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Chapter 19 : Capsular Polysaccharide

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Abstract:

The presence of what is now recognized as the polysaccharide capsule on the surface of was noted by Pasteur in the first published description of the organism in 1880, and since that time it has been the direct or indirect focus of intensive investigation [reviewed by Austrian ( )]. Studies during the first three decades of the 20th century demonstrated the existence of multiple capsular serotypes of and the fact that antibodies to the capsule conferred type-specific protection against challenge in laboratory animals. The capsular material itself was isolated by Dochez and Avery in 1917 ( ), but the fact that it was immunogenic led them to believe that this “soluble substance of the pneumococcus” was proteinaceous in nature. It was not until 1925 that Avery and colleagues ( ) demonstrated that the pneumococcal capsule consisted of polysaccharide, the first nonprotein antigen to be recognized.

Citation: Paton J, Trappetti C. 2019. Capsular Polysaccharide, p 304-315. In Fischetti V, Novick R, Ferretti J, Portnoy D, Braunstein M, Rood J (ed), Gram-Positive Pathogens, Third Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.GPP3-0019-2018
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Figures

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Figure 1

Comparison of the CPS biological repeat unit structures of serotypes 6A, 6B, 14, 15B, 15C 19F, 19A, 19B, and 19C. These are based on published chemical repeat unit structures ( ), adjusting for the fact that Glc is the first sugar of the biological repeat unit.

Citation: Paton J, Trappetti C. 2019. Capsular Polysaccharide, p 304-315. In Fischetti V, Novick R, Ferretti J, Portnoy D, Braunstein M, Rood J (ed), Gram-Positive Pathogens, Third Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.GPP3-0019-2018
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Image of Figure 2
Figure 2

Organization of the loci from selected serotypes. Gene and locus designations are as published. Open reading frames (ORFs) within the DNA sequence are indicated by large boxed arrows. Highly conserved ORFs, or those encoding proteins belonging to a particular functional group, are identified as shown in the legend at the bottom of the figure. Assignment of an ORF to a given function-related group is based on the published information for each locus as well as on additional database comparisons for some of the ORFs. The short boxed arrows represent cryptic ORFs not required for CPS biosynthesis in the respective serotype.

Citation: Paton J, Trappetti C. 2019. Capsular Polysaccharide, p 304-315. In Fischetti V, Novick R, Ferretti J, Portnoy D, Braunstein M, Rood J (ed), Gram-Positive Pathogens, Third Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.GPP3-0019-2018
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References

/content/book/10.1128/9781683670131.chap19
1. Austrian R . 1981. Pneumococcus: the first one hundred years. Rev Infect Dis 3 : 183 189.[CrossRef][PubMed]
2. Austrian R . 1981. Some observations on the pneumococcus and on the current status of pneumococcal disease and its prevention. Rev Infect Dis 3( Suppl) : S1 S17.[CrossRef]
3. Dochez AR,, Avery OT . 1917. The elaboration of specific soluble substance by pneumococcus during growth. J Exp Med 26 : 477 493.[CrossRef]
4. Avery OT,, Heidelberger M . 1925. Immunological relationships of cell constituents of pneumococcus. J Exp Med 42 : 367 376.[CrossRef][PubMed]
5. Avery OT,, Morgan HJ . 1925. Immunological reactions of the isolated carbohydrate and protein of pneumococcus. J Exp Med 42 : 347 353.[CrossRef]
