Phosphatidylcholine biosynthesis in Xanthomonas campestris via a yeast-like acylation pathway

Molecular Microbiology

Volumn 91, Issue 4, 2014, Pages 736-750

  Moser, Roman ^a   Aktas, Meriyem ^a   Narberhaus, Franz ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCEROPHOSPHORYLCHOLINE; PHOSPHATIDYLCHOLINE;

ACYLATION; METABOLISM; XANTHOMONAS CAMPESTRIS;

ACYLATION; GLYCERYLPHOSPHORYLCHOLINE; METABOLIC NETWORKS AND PATHWAYS; PHOSPHATIDYLCHOLINES; XANTHOMONAS CAMPESTRIS;

EID: 84893727695     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12492     Document Type: Article

References (73)

1. Aktas, M., and Narberhaus, F. (2009) In vitro characterization of the enzyme properties of the phospholipid N-methyltransferase PmtA from Agrobacterium tumefaciens. J Bacteriol 191: 2033-2041.
2. Aktas, M., Wessel, M., Hacker, S., Klüsener, S., Gleichenhagen, J., and Narberhaus, F. (2010) Phosphatidylcholine biosynthesis and its significance in bacteria interacting with eukaryotic cells. Eur J Cell Biol 89: 888-894.
3. Aktas, M., Jost, K.A., Fritz, C., and Narberhaus, F. (2011) Choline uptake in Agrobacterium tumefaciens by the high-affinity ChoXWV transporter. J Bacteriol 193: 5119-5129.
4. Ames, G.F. (1968) Lipids of Salmonella typhimurium and Escherichia coli: structure and metabolism. J Bacteriol 95: 833-843.
5. Avelange-Macherel, M.H., Ly-Vu, B., Delaunay, J., Richomme, P., and Leprince, O. (2006) NMR metabolite profiling analysis reveals changes in phospholipid metabolism associated with the re-establishment of desiccation tolerance upon osmotic stress in germinated radicles of cucumber. Plant Cell Environ 29: 471-482.
6. Bay, D.C., and Turner, R.J. (2013) Membrane composition influences the topology bias of bacterial integral membrane proteins. Biochim Biophys Acta 1828: 260-270.
7. Benghezal, M., Roubaty, C., Veepuri, V., Knudsen, J., and Conzelmann, A. (2007) SLC1 and SLC4 encode partially redundant acyl-coenzyme A 1-acylglycerol-3-phosphate O-acyltransferases of budding yeast. J Biol Chem 282: 30845-30855.
8. Bligh, E.G., and Dyer, W.J. (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917.
9. Boncompagni, E., Osteras, M., Poggi, M.C., and le Rudulier, D. (1999) Occurrence of choline and glycine betaine uptake and metabolism in the family rhizobiaceae and their roles in osmoprotection. Appl Environ Microbiol 65: 2072-2077.
10. Büttner, D., and Bonas, U. (2010) Regulation and secretion of Xanthomonas virulence factors. FEMS Microbiol Rev 34: 107-133.
11. Campbell, J.W., and Cronan, J.E., Jr (2001) Bacterial fatty acid biosynthesis: targets for antibacterial drug discovery. Annu Rev Microbiol 55: 305-332.
12. Carman, G.M., and Han, G.S. (2009) Regulation of phospholipid synthesis in yeast. J Lipid Res 50 (Suppl.): S69-S73.
13. Carman, G.M., and Han, G.S. (2011) Regulation of phospholipid synthesis in the yeast Saccharomyces cerevisiae. Annu Rev Biochem 80: 859-883.
14. Conde-Alvarez, R., Grilló, M.J., Salcedo, S.P., de Miguel, M.J., Fugier, E., Gorvel, J.P., etal. (2006) Synthesis of phosphatidylcholine, a typical eukaryotic phospholipid, is necessary for full virulence of the intracellular bacterial parasite Brucella abortus. Cell Microbiol 8: 1322-1335.
15. Conover, G.M., Martínez-Morales, F., Heidtman, M.I., Luo, Z.Q., Tang, M., Chen, C., etal. (2008) Phosphatidylcholine synthesis is required for optimal function of Legionella pneumophila virulence determinants. Cell Microbiol 10: 514-528.
16. Cronan, J.E. (2003) Bacterial membrane lipids: where do we stand? Annu Rev Microbiol 57: 203-224.
