Pyruvate Oxidase Influences the Sugar Utilization Pattern and Capsule Production in Streptococcus pneumoniae

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Carvalho, Sandra M ^a   Farshchi Andisi, Vahid ^b   Gradstedt, Henrik ^b   Neef, Jolanda ^b   Kuipers, Oscar P ^c   Neves, Ana R ^a,d   Bijlsma, Jetta J E ^b  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

^d Chalmers University of Technology   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; HYDROGEN PEROXIDE; MUTANT PROTEIN; PYRUVATE OXIDASE; SUGAR;

AEROBIC FERMENTATION; ARTICLE; BACTERIAL CAPSULE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL VIRULENCE; CARBOHYDRATE TRANSPORT; CONTROLLED STUDY; CPS GENE; DEATH; EVOLUTIONARY ADAPTATION; GENE INACTIVATION; GENE MUTATION; GENETIC TRANSCRIPTION; METABOLITE; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; OXIDATIVE STRESS; OXYGENATION; PHENOTYPE; SPXB GENE; STREPTOCOCCUS PNEUMONIAE; SURVIVAL; TRANSCRIPTOMICS;

BACTERIAL CAPSULES; BACTERIAL PROTEINS; CARBOHYDRATE METABOLISM; FERMENTATION; GENE DELETION; GENE SILENCING; GLUCOSE; METABOLOME; MUTATION; OPERON; OXYGEN CONSUMPTION; PHOSPHORYLATION; PYRUVATE OXIDASE; STREPTOCOCCUS PNEUMONIAE; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

BACTERIA (MICROORGANISMS); STREPTOCOCCUS PNEUMONIAE;

EID: 84879743831     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068277     Document Type: Article

References (70)

1. Obaro S, Adegbola R, (2002) The pneumococcus: carriage, disease and conjugate vaccines. J Med Microbiol 51: 98-104. PubMed: 11863272.
2. Avery OT, Dubos R, (1931) The protective action of a specific enzyme against type III pneumococcus infection in mice. J Exp Med 54: 73-89. doi:10.1084/jem.54.1.73. PubMed: 19869903.
3. Kadioglu A, Weiser JN, Paton JC, Andrew PW, (2008) The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat Rev Microbiol 6: 288-301. doi:10.1038/nrmicro1871. PubMed: 18340341.
4. Magee AD, Yother J, (2001) Requirement for capsule in colonization by Streptococcus pneumoniae. Infect Immun 69: 3755-3761. doi:10.1128/IAI.69.6.3755-3761.2001. PubMed: 11349040.
5. 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. doi:10.1128/IAI.69.4.2309-2317.2001. PubMed: 11254588.
6. Song JH, Dagan R, Klugman KP, Fritzell B, (2012) The relationship between pneumococcal serotypes and antibiotic resistance. Vaccine 30: 2728-2737. doi:10.1016/j.vaccine.2012.01.091. PubMed: 22330126.
7. Iannelli F, Pearce BJ, Pozzi G, (1999) The type 2 capsule locus of Streptococcus pneumoniae. J Bacteriol 181: 2652-2654. PubMed: 10198036.
8. Hardy GG, Caimano MJ, Yother J, (2000) Capsule biosynthesis and basic metabolism in Streptococcus pneumoniae are linked through the cellular phosphoglucomutase. J Bacteriol 182: 1854-1863. doi:10.1128/JB.182.7.1854-1863.2000. PubMed: 10714989.
9. Bentley SD, Aanensen DM, Mavroidi A, Saunders D, Rabbinowitsch E, et al. (2006) Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLOS Genet 2: e31. doi:10.1371/journal.pgen.0020031. PubMed: 16532061.
10. 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. doi:10.1086/383352. PubMed: 15122528.
11. 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. PubMed: 12101293.
12. Hammerschmidt S, Wolff S, Hocke A, Rosseau S, Müller E, et al. (2005) Illustration of pneumococcal polysaccharide capsule during adherence and invasion of epithelial cells. Infect Immun 73: 4653-4667. doi:10.1128/IAI.73.8.4653-4667.2005. PubMed: 16040978.