6. Skov Sørensen UB,, Blom J,, Birch-Andersen A,, Henrichsen J . 1988. Ultrastructural localization of capsules, cell wall polysaccharide, cell wall proteins, and F antigen in pneumococci. Infect Immun 56 : 1890 1896.[PubMed]
7. Sørensen UBS,, Henrichsen J,, Chen HC,, Szu SC . 1990. Covalent linkage between the capsular polysaccharide and the cell wall peptidoglycan of Streptococcus pneumoniae revealed by immunochemical methods. Microb Pathog 8 : 325 334.[CrossRef]
8. Geno KA,, Saad JS,, Nahm MH . 2017. Discovery of novel pneumococcal serotype 35D, a natural WciG-deficient variant of serotype 35B. J Clin Microbiol 55 : 1416 1425.[CrossRef][PubMed]
9. Geno KA,, Gilbert GL,, Song JY,, Skovsted IC,, Klugman KP,, Jones C,, Konradsen HB,, Nahm MH . 2015. Pneumococcal capsules and their types: past, present, and future. Clin Microbiol Rev 28 : 871 899.[CrossRef]
10. Avery OT,, Dubos R . 1931. The protective action of a specific enzyme against type III pneumococcus infections in mice. J Exp Med 54 : 73 89.[CrossRef][PubMed]
11. Bender MH,, Yother J . 2001. CpsB is a modulator of capsule-associated tyrosine kinase activity in Streptococcus pneumoniae. J Biol Chem 276 : 47966 47974.[CrossRef][PubMed]
12. Hardy GG,, Magee AD,, Ventura CL,, Caimano MJ,, Yother J . 2001. Essential role for cellular phosphoglucomutase in virulence of type 3 Streptococcus pneumoniae. Infect Immun 69 : 2309 2317.[CrossRef][PubMed]
13. Magee AD,, Yother J . 2001. Requirement for capsule in colonization by Streptococcus pneumoniae. Infect Immun 69 : 3755 3761.[CrossRef][PubMed]
14. Morona JK,, Miller DC,, Morona R,, Paton JC . 2004. The effect that mutations in the conserved capsular polysaccharide biosynthesis genes cpsA, cpsB, and cpsD have on virulence of Streptococcus pneumoniae. J Infect Dis 189 : 1905 1913.[CrossRef][PubMed]
15. Marsh R,, Smith-Vaughan H,, Hare KM,, Binks M,, Kong F,, Warning J,, Gilbert GL,, Morris P,, Leach AJ . 2010. The nonserotypeable pneumococcus: phenotypic dynamics in the era of anticapsular vaccines. J Clin Microbiol 48 : 831 835.[CrossRef][PubMed]
16. Keller LE,, Robinson DA,, McDaniel LS . 2016. Nonencapsulated Streptococcus pneumoniae: emergence and pathogenesis. MBio 7 : e01792.[CrossRef][PubMed]
17. Griffith F . 1928. The significance of pneumococcal types. J Hyg (Lond) 27 : 113 159.[CrossRef]
18. Avery OT,, Macleod CM,, McCarty M . 1944. Studies on the chemical nature of the substance inducing transformation of pneumococcal types. Induction of transformation by a desoxyribonucleic acid fraction isolated from pneumococcus type III. J Exp Med 79 : 137 158.[CrossRef][PubMed]
19. Nelson AL,, Roche AM,, Gould JM,, Chim K,, Ratner AJ,, Weiser JN . 2007. Capsule enhances pneumococcal colonization by limiting mucus-mediated clearance. Infect Immun 75 : 83 90.[CrossRef][PubMed]
20. Hyams C,, Camberlein E,, Cohen JM,, Bax K,, Brown JS . 2010. The Streptococcus pneumoniae capsule inhibits complement activity and neutrophil phagocytosis by multiple mechanisms. Infect Immun 78 : 704 715.[CrossRef][PubMed]
21. Abeyta M,, Hardy GG,, Yother J . 2003. Genetic alteration of capsule type but not PspA type affects accessibility of surface-bound complement and surface antigens of Streptococcus pneumoniae. Infect Immun 71 : 218 225.[CrossRef][PubMed]
22. Wartha F,, Beiter K,, Albiger B,, Fernebro J,, Zychlinsky A,, Normark S,, Henriques-Normark B . 2007. Capsule and d-alanylated lipoteichoic acids protect Streptococcus pneumoniae against neutrophil extracellular traps. Cell Microbiol 9 : 1162 1171.[CrossRef][PubMed]
23. de Vos AF,, Dessing MC,, Lammers AJ,, de Porto AP,, Florquin S,, de Boer OJ,, de Beer R,, Terpstra S,, Bootsma HJ,, Hermans PW,, van ’t Veer C,, van der Poll T . 2015. The polysaccharide capsule of Streptococcus pneumonia partially impedes MyD88-mediated immunity during pneumonia in mice. PLoS One 10 : e0118181.[CrossRef][PubMed]