17. Cronan, J.E., Jr (1974) Regulation of the fatty acid composition of the membrane phospholipids of Escherichia coli. Proc Natl Acad Sci USA 71: 3758-3762.
18. Daniels, M.J., Barber, C.E., Turner, P.C., Sawczyc, M.K., Byrde, R.J., and Fielding, A.H. (1984) Cloning of genes involved in pathogenicity of Xanthomonas campestris pv. campestris using the broad host range cosmid pLAFR1. EMBO J 3: 3323-3328.
19. Das, P.K., Basu, M., and Chatterjee, G.C. (1979) Lipid profile of the strains of Agrobacterium tumefaciens in relation to agrocin resistance. J Gen Appl Microbiol 25: 1-9.
20. Davidson, A.L., Dassa, E., Orelle, C., and Chen, J. (2008) Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72: 317-364, table of contents.
21. Dowhan, W., Mileykovskaya, E., and Bogdanov, M. (2004) Diversity and versatility of lipid-protein interactions revealed by molecular genetic approaches. Biochim Biophys Acta 1666: 19-39.
22. Estrada, P., Acebal, C., Bauluz, C., Casals, C., and Arche, R. (1984) Influence of temperature on stability and activity of lysolecithin acyltransferase and acyl-CoA hydrolase from rabbit lung. Biochem Int 8: 339-346.
23. Falcone, D.L., Ogas, J.P., and Somerville, C.R. (2004) Regulation of membrane fatty acid composition by temperature in mutants of Arabidopsis with alterations in membrane lipid composition. BMC Plant Biol 4: 17.
24. Fu, J.F., and Tseng, Y.H. (1990) Construction of lactose-utilizing Xanthomonas campestris and production of xanthan gum from whey. Appl Environ Microbiol 56: 919-923.
25. Gallazzini, M., and Burg, M.B. (2009) What's new about osmotic regulation of glycerophosphocholine. Physiology (Bethesda) 24: 245-249.
26. Gallazzini, M., Ferraris, J.D., and Burg, M.B. (2008) GDPD5 is a glycerophosphocholine phosphodiesterase that osmotically regulates the osmoprotective organic osmolyte GPC. Proc Natl Acad Sci USA 105: 11026-11031.
27. Geiger, O., González-Silva, N., López-Lara, I.M., and Sohlenkamp, C. (2010) Amino acid-containing membrane lipids in bacteria. Prog Lipid Res 49: 46-60.
28. Geiger, O., López-Lara, I.M., and Sohlenkamp, C. (2013) Phosphatidylcholine biosynthesis and function in bacteria. Biochim Biophys Acta 1831: 503-513.
29. Gibellini, F., and Smith, T.K. (2010) The Kennedy pathway - de novo synthesis of phosphatidylethanolamine and phosphatidylcholine. IUBMB Life 62: 414-428.
30. Gold, V.A., Robson, A., Bao, H., Romantsov, T., Duong, F., and Collinson, I. (2010) The action of cardiolipin on the bacterial translocon. Proc Natl Acad Sci USA 107: 10044-10049.
31. Hacker, S., Gödeke, J., Lindemann, A., Mesa, S., Pessi, G., and Narberhaus, F. (2008a) Global consequences of phosphatidylcholine reduction in Bradyrhizobium japonicum. Mol Genet Genomics 280: 59-72.
32. Hacker, S., Sohlenkamp, C., Aktas, M., Geiger, O., and Narberhaus, F. (2008b) Multiple phospholipid N-methyltransferases with distinct substrate specificities are encoded in Bradyrhizobium japonicum. J Bacteriol 190: 571-580.
33. den Kamp, J.A., Redai, I., and van Deenen, L.L. (1969) Phospholipid composition of Bacillus subtilis. J Bacteriol 99: 298-303.
34. Kaneshiro, T., and Law, J.H. (1964) Phosphatidylcholine synthesis in Agrobacterium tumefaciens. I. Purification and properties of a phosphatidylethanolamine N-methyltransferase. J Biol Chem 239: 1705-1713.
35. Kent, C., Gee, P., Lee, S.Y., Bian, X., and Fenno, J.C. (2004) A CDP-choline pathway for phosphatidylcholine biosynthesis in Treponema denticola. Mol Microbiol 51: 471-481.
36. Klüsener, S., Aktas, M., Thormann, K.M., Wessel, M., and Narberhaus, F. (2009) Expression and physiological relevance of Agrobacterium tumefaciens phosphatidylcholine biosynthesis genes. J Bacteriol 191: 365-374.