13. 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. doi:10.1086/514205. PubMed: 9466523.
14. Kim JO, Romero-Steiner S, Sørensen UB, Blom J, Carvalho M, et al. (1999) Relationship between cell surface carbohydrates and intrastrain variation on opsonophagocytosis of Streptococcus pneumoniae. Infect Immun 67: 2327-2333. PubMed: 10225891.
15. Nelson AL, Roche AM, Gould JM, Chim K, Ratner AJ, et al. (2007) Capsule enhances pneumococcal colonization by limiting mucus-mediated clearance. Infect Immun 75: 83-90. doi:10.1128/IAI.01475-06. PubMed: 17088346.
16. Overweg K, Pericone CD, Verhoef GG, Weiser JN, Meiring HD, et al. (2000) Differential protein expression in phenotypic variants of Streptococcus pneumoniae. Infect Immun 68: 4604-4610. doi:10.1128/IAI.68.8.4604-4610.2000. PubMed: 10899862.
17. Spellerberg B, Cundell DR, Sandros J, Pearce BJ, Idanpaan-Heikkila I, et al. (1996) Pyruvate oxidase, as a determinant of virulence in Streptococcus pneumoniae. Mol Microbiol 19: 803-813. doi:10.1046/j.1365-2958.1996.425954.x. PubMed: 8820650.
18. Pericone CD, Bae D, Shchepetov M, McCool T, Weiser JN, (2002) Short-sequence tandem and nontandem DNA repeats and endogenous hydrogen peroxide production contribute to genetic instability of Streptococcus pneumoniae. J Bacteriol 184: 4392-4399. doi:10.1128/JB.184.16.4392-4399.2002. PubMed: 12142409.
19. Pericone CD, Park S, Imlay JA, Weiser JN, (2003) Factors contributing to hydrogen peroxide resistance in Streptococcus pneumoniae include pyruvate oxidase (SpxB) and avoidance of the toxic effects of the fenton reaction. J Bacteriol 185: 6815-6825. doi:10.1128/JB.185.23.6815-6825.2003. PubMed: 14617646.
20. Pericone CD, Overweg K, Hermans PW, Weiser JN, (2000) Inhibitory and bactericidal effects of hydrogen peroxide production by Streptococcus pneumoniae on other inhabitants of the upper respiratory tract. Infect Immun 68: 3990-3997. doi:10.1128/IAI.68.7.3990-3997.2000. PubMed: 10858213.
21. Duane PG, Rubins JB, Weisel HR, Janoff EN, (1993) Identification of hydrogen peroxide as a Streptococcus pneumoniae toxin for rat alveolar epithelial cells. Infect Immun 61: 4392-4397. PubMed: 8406830.
22. Hirst RA, Sikand KS, Rutman A, Mitchell TJ, Andrew PW, et al. (2000) Relative roles of pneumolysin and hydrogen peroxide from Streptococcus pneumoniae in inhibition of ependymal ciliary beat frequency. Infect Immun 68: 1557-1562. doi:10.1128/IAI.68.3.1557-1562.2000. PubMed: 10678974.
23. 2 mediate brain cell apoptosis during meningitis. J Clin Invest 109: 19-27. doi:10.1172/JCI200212035. PubMed: 11781347.
24. Regev-Yochay G, Trzcinski K, Thompson CM, Lipsitch M, Malley R, (2007) SpxB is a suicide gene of Streptococcus pneumoniae and confers a selective advantage in an in vivo competitive colonization model. J Bacteriol 189: 6532-6539. doi:10.1128/JB.00813-07. PubMed: 17631628.
25. Pesakhov S, Benisty R, Sikron N, Cohen Z, Gomelsky P, et al. (2007) Effect of hydrogen peroxide production and the Fenton reaction on membrane composition of Streptococcus pneumoniae. Biochim Biophys Acta 1768: 590-597. doi:10.1016/j.bbamem.2006.12.016. PubMed: 17292324.
26. 2 produced by Streptococcus pneumoniae controls FabF activity. Biochim Biophys Acta 1801: 1098-1104. doi:10.1016/j.bbalip.2010.06.004. PubMed: 20601114.
