Biosynthesis of teichoic acids in Streptococcus pneumoniae and closely related species: Lessons from genomes

Microbial Drug Resistance

Volumn 18, Issue 3, 2012, Pages 344-358

  Denapaite, Dalia ^a   Brückner, Reinhold ^a   Hakenbeck, Regine ^a   Vollmer, Waldemar ^b  

^a University of Koblenz Landau   (Germany)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOTRANSFERASE; CHOLINE; CHOLINE KINASE; CHOLINE PHOSPHATE CYTIDYLYLTRANSFERASE; GLYCOSYLTRANSFERASE; LIPOTEICHOIC ACID; PHOSPHOTRANSFERASE; RIBULOSE PHOSPHATE; TEICHOIC ACID;

BACTERIAL CELL WALL; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM MUTANT; CARBOHYDRATE SYNTHESIS; CONTROLLED STUDY; CYTOPLASM; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVIEW; STREPTOCOCCUS MITIS; STREPTOCOCCUS ORALIS; STREPTOCOCCUS PNEUMONIAE;

BACTERIAL PROTEINS; BASE SEQUENCE; CELL WALL; CHOLINE; COMPUTATIONAL BIOLOGY; GENOME, BACTERIAL; GENOMICS; MOLECULAR SEQUENCE DATA; STREPTOCOCCUS MITIS; STREPTOCOCCUS ORALIS; STREPTOCOCCUS PNEUMONIAE; TEICHOIC ACIDS;

STREPTOCOCCUS MITIS; STREPTOCOCCUS ORALIS; STREPTOCOCCUS PNEUMONIAE;

EID: 84862018744     PISSN: 10766294     EISSN: 19318448     Source Type: Journal    
DOI: 10.1089/mdr.2012.0026     Document Type: Review

References (94)

1. Aanensen, D.M., A. Mavroidi, S.D. Bentley, P.R. Reeves, and B.G. Spratt. 2007. Predicted functions and linkage specificities of the products of the Streptococcus pneumoniae capsular biosynthetic loci. J. Bacteriol. 189:7856-7876.
2. Allison, S.E., M.A. D'Elia, S. Arar, M.A. Monteiro, and E.D. Brown. 2011. Studies of the genetics, function, and kinetic mechanism of TagE, the wall teichoic acid glycosyl-transferase in Bacillus subtilis 168. J. Biol. Chem. 286:23708-23716.
3. Baur, S., J. Marles-Wright, S. Buckenmaier, R.J. Lewis, and W. Vollmer. 2009. Synthesis of CDP-activated ribitol for teichoic acid precursors in Streptococcus pneumoniae. J. Bacteriol. 191:1200-1210.
4. Bendtsen, J.D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
5. Berg, S., M. Edman, L. Li, M. Wikstrom, and A. Wieslander. 2001. Sequence properties of the 1,2-diacylglycerol 3-glucosyltransferase from Acholeplasma laidlawii membranes. Recognition of a large group of lipid glycosyltransferases in eubacteria and archaea. J. Biol. Chem. 276:22056-22063.
6. Bergström, N., P.E. Jansson, M. Kilian, and U.B. Skov Sorensen. 2000. Structures of two cell wall-associated polysaccharides of a Streptococcus mitis biovar 1 strain. A unique teichoic acid-like polysaccharide and the group O antigen which is a C-polysaccharide in common with pneumococci. Eur. J. Biochem. 267:7147-7157.
7. Bergström, N., P.E. Jansson, M. Kilian, and U.B. Skov Sorensen. 2003. A unique variant of streptococcal group O-antigen (C-polysaccharide) that lacks phosphocholine. Eur. J. Biochem. 270:2157-2162.
8. Briles, E.B., and A. Tomasz. 1975. Membrane lipoteichoic acid is not a precursor to wall teichoic acid in pneumococci. J. Bacteriol. 122:335-337.
9. Brown, S., T. Meredith, J. Swoboda, and S. Walker. 2010. Staphylococcus aureus and Bacillus subtilis W23 make polyribitol wall teichoic acids using different enzymatic pathways. Chem. Biol. 17:1101-1110.
10. Brundish, D.E., N. Shaw, and J. Baddiley. 1965. The glycolipids from the non-capsulated strain of Pneumococcus I-192R, A.T.C.C. 12213. Biochem. J. 97:158-165.