24. MacLEOD CM,, Kraus MR . 1950. Relation of virulence of pneumococcal strains for mice to the quantity of capsular polysaccharide formed in vitro. J Exp Med 92 : 1 9.[CrossRef]
25. Hyams C,, Yuste J,, Bax K,, Camberlein E,, Weiser JN,, Brown JS . 2010. Streptococcus pneumoniae resistance to complement-mediated immunity is dependent on the capsular serotype. Infect Immun 78 : 716 725.[CrossRef][PubMed]
26. Kelly T,, Dillard JP,, Yother J . 1994. Effect of genetic switching of capsular type on virulence of Streptococcus pneumoniae. Infect Immun 62 : 1813 1819.[PubMed]
27. Nesin M,, Ramirez M,, Tomasz A . 1998. Capsular transformation of a multidrug-resistant Streptococcus pneumoniae in vivo. J Infect Dis 177 : 707 713.[CrossRef][PubMed]
28. Trzciński K,, Li Y,, Weinberger DM,, Thompson CM,, Cordy D,, Bessolo A,, Malley R,, Lipsitch M . 2015. Effect of serotype on pneumococcal competition in a mouse colonization model. MBio 6 : e00902-15.[CrossRef][PubMed]
29. Zafar MA,, Hamaguchi S,, Zangari T,, Cammer M,, Weiser JN . 2017. Capsule type and amount affect shedding and transmission of Streptococcus pneumoniae. MBio 8 : e00989-17.[CrossRef][PubMed]
30. Hyams C,, Trzcinski K,, Camberlein E,, Weinberger DM,, Chimalapati S,, Noursadeghi M,, Lipsitch M,, Brown JS . 2013. Streptococcus pneumoniae capsular serotype invasiveness correlates with the degree of factor H binding and opsonization with C3b/iC3b. Infect Immun 81 : 354 363.[CrossRef][PubMed]
31. Lee CJ,, Banks SD,, Li JP . 1991. Virulence, immunity, and vaccine related to Streptococcus pneumoniae. Crit Rev Microbiol 18 : 89 114.[CrossRef][PubMed]
32. Douglas RM,, Paton JC,, Duncan SJ,, Hansman DJ . 1983. Antibody response to pneumococcal vaccination in children younger than five years of age. J Infect Dis 48 : 131 137.
33. O’Brien KL,, Millar EV,, Zell ER,, Bronsdon M,, Weatherholtz R,, Reid R,, Becenti J,, Kvamme S,, Whitney CG,, Santosham M . 2007. Effect of pneumococcal conjugate vaccine on nasopharyngeal colonization among immunized and unimmunized children in a community-randomized trial. J Infect Dis 196 : 1211 1220.[CrossRef][PubMed]
34. Centers for Disease Control and Prevention (CDC) . 2005. Direct and indirect effects of routine vaccination of children with 7-valent pneumococcal conjugate vaccine on incidence of invasive pneumococcal disease--United States, 1998-2003. MMWR Morb Mortal Wkly Rep 54 : 893897.[PubMed]
35. Brueggemann AB,, Pai R,, Crook DW,, Beall B . 2007. Vaccine escape recombinants emerge after pneumococcal vaccination in the United States. PLoS Pathog 3 : e168.[CrossRef][PubMed]
36. Hicks LA,, Harrison LH,, Flannery B,, Hadler JL,, Schaffner W,, Craig AS,, Jackson D,, Thomas A,, Beall B,, Lynfield R,, Reingold A,, Farley MM,, Whitney CG . 2007. Incidence of pneumococcal disease due to non-pneumococcal conjugate vaccine (PCV7) serotypes in the United States during the era of widespread PCV7 vaccination, 1998-2004. J Infect Dis 196 : 1346 1354.[CrossRef][PubMed]
37. Klugman KP . 2009. The significance of serotype replacement for pneumococcal disease and antibiotic resistance. Adv Exp Med Biol 634 : 121 128.[CrossRef][PubMed]
38. von Gottberg A,, de Gouveia L,, Tempia S,, Quan V,, Meiring S,, von Mollendorf C,, Madhi SA,, Zell ER,, Verani JR,, O’Brien KL,, Whitney CG,, Klugman KP,, Cohen C, GERMS-SA Investigators . 2014. Effects of vaccination on invasive pneumococcal disease in South Africa. N Engl J Med 371 : 1889 1899.[CrossRef][PubMed]
39. Austrian R,, Bernheimer HP,, Smith EEB,, Mills GT . 1959. Simultaneous production of two capsular polysaccharides by pneumococcus. II. The genetic and biochemical bases of binary capsulation. J Exp Med 110 : 585 602.[CrossRef][PubMed]