37. Klüsener, S., Hacker, S., Tsai, Y.L., Bandow, J.E., Gust, R., Lai, E.M., and Narberhaus, F. (2010) Proteomic and transcriptomic characterization of a virulence-deficient phosphatidylcholine-negative Agrobacterium tumefaciens mutant. Mol Genet Genomics 283: 575-589.
38. Kozloff, L.M., Turner, M.A., Arellano, F., and Lute, M. (1991) Phosphatidylinositol, a phospholipid of ice-nucleating bacteria. J Bacteriol 173: 2053-2060.
39. Könneke, M., and Widdel, F. (2003) Effect of growth temperature on cellular fatty acids in sulphate-reducing bacteria. Environ Microbiol 5: 1064-1070.
40. Kumari, S., Beatty, C.M., Browning, D.F., Busby, S.J., Simel, E.J., Hovel-Miner, G., and Wolfe, A.J. (2000) Regulation of acetyl coenzyme A synthetase in Escherichia coli. J Bacteriol 182: 4173-4179.
41. Li, Z., and Vance, D.E. (2008) Phosphatidylcholine and choline homeostasis. J Lipid Res 49: 1187-1194.
42. Malek, A.A., Wargo, M.J., and Hogan, D.A. (2012) Absence of membrane phosphatidylcholine does not affect virulence and stress tolerance phenotypes in the opportunistic pathogen Pseudomonas aeruginosa. PLoS ONE 7: e30829.
43. Medeot, D.B., Bueno, M.A., Dardanelli, M.S., and de Lema, M.G. (2007) Adaptational changes in lipids of Bradyrhizobium SEMIA 6144 nodulating peanut as a response to growth temperature and salinity. Curr Microbiol 54: 31-35.
44. Minder, A.C., de Rudder, K.E., Narberhaus, F., Fischer, H.M., Hennecke, H., and Geiger, O. (2001) Phosphatidylcholine levels in Bradyrhizobium japonicum membranes are critical for an efficient symbiosis with the soybean host plant. Mol Microbiol 39: 1186-1198.
45. Oursel, D., Loutelier-Bourhis, C., Orange, N., Chevalier, S., Norris, V., and Lange, C.M. (2007) Lipid composition of membranes of Escherichia coli by liquid chromatography/tandem mass spectrometry using negative electrospray ionization. Rapid Commun Mass Spectrom 21: 1721-1728.
46. Rajagopal, L., Sundari, C.S., Balasubramanian, D., and Sonti, R.V. (1997) The bacterial pigment xanthomonadin offers protection against photodamage. FEBS Lett 415: 125-128.
47. Rand, J.B. (2007) Acetylcholine. WormBook 1-21.
48. van der Rest, B., Boisson, A.M., Gout, E., Bligny, R., and Douce, R. (2002) Glycerophosphocholine metabolism in higher plant cells. Evidence of a new glyceryl-phosphodiester phosphodiesterase. Plant Physiol 130: 244-255.
49. Röttig, A., and Steinbüchel, A. (2013) Acyltransferases in bacteria. Microbiol Mol Biol Rev 77: 277-321.
50. de Rudder, K.E., Sohlenkamp, C., and Geiger, O. (1999) Plant-exuded choline is used for rhizobial membrane lipid biosynthesis by phosphatidylcholine synthase. J Biol Chem 274: 20011-20016.
51. Schäfer, A., Tauch, A., Jager, W., Kalinowski, J., Thierbach, G., and Pühler, A. (1994) Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145: 69-73.
52. Schmidl, S.R., Otto, A., Lluch-Senar, M., Pinol, J., Busse, J., Becher, D., and Stülke, J. (2011) A trigger enzyme in Mycoplasma pneumoniae: impact of the glycerophosphodiesterase GlpQ on virulence and gene expression. PLoS Pathog 7: e1002263.
53. Sherr, S.I., and Law, J.H. (1965) Phosphatidylcholine synthesis in Agrobacterium tumefaciens. II. Uptake and utilization of choline. J Biol Chem 240: 3760-3765.
54. 31P NMR spectroscopy shows an increase in glycerophosphorylcholine concentration without alterations in mitochondrial function in the prefrontal cortex of medicated schizophrenic patients at rest. Eur J Neurosci 20: 749-756.
55. Sohlenkamp, C., de Rudder, K.E., Rohrs, V., López-Lara, I.M., and Geiger, O. (2000) Cloning and characterization of the gene for phosphatidylcholine synthase. J Biol Chem 275: 18919-18925.
