Advertisement

Characterization of ornithine and glutamine lipids extracted from cell membranes of Rhodobacter sphaeroides

  • Xi Zhang
  • Shelagh M. Ferguson-Miller
  • Gavin E. ReidEmail author
Articles

Abstract

The identification and structural characterization of a series of ornithine lipids extracted from the cell membranes of wild-type Rhodobacter sphaeroides, as well as from a glycerophosphocholine-deficient strain, have been achieved by multistage tandem mass spectrometry of their protonated and deprotonated precursor ions in a linear quadrupole ion trap. Systematic examination of the multistage gas-phase fragmentation reactions of these ions, combined with the use of hydrogen/deuterium exchange, has enabled the pathways responsible for sequential losses of the 3-hydroxy linked fatty acyl chain and the amide linked 3-OH fatty acyl chain from these lipids, as well as for formation of the previously reported ornithine specific positively charged “fingerprint” ion at m/z 115, to be determined. Additionally, the fragmentation pathways responsible for formation of a previously unreported ornithine lipid head group-specific product ion at m/z 131 in negative ion mode have been examined. Based on these results, and by comparison with the fragmentation behavior of model lipoamino acid standard compounds, a series of novel glutamine containing lipids have also been identified, with analogous structures but with masses 14 Da higher than those of several of the ornithine lipids observed in this study. Characteristic “fingerprint” ions indicative of these glutamine lipids were found at m/z 147, 130, and 129 in positive ion mode and at m/z 145 and 127 in negative ion mode. The results from this study establish an experimental basis for future efforts aimed at the sensitive identification, characterization, and quantitative analysis of ornithine and glutamine lipids in complex unfractionated cellular extracts.