11. Campbell, H.A., and C. Kent. 2001. The CTP:phosphocholine cytidylyltransferase encoded by the licC gene of Streptococcus pneumoniae: cloning, expression, purification, and characterization. Biochim. Biophys. Acta 1534:85-95.
12. Claverys, J.P., B. Martin, and L.S. Håvarstein. 2007. Competence-induced fratricide in streptococci. Mol. Microbiol. 64:1423-1433.
13. Coyne, M.J., A.O. Tzianabos, B.C. Mallory, V.J. Carey, D.L. Kasper, and L.E. Comstock. 2001. Polysaccharide biosynthesis locus required for virulence of Bacteroides fragilis. Infect. Immun. 69:4342-4350.
14. Dagkessamanskaia, A., M. Moscoso, V. Henard, S. Guiral, K. Overweg, M. Reuter, B. Martin, J. Wells, and J.P. Claverys. 2004. Interconnection of competence, stress and CiaR regulons in Streptococcus pneumoniae: competence triggers stationary phase autolysis of ciaR mutant cells. Mol. Microbiol. 51:1071-1086.
15. Damjanovic, M., A.S. Kharat, A. Eberhardt, A. Tomasz, and W. Vollmer. 2007. The essential tacF gene is responsible for the choline-dependent growth phenotype of Streptococcus pneumoniae. J. Bacteriol. 189:7105-7111.
16. Denapaite, D., R. Brückner, M. Nuhn, P. Reichmann, B. Henrich, P. Maurer, Y. Schähle, P. Selbmann, W. Zimmermann, R. Wambutt, et al. 2010. The genome of Streptococcus mitis B6 - what is a commensal? PLoS One 5:e9426.
17. Desai, B.V., H. Reiter, and D.A. Morrison. 2003. Choline starvation induces the gene licD2 in Streptococcus pneumoniae. J. Bacteriol. 185:371-373.
18. Donati, C., N.L. Hiller, H. Tettelin, A. Muzzi, N.J. Croucher, S.V. Angiuoli, M. Oggioni, J.C. Dunning Hotopp, F.Z. Hu, D.R. Riley, et al. 2010. Structure and dynamics of the pan-genome of Streptococcus pneumoniae and closely related species. Genome Biol. 11:R107.
19. Draing, C., M. Pfitzenmaier, S. Zummo, G. Mancuso, A. Geyer, T. Hartung, and von S. Aulock. 2006. Comparison of lipoteichoic acid from different serotypes of Streptococcus pneumoniae. J. Biol. Chem. 281:33849-33859.
20. Eberhardt, A., C.N. Hoyland, D. Vollmer, S. Bisle, R.M. Cleverley, O. Johnsborg, L.S. Havarstein, R.J. Lewis, and W. Vollmer. 2012. Attachment of type 2 capsular polysaccharide to the cell wall in Streptococcus pneumoniae. Microb Drug Resist 18:240-255.
21. Eberhardt, A., L.J. Wu, J. Errington, W. Vollmer, and J.W. Veening. 2009. Cellular localization of choline-utilization proteins in Streptococcus pneumoniae using novel fluorescent reporter systems. Mol. Microbiol. 74:395-408.
22. Edman, M., S. Berg, P. Storm, M. Wikstrom, S. Vikstrom, A. Ohman, and A. Wieslander. 2003. Structural features of glycosyltransferases synthesizing major bilayer and non-bilayer- prone membrane lipids in Acholeplasma laidlawii and Streptococcus pneumoniae. J. Biol. Chem. 278:8420-8428.
23. Fan, X., C.D. Pericone, E. Lysenko, H. Goldfine, and J.N. Weiser. 2003. Multiple mechanisms for choline transport and utilization in Haemophilus influenzae. Mol. Microbiol. 50:537-548.
24. Finn, R.D., J. Mistry, J. Tate, P. Coggill, A. Heger, J.E. Pollington, O.L. Gavin, P. Gunasekaran, G. Ceric, K. Forslund, et al. 2010. The Pfam protein families database. Nucleic Acids Res. 38:D211-D222.