40. Bernheimer HP,, Wermundsen IE,, Austrian R . 1967. Qualitative differences in the behavior of pneumoncoccal deoxyribonucleic acids transforming to the same capsular type. J Bacteriol 93 : 320 333.[PubMed]
41. Guidolin A,, Morona JK,, Morona R,, Hansman D,, Paton JC . 1994. Nucleotide sequence analysis of genes essential for capsular polysaccharide biosynthesis in Streptococcus pneumoniae type 19F. Infect Immun 62 : 5384 5396.[PubMed]
42. Dillard JP,, Vandersea MW,, Yother J . 1995. Characterization of the cassette containing genes for type 3 capsular polysaccharide biosynthesis in Streptococcus pneumoniae. J Exp Med 181 : 973 983.[CrossRef][PubMed]
43. Arrecubieta C,, García E,, López R . 1995. Sequence and transcriptional analysis of a DNA region involved in the production of capsular polysaccharide in Streptococcus pneumoniae type 3. Gene 167 : 1 7.[CrossRef]
44. Morona JK,, Morona R,, Paton JC . 1997. Characterization of the locus encoding the Streptococcus pneumoniae type 19F capsular polysaccharide biosynthetic pathway. Mol Microbiol 23 : 751 763.[CrossRef][PubMed]
45. Morona JK,, Morona R,, Paton JC . 1997. Molecular and genetic characterization of the capsule biosynthesis locus of Streptococcus pneumoniae type 19B. J Bacteriol 179 : 4953 4958.[CrossRef][PubMed]
46. Kolkman MAB,, van der Zeijst BAM,, Nuijten PJM . 1997. Functional analysis of glycosyltransferases encoded by the capsular polysaccharide biosynthesis locus of Streptococcus pneumoniae serotype 14. J Biol Chem 272 : 19502 19508.[CrossRef][PubMed]
47. Kolkman MAB,, Wakarchuk W,, Nuijten PJM,, van der Zeijst BAM . 1997. Capsular polysaccharide synthesis in Streptococcus pneumoniae serotype 14: molecular analysis of the complete cps locus and identification of genes encoding glycosyltransferases required for the biosynthesis of the tetrasaccharide subunit. Mol Microbiol 26 : 197 208.[CrossRef][PubMed]
48. Muñoz R,, Mollerach M,, López R,, García E . 1997. Molecular organization of the genes required for the synthesis of type 1 capsular polysaccharide of Streptococcus pneumoniae: formation of binary encapsulated pneumococci and identification of cryptic dTDP-rhamnose biosynthesis genes. Mol Microbiol 25 : 79 92.[CrossRef]
49. Llull D,, López R,, García E,, Muñoz R . 1998. Molecular structure of the gene cluster responsible for the synthesis of the polysaccharide capsule of Streptococcus pneumoniae type 33F. Biochim Biophys Acta 1443 : 217 224.[CrossRef]
50. Ramirez M,, Tomasz A . 1998. Molecular characterization of the complete 23F capsular polysaccharide locus of Streptococcus pneumoniae. J Bacteriol 180 : 5273 5278.[PubMed]
51. Morona JK,, Morona R,, Paton JC . 1999. Analysis of the 5′ portion of the type 19A capsule locus identifies two classes of cpsC, cpsD, and cpsE genes in Streptococcus pneumoniae. J Bacteriol 181 : 3599 3605.[PubMed]
52. Morona JK,, Morona R,, Paton JC . 1999. Comparative genetics of capsular polysaccharide biosynthesis in Streptococcus pneumoniae types belonging to serogroup 19. J Bacteriol 181 : 5355 5364.[PubMed]
53. Morona JK,, Miller DC,, Coffey TJ,, Vindurampulle CJ,, Spratt BG,, Morona R,, Paton JC . 1999. Molecular and genetic characterization of the capsule biosynthesis locus of Streptococcus pneumoniae type 23F. Microbiology 145 : 781 789.[CrossRef][PubMed]
54. Llull D,, Muñoz R,, López R,, García E . 1999. A single gene ( tts) located outside the cap locus directs the formation of Streptococcus pneumoniae type 37 capsular polysaccharide. Type 37 pneumococci are natural, genetically binary strains. J Exp Med 190 : 241 251.[CrossRef][PubMed]
55. Muñoz R,, Mollerach M,, López R,, García E . 1999. Characterization of the type 8 capsular gene cluster of Streptococcus pneumoniae. J Bacteriol 181 : 6214 6219.