Keywords

Ornithine Collision Induce Dissociation Rhodobacter Sphaeroides Fatty Acyl Chain LIPIDOME Analysis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Gorchein, A. Distribution and Metabolism of Ornithine in Rhodopseudomonas sphaeroides. Proc. Roy. Soc. Ser. B 1968, 170, 265–278.CrossRefGoogle Scholar
  2. 2.
    Shively, J. M.; Knoche, H. W. Isolation of an Ornithine-Containing Lipid from Thiobacillus thiooxidans. J. Bacteriol 1969, 98, 829–830.Google Scholar
  3. 3.
    Knoche, H. W.; Shively, J. M. The Structure of an Ornithine-Containing Lipid from Thiobacillus thiooxidans. J. Biol. Chem 1972, 247, 170–178.Google Scholar
  4. 4.
    Lopez-Lara, I. M.; Sohlenkamp, C.; Geiger, O. Membrane Lipids in Plant-Associated Bacteria: Their Biosyntheses and Possible Functions. Mol. Plant-Microbe Interact 2003, 16, 567–579.CrossRefGoogle Scholar
  5. 5.
    Minnikin, D. E.; Abdolrahimzadeh, H. Replacement of Phosphatidylethanolamine and Acidic Phospholipids by an Ornithine-Amide Lipid and a Minor Phosphorus-Free Lipid in Pseudomonas fluorescens NCMB 129. FEBS (Fed. Eur. Biochem. Soc.) Lett 1974, 43, 257–260.CrossRefGoogle Scholar
  6. 6.
    Benning, C.; Huang, Z.-H.; Gage, D. A. Accumulation of a Novel Glycolipid and a Betaine Lipid in Cells of Rhodobacter sphaeroides grown under phosphate limitation. Arch. Biochem. Biophys 1995, 317, 103–111.CrossRefGoogle Scholar
  7. 7.
    Lopez-Lara, I. M.; Gao, J.-L.; Soto, M. J.; Solares-Perez, A.; Weissenmayer, B.; Sohlenkamp, C.; Verroios, G. P.; Thomas-Oates, J.; Geiger, O. Phosphorus-Free Membrane Lipids of Sinorhizobium meliloti Are Not Required for the Symbiosis with Alfalfa but Contribute to Increased Cell Yields Under Phosphorus-Limiting Conditions of Growth. Mol. Plant-Microbe Interact 2005, 18, 973–982.CrossRefGoogle Scholar
  8. 8.
    Weissenmayer, B.; Gao, J.-L.; Lopez-Lara, I. M.; Geiger, O. Identification of a Gene Required for the Biosynthesis of Ornithine-Derived Lipids. Mol. Microbiol 2002, 45, 721–733.CrossRefGoogle Scholar
  9. 9.
    Taylor, C. J.; Anderson, A. J.; Wilkinson, S. G. Phenotypic Variation of Lipid Composition in Burkholderia cepacia: A Response to Increased Growth Temperature is a Greater Content of 2-Hydroxy Acids in Phosphatidylethanolamine and Ornithine Amide Lipid. Microbiology (Reading, U.K.) 1998, 144, 1737–1745.CrossRefGoogle Scholar
  10. 10.
    Rojas-Jimenez, K.; Sohlenkamp, C.; Geiger, O.; Martinez-Romero, E.; Werner, D.; Vinuesa, P. A CIC chloride Channel Homolog and Ornithine-Containing Membrane Lipids of Rhizobium tropici CIAT899 are Involved in Symbiotic Efficiency and Acid Tolerance. Mol. Plant-Microbe Interact 2005, 18, 1175–1185.CrossRefGoogle Scholar
  11. 11.
    Kawai, Y.; Yano, I. Ornithine-Containing Lipid of Bordetella pertussis, a new type of hemagglutinin. Eur. J. Biochem 1983, 136, 531–538.CrossRefGoogle Scholar
  12. 12.
    Kawai, Y.; Akagawa, K. Macrophage Activation of an Ornithine-Containing Lipid or a Serine-Containing Lipid. Infect. Immun 1989, 57, 2086–2091.Google Scholar
  13. 13.
    Kawai, Y.; Nakagawa, Y.; Matuyama, T.; Akagawa, K.; Itagawa, K.; Fukase, K.; Kusumoto, S.; Nishijima, M.; Yano, I. A Typical Bacterial Ornithine-Containing Lipid N & ;α-(D)-[3-(Hexadecanoyloxy)Hexadecanoyl]-Ornithine is a Strong Stimulant for Macrophages and a Useful Adjuvant. FEMS Immunol. Med. Microbiol 1999, 23, 67–73.Google Scholar
  14. 14.
    Aygun-Sunar, S.; Mandaci, S.; Koch, H.-G.; Murray, I. V. J.; Goldfine, H.; Daldal, F. Ornithine Lipid is Required for Optimal Steady-State Amounts of c-Type cytochromes in Rhodobacter capsulatus. Mol. Microbiol 2006, 61, 418–435.CrossRefGoogle Scholar
  15. 15.
    Tamot, B.; Zhang, X.; Hiser, C.; Reid, G. E.; Ferguson-Miller, S. M.; Benning, C. Cytochrome c Oxidase Produced in a Cardiolipin-Deficient Mutant of Rhodobacter sphaeroides is Fully Functional and Crystallizable. 2008, unpublished.Google Scholar
  16. 16.
    Benning, C.; Beatty, J. T.; Prince, R. C.; Somerville, C. R. The Sulfolipid Sulfoquinovosyldiacylglycerol is Not Required for Photosynthetic Electron Transport in Rhodobacter sphaeroides but enhances growth under phosphate limitation. Proc. Natl. Acad. Sci. U.S.A. 1993, 90, 1561–1565.CrossRefGoogle Scholar
  17. 17.
    Arondel, V.; Benning, C.; Somerville, C. R. Isolation and Functional Expression in Escherichia coli of a gene encoding phosphatidylethanolamine methyltransferase (EC 2.1.1.17) from Rhodobacter sphaeroides. J. Biol. Chem. 1993, 268, 16002–16008.Google Scholar
  18. 18.
    Yasutaka, T.; Yuzi, Y.; Keiji, K. A New Lysine-Containing Lipid Isolated from Agrobacterium tumefaciens. Agric. Biol. Chem 1976, 40, 1449–1450.CrossRefGoogle Scholar
  19. 19.
    Kawai, Y.; Ishida Okawara, A.; Okuyama, H.; Kura, F.; Suzuki, K. Modulation of Chemotaxis, O2 Production and Myeloperoxidase Release from Human Polymorphonuclear Leukocytes by the Ornithine-Containing Lipid and the Serine-Glycine-Containing Lipid of Flavobacterium. FEMS Immunol. Med. Microbiol 2000, 28, 205–209.Google Scholar