25. Fischer, W. 1988. Physiology of lipoteichoic acids in bacteria. Adv. Microb. Physiol. 29:233-302.
26. Fischer, W. 1994. Lipoteichoic acids and lipoglycans. In J.-M. Ghuysen and R. Hakenbeck (eds.), Bacterial Cell Wall. Elsevier Science B.V., Amsterdam, pp. 199-215.
27. Fischer, W. 1997. Pneumococcal lipoteichoic and teichoic acid. Microb. Drug Resist. 3:309-325.
28. Fischer, W., T. Behr, R. Hartmann, J. Peter-Katalinic, and H. Egge. 1993. Teichoic acid and lipoteichoic acid of Streptococcus pneumoniae possess identical chain structures. A re-investigation of teichoid acid (C polysaccharide). Eur. J. Biochem. 215:851-857.
29. Gehre, F., S.L. Leib, D. Grandgirard, J. Kummer, A. Buhlmann, F. Simon, R. Gaumann, A.S. Kharat, M.G. Tauber, and A. Tomasz. 2008. Essential role of choline for pneumococcal virulence in an experimental model of meningitis. J. Intern. Med. 264:143-154.
30. Gehre, F., R. Spisek, A.S. Kharat, P. Matthews, A. Kukreja, R.M. Anthony, M.V. Dhodapkar, W. Vollmer, and A. Tomasz. 2009. Role of teichoic acid choline moieties in the virulence of Streptococcus pneumoniae. Infect. Immun. 77:2824-2831.
31. Gonzalez, A., D. Llull, M. Morales, P. Garcia, and E. Garcia. 2008. Mutations in the tacF gene of clinical strains and laboratory transformants of Streptococcus pneumoniae: impact on choline auxotrophy and growth rate. J. Bacteriol. 190:4129-4138.
32. Grebe, T., J. Paik, and R. Hakenbeck. 1997. A novel resistance mechanism against beta-lactams in Streptococcus pneumoniae involves CpoA, a putative glycosyltransferase. J. Bacteriol. 179:3342-3349.
33. Gründling, A., and O. Schneewind. 2007. Synthesis of glycerol phosphate lipoteichoic acid in Staphylococcus aureus. Proc. Natl. Acad. Sci. U. S. A. 104:8478-8483.
34. Haas, W., D. Kaushal, J. Sublett, C. Obert, and E.I. Tuomanen. 2005. Vancomycin stress response in a sensitive and a tolerant strain of Streptococcus pneumoniae. J. Bacteriol. 187:8205-8210.
35. Hakenbeck, R., A. Madhour, D. Denapaite, and R. Brückner. 2009. Versatility of choline metabolism and choline- binding proteins in Streptococcus pneumoniae and commensal streptococci. FEMS Microbiol. Rev. 33:572-586.
36. Halfmann, A., M. Kovacs, R. Hakenbeck, and R. Brückner. 2007. Identification of the genes directly controlled by the response regulator CiaR in Streptococcus pneumoniae: five out of 15 promotors drive expression of small non-coding RNAs. Mol. Microbiol. 66:110-126.
37. Halfmann, A., A. Schnorpfeil, M. Müller, P. Marx, U. Günzler, R. Hakenbeck, and R. Brückner. 2011. Activity of the two-component regulatory system CiaRH in Streptococcus pneumoniae R6. J Mol. Microbiol. Biotechnol. 20: 96-104.
38. Håvarstein, L.S., B. Martin, O. Johnsborg, C. Granadel, and J.P. Claverys. 2006. New insights into the pneumococcal fratricide: relationship to clumping and identification of a novel immunity factor. Mol. Microbiol. 59:1297-2307.
39. Hirokawa, T., S. Boon-Chieng, and S. Mitaku. 1998. SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics (Oxford, England) 14: 378-379.
40. Hogg, S.D., R.A. Whiley, and J.J. De Soet. 1997. Occurrence of lipoteichoic acid in oral streptococci. Int. J. Syst. Bacteriol. 47:62-66.
41. Horne, D.S., and A. Tomasz. 1993. Possible role of a choline-containing teichoic acid in the maintenance of normal cell shape and physiology in Streptococcus oralis. J. Bacteriol. 175:1717-1722.
42. Hoskins, J., W.E. Alborn, Jr., J. Arnold, L.C. Blaszczak, S. Burgett, B.S. DeHoff, S.T. Estrem, L. Fritz, D.J. Fu, W. Fuller, et al. 2001. Genome of the bacterium Streptococcus pneumoniae strain R6. J. Bacteriol. 183:5709-5717.