56. Iannelli F,, Pearce BJ,, Pozzi G . 1999. The type 2 capsule locus of Streptococcus pneumoniae. J Bacteriol 181 : 2652 2654.[PubMed]
57. Jiang SM,, Wang L,, Reeves PR . 2001. Molecular characterization of Streptococcus pneumoniae type 4, 6B, 8, and 18C capsular polysaccharide gene clusters. Infect Immun 69 : 1244 1255.[CrossRef][PubMed]
58. van Selm S,, Kolkman MA,, van der Zeijst BA,, Zwaagstra KA,, Gaastra W,, van Putten JP . 2002. Organization and characterization of the capsule biosynthesis locus of Streptococcus pneumoniae serotype 9V. Microbiology 148 : 1747 1755.[CrossRef][PubMed]
59. van Selm S,, van Cann LM,, Kolkman MA,, van der Zeijst BA,, van Putten JP . 2003. Genetic basis for the structural difference between Streptococcus pneumoniae serotype 15B and 15C capsular polysaccharides. Infect Immun 71 : 6192 6198.[CrossRef][PubMed]
60. Bentley SD,, Aanensen DM,, Mavroidi A,, Saunders D,, Rabbinowitsch E,, Collins M,, Donohoe K,, Harris D,, Murphy L,, Quail MA,, Samuel G,, Skovsted IC,, Kaltoft MS,, Barrell B,, Reeves PR,, Parkhill J,, Spratt BG . 2006. Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLoS Genet 2 : e31.[CrossRef][PubMed]
61. Dillard JP,, Yother J . 1994. Genetic and molecular characterization of capsular polysaccharide biosynthesis in Streptococcus pneumoniae type 3. Mol Microbiol 12 : 959 972.[CrossRef][PubMed]
62. García E,, García P,, López R . 1993. Cloning and sequencing of a gene involved in the synthesis of the capsular polysaccharide of Streptococcus pneumoniae type 3. Mol Gen Genet 239 : 188 195.[PubMed]
63. Arrecubieta C,, López R,, García E . 1994. Molecular characterization of cap3A, a gene from the operon required for the synthesis of the capsule of Streptococcus pneumoniae type 3: sequencing of mutations responsible for the unencapsulated phenotype and localization of the capsular cluster on the pneumococcal chromosome. J Bacteriol 176 : 6375 6383.[CrossRef][PubMed]
64. Arrecubieta C,, López R,, García E . 1996. Type 3-specific synthase of Streptococcus pneumoniae (Cap3B) directs type 3 polysaccharide biosynthesis in Escherichia coli and in pneumococcal strains of different serotypes. J Exp Med 184 : 449 455.[CrossRef][PubMed]
65. DeAngelis PL,, Papaconstantinou J,, Weigel PH . 1993. Molecular cloning, identification, and sequence of the hyaluronan synthase gene from group A Streptococcus pyogenes. J Biol Chem 268 : 19181 19184.[PubMed]
66. Keenleyside WJ,, Whitfield C . 1996. A novel pathway for O-polysaccharide biosynthesis in Salmonella enterica serovar Borreze. J Biol Chem 271 : 28581 28592.[CrossRef][PubMed]
67. Mollerach M,, López R,, García E . 1998. Characterization of the galU gene of Streptococcus pneumoniae encoding a uridine diphosphoglucose pyrophosphorylase: a gene essential for capsular polysaccharide biosynthesis. J Exp Med 188 : 2047 2056.[CrossRef][PubMed]
68. Cartee RT,, Forsee WT,, Jensen JW,, Yother J . 2001. Expression of the Streptococcus pneumoniae type 3 synthase in Escherichia coli. Assembly of type 3 polysaccharide on a lipid primer. J Biol Chem 276 : 48831 48839.[CrossRef][PubMed]
69. Llull D,, García E,, López R . 2001. Tts, a processive beta-glucosyltransferase of Streptococcus pneumoniae, directs the synthesis of the branched type 37 capsular polysaccharide in Pneumococcus and other gram-positive species. J Biol Chem 276 : 21053 21061.[CrossRef][PubMed]
70. Yother J . 2011. Capsules of Streptococcus pneumoniae and other bacteria: paradigms for polysaccharide biosynthesis and regulation. Annu Rev Microbiol 65 : 563 581.[CrossRef][PubMed]
71. Whitfield C,, Paiment A . 2003. Biosynthesis and assembly of group 1 capsular polysaccharides in Escherichia coli and related extracellular polysaccharides in other bacteria. Carbohydr Res 338 : 2491 2502.[CrossRef][PubMed]