27. Orihuela CJ, Gao G, McGee M, Yu J, Francis KP, et al. (2003) Organ-specific models of Streptococcus pneumoniae disease. Scand J Infect Dis 35: 647-652. doi:10.1080/00365540310015854. PubMed: 14620149.
28. Ramos-Montañez S, Tsui HC, Wayne KJ, Morris JL, Peters LE, et al. (2008) Polymorphism and regulation of the spxB (pyruvate oxidase) virulence factor gene by a CBS-HotDog domain protein (SpxR) in serotype 2 Streptococcus pneumoniae. Mol Microbiol 67: 729-746. PubMed: 18179423.
29. Weiser JN, Bae D, Epino H, Gordon SB, Kapoor M, et al. (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. doi:10.1128/IAI.69.9.5430-5439.2001. PubMed: 11500414.
30. Bijlsma JJ, Burghout P, Kloosterman TG, Bootsma HJ, de Jong A, et al. (2007) Development of Genomic Array Footprinting for Identification of Conditionally Essential Genes in Streptococcus pneumoniae. Appl Environ Microbiol 73: 1514-1524. doi:10.1128/AEM.01900-06. PubMed: 17261526.
31. Allegrucci M, Sauer K, (2008) Formation of Streptococcus pneumoniae non-phase-variable colony variants is due to increased mutation frequency present under biofilm growth conditions. J Bacteriol 190: 6330-6339. doi:10.1128/JB.00707-08. PubMed: 18658260.
32. Ramos-Montañez S, Kazmierczak KM, Hentchel KL, Winkler ME, (2010) Instability of ackA (acetate kinase) mutations and their effects on acetyl phosphate and ATP amounts in Streptococcus pneumoniae D39. J Bacteriol 192: 6390-6400. doi:10.1128/JB.00995-10. PubMed: 20952579.
33. Kloosterman TG, Bijlsma JJ, Kok J, Kuipers OP, (2006) To have neighbour's fare: extending the molecular toolbox for Streptococcus pneumoniae. Microbiology 152: 351-359. doi:10.1099/mic.0.28521-0. PubMed: 16436423.
34. Taniai H, Iida K, Seki M, Saito M, Shiota S, et al. (2008) Concerted action of lactate oxidase and pyruvate oxidase in aerobic growth of Streptococcus pneumoniae: role of lactate as an energy source. J Bacteriol 190: 3572-3579. doi:10.1128/JB.01882-07. PubMed: 18344365.
35. Yum DY, Lee BY, Pan JG, (1999) Identification of the yqhE and yafB genes encoding two 2, 5-diketo-D-gluconate reductases in Escherichia coli. Appl Environ Microbiol 65: 3341-3346. PubMed: 10427017.
36. Maruyama Y, Nakamichi Y, Itoh T, Mikami B, Hashimoto W, et al. (2009) Substrate specificity of streptococcal unsaturated glucuronyl hydrolases for sulfated glycosaminoglycan. J Biol Chem 284: 18059-18069. doi:10.1074/jbc.M109.005660. PubMed: 19416976.
37. Marion C, Stewart JM, Tazi MF, Burnaugh AM, Linke CM, et al. (2012) Streptococcus pneumoniae can utilize multiple sources of hyaluronic acid for growth. Infect Immun 80: 1390-1398. doi:10.1128/IAI.05756-11. PubMed: 22311922.
38. Sedewitz B, Schleifer KH, Götz F, (1984) Physiological role of pyruvate oxidase in the aerobic metabolism of Lactobacillus plantarum. J Bacteriol 160: 462-465. PubMed: 6480562.
39. Seki M, Iida K, Saito M, Nakayama H, Yoshida S, (2004) Hydrogen peroxide production in Streptococcus pyogenes: involvement of lactate oxidase and coupling with aerobic utilization of lactate. J Bacteriol 186: 2046-2051. doi:10.1128/JB.186.7.2046-2051.2004. PubMed: 15028688.