  20. 20.
    Pulfer, M.; Murphy, R. C. Electrospray Mass Spectrometry of Phospholipids. Mass Spectrom. Rev 2003, 22, 332–364.CrossRefGoogle Scholar
  21. 21.
    Zhang, X.; Reid, G. E. Multistage Tandem Mass Spectrometry of Anionic Phosphatidylcholine Lipid Adducts Reveals Novel Dissociation Pathways. Int. J. Mass Spectrom 2006, 252, 242–255.CrossRefGoogle Scholar
  22. 22.
    Linscheid, M.; Diehl, B. W. K.; Oevermoehle, M.; Riedl, I.; Heinz, E. Membrane Lipids of Rhodopseudomonas viridis. Biochim. Biophys. Acta, Lipid Metab 1997, 1347, 151–163.CrossRefGoogle Scholar
  23. 23.
    Hilker, D. R.; Gross, M. L.; Knocke, H. W.; Shively, J. M. The Interpretation of the Mass Spectrum of an Ornithine-Containing Lipid from Thiobacillus thiooxidans. Biomed. Mass Spectrom 1978, 5, 64–71.CrossRefGoogle Scholar
  24. 24.
    Tomer, K. B.; Crow, F. W.; Knoche, H. W.; Gross, M. L. Fast Atom Bombardment and Mass Spectrometry/Mass Spectrometry for Analysis of a Mixture of Ornithine-Containing Lipids from Thiobacillus thiooxidans. Anal. Chem 1983, 55, 1033–1036.CrossRefGoogle Scholar
  25. 25.
    Geiger, O.; Rohrs, V.; Weissenmayer, B.; Finan, T. M.; Thomas-Oates, J. E. The Regulator Gene phoB Mediates Phosphate Stress-Controlled Synthesis of the Membrane Lipid Diacylglyceryl-N,N,N-Trimethylhomoserine in Rhizobium (Sinorhizobium) meliloti. Mol. Microbiol 1999, 32, 63–73.CrossRefGoogle Scholar
  26. 26.
    Hilker, D. R.; Knoche, H. W.; Gross, M. L. Thermolysis Chemical Ionization of a Complex Polar Lipid. Biomed. Mass Spectrom 1979, 6, 356–358.CrossRefGoogle Scholar
  27. 27.
    Cerny, R. L.; Tomer, K. B.; Gross, M. L. Desorption Ionization Combined with Tandem Mass Spectrometry: Advantages for Investigating Complex Lipids, Disaccharides, and Organometallic complexes. Org. Mass Spectrom 1986, 21, 655–660.CrossRefGoogle Scholar
  28. 28.
    Reid, G. E.; Simpson, R. J.; O’Hair, R. A. J. A Mass Spectrometric and Ab Initio Study of the Pathways for Dehydration of Simple Glycine and Cysteine-Containing Peptide [M + H]+ ions. J. Am. Soc. Mass Spectrom 1998, 9, 945–956.CrossRefGoogle Scholar
  29. 29.
    Zhen, Y.; Qian, J.; Follmann, K.; Hayward, T.; Nilsson, T.; Dahn, M.; Hilmi, Y.; Hamer, A. G.; Hosler, J. P.; Ferguson-Miller, S. Overexpression and Purification of Cytochrome c oxidase from Rhodobacter sphaeroides. Protein Expr. Purif. 1998, 13, 326–336.CrossRefGoogle Scholar
  30. 30.
    Awasthi, Y. C.; Chuang, T. F.; Keenan, T. W.; Crane, F. L. Tightly Bound Cardiolipin in Cytochrome Oxidase. Biochim. Biophys. Acta Bioenerg 1971, 226, 42–52.CrossRefGoogle Scholar
  31. 31.
    Fahy, E.; Subramaniam, S.; Brown, H. A.; Glass, C. K.; Merrill, A. H. Jr.; Murphy, R. C.; Raetz, C. R. H.; Russell, D. W.; Seyama, Y.; Shaw, W.; Shimizu, T.; Spener, F.; van Meer, G.; Van Nieuwenhze, M. S.; White, S. H.; Witztum, J. L.; Dennis, E. A. A Comprehensive Classification System for Lipids. J. Lipid Res 2005, 46, 839–862.CrossRefGoogle Scholar
  32. 32.
    Bowie, J. H.; Brinkworth, C. S.; Dua, S. Collision-Induced Fragmentations of the (M − H) Parent Anions of Underivatized Peptides: An Aid to Structure Determination and Some Unusual Negative Ion Cleavages. Mass Spectrom. Rev 2002, 21, 87–107.CrossRefGoogle Scholar
  33. 33.
    Bowie, J. H. The Fragmentations of Even-Electron Organic Negative Ions. Mass Spectrom. Rev 1990, 9, 349–379.CrossRefGoogle Scholar
  34. 34.
    Eckersley, M.; Bowie, J. H.; Hayes, R. N. Collision-Induced Dissociations of Deprotonated & ;α-Amino Acids: The Occurrence of Specific Proton Transfers Preceding Fragmentation. Int. J. Mass Spectrom. Ion Processes 1989, 93, 199–213.CrossRefGoogle Scholar
  35. 35.
    Klug, R. M.; Benning, C. Two Enzymes of Diacylglyceryl-O-4′-(N,N,N-Trimethyl)-Homoserine Biosynthesis are Encoded by btaA and btaB in the purple bacterium. Rhodobacter sphaeroides. Proc. Natl. Acad. Sci. U.S.A 2001, 98, 5910–5915.CrossRefGoogle Scholar
  36. 36.
    O’Hair, R. A. J. The Role of Nucleophile-Electrophile Interactions in the Unimolecular and Bimolecular Gas-Phase Ion Chemistry of Peptides and Related Systems. J. Mass Spectrom 2000, 35, 1377–1381.CrossRefGoogle Scholar
  37. 37.
    Grogan, D. W.; Cronan, J. E. J. Cyclopropane Ring Formation in Membrane Lipids of Cacteria. Microbiol. Mol. Biol. Rev 1997, 61, 429–441.Google Scholar
  38. 38.
    Froelich, J. M.; Reid, G. E. The Origin and Control of Ex Vivo Oxidative Peptide Modifications Prior to Mass Spectrometry Analysis. Proteomics 2008, 8, 1334–1345.CrossRefGoogle Scholar

Copyright information

© American Society for Mass Spectrometry 2009

Authors and Affiliations

  • Xi Zhang
    • 1
    • 2
  • Shelagh M. Ferguson-Miller
    • 2
  • Gavin E. Reid
    • 1
    • 2
    Email author
  1. 1.Department of ChemistryMichigan State UniversityEast LansingUSA
  2. 2.Department of Biochemistry and Molecular BiologyMichigan State UniversityEast LansingUSA

Personalised recommendations