72. Kolkman MAB,, Morrison DA,, Van Der Zeijst BAM,, Nuijten PJM . 1996. The capsule polysaccharide synthesis locus of Streptococcus pneumoniae serotype 14: identification of the glycosyl transferase gene cps14E. J Bacteriol 178 : 3736 3741.[CrossRef][PubMed]
73. Larson TR,, Yother J . 2017. Streptococcus pneumoniae capsular polysaccharide is linked to peptidoglycan via a direct glycosidic bond to β- d- N-acetylglucosamine. Proc Natl Acad Sci U S A 114 : 5695 5700.[CrossRef][PubMed]
74. Eberhardt A,, Hoyland CN,, Vollmer D,, Bisle S,, Cleverley RM,, Johnsborg O,, Håvarstein LS,, Lewis RJ,, Vollmer W . 2012. Attachment of capsular polysaccharide to the cell wall in Streptococcus pneumoniae. Microb Drug Resist 18 : 240 255.[CrossRef][PubMed]
75. Morona JK,, Morona R,, Paton JC . 2006. Attachment of capsular polysaccharide to the cell wall of Streptococcus pneumoniae type 2 is required for invasive disease. Proc Natl Acad Sci U S A 103 : 8505 8510.[CrossRef][PubMed]
76. Lawrence ER,, Griffiths DB,, Martin SA,, George RC,, Hall LM . 2003. Evaluation of semiautomated multiplex PCR assay for determination of Streptococcus pneumoniae serotypes and serogroups. J Clin Microbiol 41 : 601 607.[CrossRef][PubMed]
77. Mostowy RJ,, Croucher NJ,, De Maio N,, Chewapreecha C,, Salter SJ,, Turner P,, Aanensen DM,, Bentley SD,, Didelot X,, Fraser C . 2017. Pneumococcal capsule synthesis locus cps as evolutionary hotspot with potential to generate novel serotypes by recombination. Mol Biol Evol 34 : 2537 2554.[CrossRef][PubMed]
78. Barnes DM,, Whittier S,, Gilligan PH,, Soares S,, Tomasz A,, Henderson FW . 1995. Transmission of multidrug-resistant serotype 23F Streptococcus pneumoniae in group day care: evidence suggesting capsular transformation of the resistant strain in vivo. J Infect Dis 171 : 890 896.[CrossRef][PubMed]
79. Coffey TJ,, Dowson CG,, Daniels M,, Zhou J,, Martin C,, Spratt BG,, Musser JM . 1991. Horizontal transfer of multiple penicillin-binding protein genes, and capsular biosynthetic genes, in natural populations of Streptococcus pneumoniae. Mol Microbiol 5 : 2255 2260.[CrossRef][PubMed]
80. Coffey TJ,, Enright MC,, Daniels M,, Wilkinson P,, Berrón S,, Fenoll A,, Spratt BG . 1998. Serotype 19A variants of the Spanish serotype 23F multiresistant clone of Streptococcus pneumoniae. Microb Drug Resist 4 : 51 55.[CrossRef][PubMed]
81. Coffey TJ,, Enright MC,, Daniels M,, Morona JK,, Morona R,, Hryniewicz W,, Paton JC,, Spratt BG . 1998. Recombinational exchanges at the capsular polysaccharide biosynthetic locus lead to frequent serotype changes among natural isolates of Streptococcus pneumoniae. Mol Microbiol 27 : 73 83.[CrossRef][PubMed]
82. Kroll JS,, Loynds BM,, Moxon ER . 1991. The Haemophilus influenzae capsulation gene cluster: a compound transposon. Mol Microbiol 5 : 1549 1560.[CrossRef][PubMed]
83. Chewapreecha C,, Harris SR,, Croucher NJ,, Turner C,, Marttinen P,, Cheng L,, Pessia A,, Aanensen DM,, Mather AE,, Page AJ,, Salter SJ,, Harris D,, Nosten F,, Goldblatt D,, Corander J,, Parkhill J,, Turner P,, Bentley SD . 2014. Dense genomic sampling identifies highways of pneumococcal recombination. Nat Genet 46 : 305 309.[CrossRef][PubMed]
84. Chaguza C,, Andam CP,, Harris SR,, Cornick JE,, Yang M,, Bricio-Moreno L,, Kamng’ona AW,, Parkhill J,, French N,, Heyderman RS,, Kadioglu A,, Everett DB,, Bentley SD,, Hanage WP . 2016. Recombination in Streptococcus pneumoniae lineages increase with carriage duration and size of the polysaccharide capsule. MBio 7 : e01053-16.[CrossRef][PubMed]
85. Marks LR,, Reddinger RM,, Hakansson AP . 2012. High levels of genetic recombination during nasopharyngeal carriage and biofilm formation in Streptococcus pneumoniae. MBio 3 : e00200-12.[CrossRef][PubMed]