40. Goffin P, Muscariello L, Lorquet F, Stukkens A, Prozzi D, et al. (2006) Involvement of pyruvate oxidase activity and acetate production in the survival of Lactobacillus plantarum during the stationary phase of aerobic growth. Appl Environ Microbiol 72: 7933-7940. doi:10.1128/AEM.00659-06. PubMed: 17012588.
41. Lorquet F, Goffin P, Muscariello L, Baudry JB, Ladero V, et al. (2004) Characterization and functional analysis of the poxB gene, which encodes pyruvate oxidase in Lactobacillus plantarum. J Bacteriol 186: 3749-3759. doi:10.1128/JB.186.12.3749-3759.2004. PubMed: 15175288.
42. Belanger AE, Clague MJ, Glass JI, Leblanc DJ, (2004) Pyruvate oxidase is a determinant of Avery's rough morphology. J Bacteriol 186: 8164-8171. doi:10.1128/JB.186.24.8164-8171.2004. PubMed: 15576764.
43. LeMessurier KS, Ogunniyi AD, Paton JC, (2006) Differential expression of key pneumococcal virulence genes in vivo. Microbiology 152: 305-311. doi:10.1099/mic.0.28438-0. PubMed: 16436418.
44. Li-Korotky HS, Lo CY, Zeng FR, Lo D, Banks JM, (2009) Interaction of phase variation, host and pressure/gas composition: Pneumococcal gene expression of PsaA, SpxB, Ply and LytA in simulated middle ear environments. Int J Pediatr Otorhinolaryngol, 73: 1417-22. PubMed: 19682756.
45. Yother J, (2011) Capsules of Streptococcus pneumoniae and other bacteria: paradigms for polysaccharide biosynthesis and regulation. Annu Rev Microbiol 65: 563-581. doi:10.1146/annurev.micro.62.081307.162944. PubMed: 21721938.
46. Carvalho SM, Kloosterman TG, Kuipers OP, Neves AR, (2011) CcpA ensures optimal metabolic fitness of Streptococcus pneumoniae. PLOS ONE 6: e26707. doi:10.1371/journal.pone.0026707. PubMed: 22039538.
47. Zheng L, Chen Z, Itzek A, Ashby M, Kreth J, (2011) Catabolite control protein A controls hydrogen peroxide production and cell death in Streptococcus sanguinis. J Bacteriol 193: 516-526. doi:10.1128/JB.01131-10. PubMed: 21036992.
48. Zheng L, Itzek A, Chen Z, Kreth J, (2011) Environmental influences on competitive hydrogen peroxide production in Streptococcus gordonii. Appl Environ Microbiol 77: 4318-4328. doi:10.1128/AEM.00309-11. PubMed: 21571883.
49. Lanie JA, Ng WL, Kazmierczak KM, Andrzejewski TM, Davidsen TM, et al. (2007) Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J Bacteriol 189: 38-51. doi:10.1128/JB.01148-06. PubMed: 17041037.
50. Bidossi A, Mulas L, Decorosi F, Colomba L, Ricci S, et al. (2012) A functional genomics approach to establish the complement of carbohydrate transporters in Streptococcus pneumoniae. PLOS ONE 7: e33320. doi:10.1371/journal.pone.0033320. PubMed: 22428019.
51. Burnaugh AM, Frantz LJ, King SJ, (2008) Growth of Streptococcus pneumoniae on human glycoconjugates is dependent upon the sequential activity of bacterial exoglycosidases. J Bacteriol 190: 221-230. doi:10.1128/JB.01251-07. PubMed: 17981977.
52. Terra VS, Homer KA, Rao SG, Andrew PW, Yesilkaya H, (2010) Characterization of novel beta-galactosidase activity that contributes to glycoprotein degradation and virulence in Streptococcus pneumoniae. Infect Immun 78: 348-357. doi:10.1128/IAI.00721-09. PubMed: 19841081.
53. Philips BJ, Meguer JX, Redman J, Baker EH, (2003) Factors determining the appearance of glucose in upper and lower respiratory tract secretions. Intensive Care Med 29: 2204-2210. doi:10.1007/s00134-003-1961-2. PubMed: 14647890.