43. Johnsborg, O., and L.S. Håvarstein. 2009. Pneumococcal LytR, a protein from the LytR-CpsA-Psr family, is essential for normal septum formation in Streptococcus pneumoniae. J. Bacteriol. 191:5859-5864.
44. Kawai, Y., J. Marles-Wright, R.M. Cleverley, R. Emmins, S. Ishikawa, M. Kuwano, N. Heinz, N.K. Bui, C.N. Hoyland, N. Ogasawara, et al. 2011. A widespread family of bacterial cell wall assembly proteins. EMBO J. 30:4931-4941.
45. Kern, T., M. Giffard, S. Hediger, A. Amoroso, C. Giustini, N.K. Bui, B. Joris, C. Bougault, W. Vollmer, and J.P. Simorre. 2010. Dynamics characterization of fully hydrated bacterial cell walls by solid-state NMR: evidence for cooperative binding of metal ions. J. Am. Chem. Soc. 132:10911-10919.
46. Kharat, A.S., D. Denapaite, F. Gehre, R. Brückner, W. Vollmer, R. Hakenbeck, and A. Tomasz. 2008. Different pathways of choline metabolism in two choline-independent strains of Streptococcus pneumoniae and their impact on virulence. J. Bacteriol. 190:5907-5914.
47. Kharat, A.S., and A. Tomasz. 2006. Drastic reduction in the virulence of Streptococcus pneumoniae expressing type 2 capsular polysaccharide but lacking choline residues in the cell wall. Mol. Microbiol. 60:93-107.
48. Kilian, M., K. Poulsen, T. Blomqvist, L.S. Håvarstein, M. Bek-Thomsen, H. Tettelin, and U.B. Sorensen. 2008. Evolution of Streptococcus pneumoniae and its close commensal relatives. PLoS One 3: e2683.
49. Koprivnjak, T., V. Mlakar, L. Swanson, B. Fournier, A. Peschel, and J.P. Weiss. 2006. Cation-induced transcriptional regulation of the dlt operon of Staphylococcus aureus. J. Bacteriol. 188:3622-3630.
50. Kovács, M., A. Halfmann, I. Fedtke, M. Heintz, A. Peschel, W. Vollmer, R. Hakenbeck, and R. Brückner. 2006. A Functional dlt Operon, encoding proteins required for incorporation of D-alanine in teichoic acids in gram-positive bacteria, confers resistance to cationic antimicrobial peptides in Streptococcus pneumoniae. J. Bacteriol. 188:5797-5805.
51. Krogh, A., B. Larsson, G. von Heijne, and E.L. Sonnhammer. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:567-580.
52. Kwak, B.Y., Y.M. Zhang, M. Yun, R.J. Heath, C.O. Rock, S. Jackowski, and H.W. Park. 2002. Structure and mechanism of CTP:phosphocholine cytidylyltransferase (LicC) from Streptococcus pneumoniae. J. Biol. Chem. 277:4343-4350.
53. Mascher, T., D. Zähner, M. Merai, N. Balmelle, A.B. de Saizieu, and R. Hakenbeck. 2003. The Streptococcus pneumoniae cia regulon: CiaR target sites and transcription profile analysis. J. Bacteriol. 185:60-70.
54. McGinnis, S., and T.L. Madden. 2004. BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res. 32:W20-W25.
55. Müller, M., P. Marx, R. Hakenbeck, and R. Brückner. 2010. Effect of new alleles of the histidine kinase gene ciaH on the activity of the response regulator CiaR in Streptococcus pneumoniae R6. Microbiology 157:3104-3112.
56. Neuhaus, F.C., and J. Baddiley. 2003. A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria. Microbiol. Mol. Biol. Rev. 67:686-723.
57. Ohkuni, H., Y. Todome, M. Mizuse, N. Ohtani, H. Suzuki, H. Igarashi, Y. Hashimoto, T. Ezaki, K. Harada, Y. Imada, et al. 1993. Biologically active extracellular products of oral viridans streptococci and the aetiology of Kawasaki disease. J. Med. Microbiol. 39:352-362.