86. Skov Sørensen UB,, Yao K,, Yang Y,, Tettelin H,, Kilian M . 2016. Capsular polysaccharide expression in commensal Streptococcus species: genetic and antigenic similarities to Streptococcus pneumoniae. MBio 7 : e01844-16.[CrossRef][PubMed]
87. Orihuela CJ,, Radin JN,, Sublett JE,, Gao G,, Kaushal D,, Tuomanen EI . 2004. Microarray analysis of pneumococcal gene expression during invasive disease. Infect Immun 72 : 5582 5596.[CrossRef][PubMed]
88. Ogunniyi AD,, Mahdi LK,, Trappetti C,, Verhoeven N,, Mermans D,, Van der Hoek MB,, Plumptre CD,, Paton JC . 2012. Identification of genes that contribute to the pathogenesis of invasive pneumococcal disease by in vivo transcriptomic analysis. Infect Immun 80 : 3268 3278.[CrossRef][PubMed]
89. Talbot UM,, Paton AW,, Paton JC . 1996. Uptake of Streptococcus pneumoniae by respiratory epithelial cells. Infect Immun 64 : 3772 3777.[PubMed]
90. Morona JK,, Paton JC,, Miller DC,, Morona R . 2000. Tyrosine phosphorylation of CpsD negatively regulates capsular polysaccharide biosynthesis in Streptococcus pneumoniae. Mol Microbiol 35 : 1431 1442.[CrossRef][PubMed]
91. Cieslewicz MJ,, Kasper DL,, Wang Y,, Wessels MR . 2001. Functional analysis in type Ia group B Streptococcus of a cluster of genes involved in extracellular polysaccharide production by diverse species of streptococci. J Biol Chem 276 : 139 146.[CrossRef][PubMed]
92. Morona JK,, Morona R,, Miller DC,, Paton JC . 2003. Mutational analysis of the carboxy-terminal (YGX) 4 repeat domain of CpsD, an autophosphorylating tyrosine kinase required for capsule biosynthesis in Streptococcus pneumoniae. J Bacteriol 185 : 3009 3019.[CrossRef][PubMed]
93. Bender MH,, Cartee RT,, Yother J . 2003. Positive correlation between tyrosine phosphorylation of CpsD and capsular polysaccharide production in Streptococcus pneumoniae. J Bacteriol 185 : 6057 6066.[CrossRef][PubMed]
94. Glucksmann MA,, Reuber TL,, Walker GC . 1993. Genes needed for the modification, polymerization, export, and processing of succinoglycan by Rhizobium meliloti: a model for succinoglycan biosynthesis. J Bacteriol 175 : 7045 7055.[CrossRef][PubMed]
95. Morona R,, Van Den Bosch L,, Daniels C . 2000. Evaluation of Wzz/MPA1/MPA2 proteins based on the presence of coiled-coil regions. Microbiology 146 : 1 4.[CrossRef][PubMed]
96. Morona JK,, Morona R,, Miller DC,, Paton JC . 2002. Streptococcus pneumoniae capsule biosynthesis protein CpsB is a novel manganese-dependent phosphotyrosine-protein phosphatase. J Bacteriol 184 : 577 583.[CrossRef][PubMed]
97. Weiser JN,, Bae D,, Epino H,, Gordon SB,, Kapoor M,, Zenewicz LA,, Shchepetov M . 2001. Changes in availability of oxygen accentuate differences in capsular polysaccharide expression by phenotypic variants and clinical isolates of Streptococcus pneumoniae. Infect Immun 69 : 5430 5439.[CrossRef][PubMed]
98. Geno KA,, Hauser JR,, Gupta K,, Yother J . 2014. Streptococcus pneumoniae phosphotyrosine phosphatase CpsB and alterations in capsule production resulting from changes in oxygen availability. J Bacteriol 196 : 1992 2003.[CrossRef][PubMed]
99. Henriques MX,, Rodrigues T,, Carido M,, Ferreira L,, Filipe SR . 2011. Synthesis of capsular polysaccharide at the division septum of Streptococcus pneumoniae is dependent on a bacterial tyrosine kinase. Mol Microbiol 82 : 515 534.[CrossRef][PubMed]
100. Nourikyan J,, Kjos M,, Mercy C,, Cluzel C,, Morlot C,, Noirot-Gros MF,, Guiral S,, Lavergne JP,, Veening JW,, Grangeasse C . 2015. Autophosphorylation of the bacterial tyrosine-kinase CpsD connects capsule synthesis with the cell cycle in Streptococcus pneumoniae. PLoS Genet 11 : e1005518.[CrossRef][PubMed]
