:544 (1966). 7. White, D. C.,. Bacteril. 96:1159 (1968). 8. White, D. C., and R. H. Cx, bid. 93: Bligh, E. G., and W. J. Dyer, Can. J. Bichem. Physil. 37: Sweeley, C. C., and E. A. Mscatelli, J. Lipid Res. 1:40 (1959). 11. Carter, H. E., and R. C. Gaver, bid. 8: Chang, Y. Y., and E. P. Kennedy, bid. 8:447 [Received January 30, 1969] LPDS, VOL. 5) NO. 1
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