56. Sohlenkamp, C., López-Lara, I.M., and Geiger, O. (2003) Biosynthesis of phosphatidylcholine in bacteria. Prog Lipid Res 42: 115-162.
57. Starr, M.P., and Stephens, W.L. (1964) Pigmentation and taxonomy of the genus Xanthomonas. J Bacteriol 87: 293-302.
58. Starr, M.P., Jenkins, C.L., Bussey, L.B., and Andrewes, A.G. (1977) Chemotaxonomic significance of the xanthomonadins, novel brominated aryl-polyene pigments produced by bacteria of the genus Xanthomonas. Arch Microbiol 113: 1-9.
59. Ståhl, U., Stålberg, K., Stymne, S., and Ronne, H. (2008) A family of eukaryotic lysophospholipid acyltransferases with broad specificity. FEBS Lett 582: 305-309.
60. Stålberg, K., Neal, A.C., Ronne, H., and Ståhl, U. (2008) Identification of a novel GPCAT activity and a new pathway for phosphatidylcholine biosynthesis in S.cerevisiae. J Lipid Res 49: 1794-1806.
61. Taneja, R., Malik, U., and Khuller, G.K. (1979) Effect of growth temperature on the lipid composition of Mycobacterium smegmatis ATCC 607. J Gen Microbiol 113: 413-416.
62. Vorholt, J.A. (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10: 828-840.
63. Walter, A., Korth, U., Hilgert, M., Hartmann, J., Weichel, O., Fassbender, K., etal. (2004) Glycerophosphocholine is elevated in cerebrospinal fluid of Alzheimer patients. Neurobiol Aging 25: 1299-1303.
64. Wengelnik, K., Marie, C., Russel, M., and Bonas, U. (1996) Expression and localization of HrpA1, a protein of Xanthomonas campestris pv. vesicatoria essential for pathogenicity and induction of the hypersensitive reaction. J Bacteriol 178: 1061-1069.
65. Wessel, M., Klüsener, S., Gödeke, J., Fritz, C., Hacker, S., and Narberhaus, F. (2006) Virulence of Agrobacterium tumefaciens requires phosphatidylcholine in the bacterial membrane. Mol Microbiol 62: 906-915.
66. Wilderman, P.J., Vasil, A.I., Martin, W.E., Murphy, R.C., and Vasil, M.L. (2002) Pseudomonas aeruginosa synthesizes phosphatidylcholine by use of the phosphatidylcholine synthase pathway. J Bacteriol 184: 4792-4799.
67. Xiong, M., Long, D., He, H., Li, Y., and Wang, X. (2013) Phosphatidylcholine synthesis is essential for HrpZ harpin secretion in plant pathogenic Pseudomonas syringae and non-pathogenic Pseudomonas sp. 593. Microbiol Res. pii: S0944-5013(13)00095-5. doi:0.1016/j.micres.2013.06.009
68. Yang, T.C., Leu, Y.W., Chang-Chien, H.C., and Hu, R.M. (2009) Flagellar biogenesis of Xanthomonas campestris requires the alternative sigma factors RpoN2 and FliA and is temporally regulated by FlhA, FlhB, and FlgM. J Bacteriol 191: 2266-2275.
69. Yano, Y., Nakayama, A., Ishihara, K., and Saito, H. (1998) Adaptive changes in membrane lipids of barophilic bacteria in response to changes in growth pressure. Appl Environ Microbiol 64: 479-485.
70. Zablocki, K., Miller, S.P., Garcia-Perez, A., and Burg, M.B. (1991) Accumulation of glycerophosphocholine (GPC) by renal cells: osmotic regulation of GPC:choline phosphodiesterase. Proc Natl Acad Sci USA 88: 7820-7824.
71. Zaccheo, O., Dinsdale, D., Meacock, P.A., and Glynn, P. (2004) Neuropathy target esterase and its yeast homologue degrade phosphatidylcholine to glycerophosphocholine in living cells. J Biol Chem 279: 24024-24033.
72. Zhang, Y.M., and Rock, C.O. (2008) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6: 222-233.
73. Zheng, Z., and Zou, J. (2001) The initial step of the glycerolipid pathway: identification of glycerol 3-phosphate/dihydroxyacetone phosphate dual substrate acyltransferases in Saccharomyces cerevisiae. J Biol Chem 276: 41710-41716.