101. Standish AJ,, Whittall JJ,, Morona R . 2014. Tyrosine phosphorylation enhances activity of pneumococcal autolysin LytA. Microbiology 160 : 2745 2754.[CrossRef][PubMed]
102. Hammerschmidt S,, Wolff S,, Hocke A,, Rosseau S,, Müller E,, Rohde M . 2005. Illustration of pneumococcal polysaccharide capsule during adherence and invasion of epithelial cells. Infect Immun 73 : 4653 4667.[CrossRef][PubMed]
103. Kietzman CC,, Gao G,, Mann B,, Myers L,, Tuomanen EI . 2016. Dynamic capsule restructuring by the main pneumococcal autolysin LytA in response to the epithelium. Nat Commun 7 : 10859.[CrossRef][PubMed]
104. Ogunniyi AD,, Giammarinaro P,, Paton JC . 2002. The genes encoding virulence-associated proteins and the capsule of Streptococcus pneumoniae are upregulated and differentially expressed in vivo. Microbiology 148 : 2045 2053.[CrossRef][PubMed]
105. Giammarinaro P,, Paton JC . 2002. Role of RegM, a homologue of the catabolite repressor protein CcpA, in the virulence of Streptococcus pneumoniae. Infect Immun 70 : 5454 5461.[CrossRef][PubMed]
106. Wen Z,, Sertil O,, Cheng Y,, Zhang S,, Liu X,, Wang WC,, Zhang JR . 2015. Sequence elements upstream of the core promoter are necessary for full transcription of the capsule gene operon in Streptococcus pneumoniae strain D39. Infect Immun 83 : 1957 1972.[CrossRef][PubMed]
107. Shainheit MG,, Mulé M,, Camilli A . 2014. The core promoter of the capsule operon of Streptococcus pneumoniae is necessary for colonization and invasive disease. Infect Immun 82 : 694 705.[CrossRef][PubMed]
108. Wen Z,, Liu Y,, Qu F,, Zhang JR . 2016. Allelic variation of the capsule promoter diversifies encapsulation and virulence in Streptococcus pneumoniae. Sci Rep 6 : 30176.[CrossRef][PubMed]
109. Wu K,, Xu H,, Zheng Y,, Wang L,, Zhang X,, Yin Y . 2016. CpsR, a GntR family regulator, transcriptionally regulates capsular polysaccharide biosynthesis and governs bacterial virulence in Streptococcus pneumoniae. Sci Rep 6 : 29255.[CrossRef][PubMed]
110. Zheng Y,, Zhang X,, Wang X,, Wang L,, Zhang J,, Yin Y . 2017. ComE, an essential response regulator, negatively regulates the expression of the capsular polysaccharide locus and attenuates the bacterial virulence in Streptococcus pneumoniae. Front Microbiol 8 : 277.[CrossRef][PubMed]
111. Weiser JN,, Austrian R,, Sreenivasan PK,, Masure HR . 1994. Phase variation in pneumococcal opacity: relationship between colonial morphology and nasopharyngeal colonization. Infect Immun 62 : 2582 2589.[PubMed]
112. Cundell DR,, Weiser JN,, Shen J,, Young A,, Tuomanen EI . 1995. Relationship between colonial morphology and adherence of Streptococcus pneumoniae. Infect Immun 63 : 757 761.[PubMed]
113. Kim JO,, Weiser JN . 1998. Association of intrastrain phase variation in quantity of capsular polysaccharide and teichoic acid with the virulence of Streptococcus pneumoniae. J Infect Dis 177 : 368 377.[CrossRef][PubMed]
114. Manso AS,, Chai MH,, Atack JM,, Furi L,, De Ste Croix M,, Haigh R,, Trappetti C,, Ogunniyi AD,, Shewell LK,, Boitano M,, Clark TA,, Korlach J,, Blades M,, Mirkes E,, Gorban AN,, Paton JC,, Jennings MP,, Oggioni MR . 2014. A random six-phase switch regulates pneumococcal virulence via global epigenetic changes. Nat Commun 5 : 5055.[CrossRef][PubMed]
115. Trappetti C,, Potter AJ,, Paton AW,, Oggioni MR,, Paton JC . 2011. LuxS mediates iron-dependent biofilm formation, competence, and fratricide in Streptococcus pneumoniae. Infect Immun 79 : 4550 4558.[CrossRef][PubMed]
116. Trappetti C,, McAllister LJ,, Chen A,, Wang H,, Paton AW,, Oggioni MR,, McDevitt CA,, Paton JC . 2017. Autoinducer 2 signaling via the phosphotransferase FruA drives galactose utilization by Streptococcus pneumoniae, resulting in hypervirulence. MBio 8 : e02269-16.[CrossRef]

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