58. Panina, E.M., A.G. Vitreschak, A.A. Mironov, and M.S. Gelfand. 2003. Regulation of biosynthesis and transport of aromatic amino acids in low-GC Gram-positive bacteria. FEMS Microbiol. Lett. 222:211-220.
59. Pedersen, C.M., I. Figueroa-Perez, J. Boruwa, B. Lindner, A.J. Ulmer, U. Zähringer, and R.R. Schmidt. 2010. Synthesis of the core structure of the lipoteichoic acid of Streptococcus pneumoniae. Chemistry 16:12627-12641.
60. Pedersen, C.M., I. Figueroa-Perez, B. Lindner, A.J. Ulmer, U. Zähringer, and R.R. Schmidt. 2010. Total synthesis of lipoteichoic acid of Streptococcus pneumoniae. Angew Chem. Int. Ed. Engl. 49:2585-2590.
61. Peschel, A., M. Otto, R.W. Jack, H. Kalbacher, G. Jung, and F. Götz. 1999. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J. Biol. Chem. 274:8405-8410.
62. Rahman, O., L.G. Dover, and I.C. Sutcliffe. 2009. Lipoteichoic acid biosynthesis: two steps forwards, one step sideways? Trends Microbiol. 17:219-225.
63. Rane, L., and Y. Subbarow. 1940. Choline, panthothenic acid and nicotinic acid as essential growth factors for pneumococcus. J. Biol. Chem. 134:455-456.
64. Reichmann, N.T., and A. Gründling. 2011. Location, synthesis and function of glycolipids and polyglycerolphosphate lipoteichoic acid in Gram-positive bacteria of the phylum Firmicutes. FEMS Microbiol. Lett. 319:97-105.
65. Reichmann, P., M. Nuhn, D. Denapaite, R. Brückner, B. Henrich, P. Maurer, M. Rieger, S. Klages, R. Reinhard, and R. Hakenbeck. 2011. Genome of Streptococcus oralis strain Uo5. J. Bacteriol. 193:2888-2889.
66. Rock, C.O., R.J. Heath, H.W. Park, and S. Jackowski. 2001. The licC gene of Streptococcus pneumoniae encodes a CTP:phosphocholine cytidylyltransferase. J. Bacteriol. 183: 4927-4931.
67. Rogers, P.D., T.T. Liu, K.S. Barker, G.M. Hilliard, B.K. English, J. Thornton, E. Swiatlo, and L.S. McDaniel. 2007. Gene expression profiling of the response of Streptococcus pneumoniae to penicillin. J. Antimicrob. Chemother. 59:616-626.
68. Schäffer, C., T. Wugeditsch, P. Messner, and C. Whitfield. 2002. Functional expression of enterobacterial O-polysaccharide biosynthesis enzymes in Bacillus subtilis. Appl. Environ. Microbiol. 68:4722-4730.
69. Schirner, K., J. Marles-Wright, R.J. Lewis, and J. Errington. 2009. Distinct and essential morphogenic functions for wall-and lipo-teichoic acids in Bacillus subtilis. EMBO J. 28: 830-842.
70. Schmidt, R.R., C.M. Pedersen, Y. Qiao, and U. Zähringer. 2011. Chemical synthesis of bacterial lipoteichoic acids: an insight on its biological significance. Org. Biomol. Chem. 9:2040-2052.
71. Seo, H.S., R.T. Cartee, D.G. Pritchard, and M.H. Nahm. 2008. A new model of pneumococcal lipoteichoic acid structure resolves biochemical, biosynthetic, and serologic inconsistencies of the current model. J. Bacteriol. 190: 2379-2387.
72. Severin, A., D. Horne, and A. Tomasz. 1997. Autolysis and cell wall degradation in a choline-independent strain of Streptococcus pneumoniae. Microb. Drug. Resist. 3:391-400.
73. Shine, J., and L. Dalgarno. 1974. The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc. Natl. Acad. Sci. U. S. A. 71:1342-1346.
74. Song J.-H., K.S. Ko, Lee L.-Y., J.Y. Baek, W.S. Oh, H.S. Yoon, Jeong J.-Y., and J. Chun. 2005. Identification of essential genes in Streptococcus pneumoniae by allelic replacement mutagenesis. Mol. Cells 19:365-374.