54. Wolfe AJ, (2010) Physiologically relevant small phosphodonors link metabolism to signal transduction. Curr Opin Microbiol 13: 204-209. doi:10.1016/j.mib.2010.01.002. PubMed: 20117041.
55. Price CE, Zeyniyev A, Kuipers OP, Kok J, (2011) From meadows to milk to mucosa- adaptation of Streptococcus and Lactococcus species to their nutritional environments. FEMS Microbiol Rev. PubMed: 22212109.
56. Neves AR, Pool WA, Kok J, Kuipers OP, Santos H, (2005) Overview on sugar metabolism and its control in Lactococcus lactis- the input from in vivo NMR. FEMS Microbiol Rev 29: 531-554. doi:10.1016/j.fmrre.2005.04.005. PubMed: 15939503.
57. Terzaghi BE, Sandine WE, (1975) Improved Medium for Lactic Streptococci and Their Bacteriophages. Appl Microbiol 29: 807-813. PubMed: 16350018.
58. Gualdi L, Hayre JK, Gerlini A, Bidossi A, Colomba L, et al. (2012) Regulation of neuraminidase expression in Streptococcus pneumoniae. BMC Microbiol 12: 200. doi:10.1186/1471-2180-12-200. PubMed: 22963456.
59. Maguin E, Prévost H, Ehrlich SD, Gruss A, (1996) Efficient insertional mutagenesis in lactococci and other gram-positive bacteria. J Bacteriol 178: 931-935. PubMed: 8550537.
60. Karlyshev Pallen MJ, Wren BW, (2000) Single Primer PCR procedure for Rapid Identification of Transposon Insertion Sites. BioTechniques 28: 1078-1082. PubMed: 10868271.
61. Iyer R, Baliga NS, Camilli A, (2005) Catabolite control protein A (CcpA) contributes to virulence and regulation of sugar metabolism in Streptococcus pneumoniae. J Bacteriol 187: 8340-8349. doi:10.1128/JB.187.24.8340-8349.2005. PubMed: 16321938.
62. Neef J, Andisi VF, Kim KS, Kuipers OP, Bijlsma JJ, (2011) Deletion of a cation transporter promotes lysis in Streptococcus pneumoniae. Infect Immun 79: 2314-2323. doi:10.1128/IAI.00677-10. PubMed: 21422174.
63. Meiattini F, (1988) Inorganic peroxides. In: Bergmeyer H, Grabl M, Bergmeyer J, eds. Methods of enzymatic analysis. Weinheim: Verlag Chemie. pp. pp. 566-571.
64. 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. doi:10.1073/pnas.0602148103. PubMed: 16707578.
65. Ramos A, Boels IC, de Vos WM, Santos H, (2001) Relationship between glycolysis and exopolysaccharide biosynthesis in Lactococcus lactis. Appl Environ Microbiol 67: 33-41. doi:10.1128/AEM.67.1.33-41.2001. PubMed: 11133425.
66. Blumenkrantz N, Asboe-Hansen G, (1973) New method for quantitative determination of uronic acids. Anal Biochem 54: 484-489. doi:10.1016/0003-2697(73)90377-1. PubMed: 4269305.
67. Carvalho SM, Kuipers OP, Neves AR, (2013) Environmental and nutritional factors that affect growth and metabolism of the pneumococcal serotype 2 strain D39 and its nonencapsulated derivative strain r6. PLOS ONE 8: e58492. doi:10.1371/journal.pone.0058492. PubMed: 23505518.
68. 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. doi:10.1084/jem.79.2.137. PubMed: 19871359.
69. Tettelin H, Nelson KE, Paulsen IT, Eisen JA, Read TD, et al. (2001) Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293: 498-506. doi:10.1126/science.1061217. PubMed: 11463916.
70. Sanders JW, Venema G, Kok J, Leenhouts K, (1998) Identification of a sodium chloride-regulated promoter in Lactococcus lactis by single-copy chromosomal fusion with a reporter gene. Mol Gen Genet 257: 681-685. doi:10.1007/s004380050697. PubMed: 9604892.