75. Swoboda, J.G., J. Campbell, T.C. Meredith, and S. Walker. 2010. Wall teichoic acid function, biosynthesis, and inhibition. Chembiochem 11:35-45.
76. Thanassi, J.A., S.L. Hartman-Neumann, T.J. Dougherty, B.A. Dougherty, and M.J. Pucci. 2002. Identification of 113 conserved essential genes using a high-throughput gene disruption system in Streptococcus pneumoniae. Nucleic Acids Res. 30:3152-3162.
77. Tomasz, A. 1967. Choline in the cell wall of a bacterium: novel type of polymer-linked choline in Pneumococcus. Science 157:694-697.
78. Tomasz, A. 1968. Biological consequences of the replacement of choline by ethanolamine in the cell wall of Pneumococcus: chanin formation, loss of transformability, and loss of autolysis. Proc. Natl. Acad. Sci. U. S. A. 59:86-93.
79. Tomasz, A., and M. Westphal. 1971. Abnormal autolytic enzyme in a pneumococus with altered teichoic acid composition. Proc. Natl. Acad. Sci. U. S. A. 68:2627-2630.
80. Ton-That, H., L.A. Marraffini, and O. Schneewind. 2004. Protein sorting to the cell wall envelope of Gram-positive bacteria. Biochim. Biophys. Acta 1694:269-278.
81. Vialle, S., P. Sepulcri, J. Dubayle, and P. Talaga. 2005. The teichoic acid (C-polysaccharide) synthesized by Streptococcus pneumoniae serotype 5 has a specific structure. Carbohydr. Res. 340:91-96.
82. Vollmer, W. 2008. Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbiol. Rev. 32:287-306.
83. Vollmer, W., D. Blanot, and M.A. de Pedro. 2008. Peptidoglycan structure and architecture. FEMS Microbiol. Rev. 32:149-167.
84. Vollmer, W., and A. Tomasz. 2001. Identification of the teichoic acid phosphorylcholine esterase in Streptococcus pneumoniae. Mol. Microbiol. 39:1610-1622.
85. Wang, L., D. Liu, and P.R. Reeves. 1996. C-terminal half of Salmonella enterica WbaP (RfbP) is the galactosyl-1- phosphate transferase domain catalyzing the first step of O-antigen synthesis. J. Bacteriol. 178:2598-2604.
86. Ware, D., J. Watt, and E. Swiatlo. 2005. Utilization of putrescine by Streptococcus pneumoniae during growth in choline-limited medium. J.Microbiol. (Seoul, Korea) 43:398-405.
87. Waters, L.S., and G. Storz. 2009. Regulatory RNAs in bacteria. Cell 136:615-628.
88. Weidenmaier, C., J.F. Kokai-Kun, S.A. Kristian, T. Chanturiya, H. Kalbacher, M. Gross, G. Nicholson, B. Neumeister, J.J. Mond, and A. Peschel. 2004. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat. Med. 10:243-245.
89. Weidenmaier, C., and A. Peschel. 2008. Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat. Rev. Microbiol. 6:276-287.
90. Whiting, G.C., and S.H. Gillespie. 1996. Incorporation of choline into Streptococcus pneumoniae cell wall antigens: evidence for choline kinase activity. FEMS Microbiol. Lett. 138:141-145.
91. Whiting, G.C., and S.H. Gillespie. 1996. Investigation of a choline phosphate synthesis pathway in Streptococcus pneumoniae: evidence for choline phosphate cytidylyltransferase activity. FEMS Microbiol. Lett. 143:279-284.
92. Yother, J., K. Leopold, J. White, and W. Fischer. 1998. Generation and properties of a Streptococcus pneumoniae mutant which does not require choline or analogs for growth. J. Bacteriol. 180:2093-2101.
93. Zalacain, M., S. Biswas, K.A. Ingraham, J. Ambrad, A. Bryant, A.F. Chalker, S. Iordanescu, J. Fan, F. Fan, R.D. Lunsford, et al. 2003. A global approach to identify novel broad-spectrum antibacterial targets among proteins of unknown function. J. Mol. Microbiol. Biotechnol. 6:109-126.
94. Zhang, J.R., I. Idanpaan-Heikkila, W. Fischer, and E.I. Tuomanen. 1999. Pneumococcal licD2 gene is involved in phosphorylcholine metabolism. Mol. Microbiol. 31:1477-1488.