ManLMN is a glucose transporter and central metabolic regulator in Streptococcus pneumoniae

Molecular Microbiology

Volumn 102, Issue 3, 2016, Pages 467-487

  Fleming, Eleanor ^a,b   Camilli, Andrew ^a,b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATABOLITE CONTROL PROTEIN A; GLUCOSE; GLUCOSE TRANSPORTER; LACTOSE; MANLMN PROTEIN; SMRC PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR; BACTERIAL PROTEIN; DNA BINDING PROTEIN; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE; REPRESSOR PROTEIN;

ARTICLE; BACTERIAL GROWTH; CARBOHYDRATE METABOLISM; CARBON CATABOLITE REPRESSION; CATABOLITE REPRESSION; CONTROLLED STUDY; GENE EXPRESSION; GENE INDUCTION; NONHUMAN; OPERON; PHOSPHOENOLPYRUVATE DEPENDENT PHOSPHOTRANSFERASE SYSTEM; PRIORITY JOURNAL; STREPTOCOCCUS PNEUMONIAE; TRANSCRIPTION REGULATION; GENETICS; HUMAN; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CARBOHYDRATE METABOLISM; CATABOLITE REPRESSION; DNA-BINDING PROTEINS; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; HUMANS; OPERON; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE SYSTEM; REPRESSOR PROTEINS; STREPTOCOCCUS PNEUMONIAE;

EID: 84982292346     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13473     Document Type: Article

References (61)

1. Abranches, J., Chen, Y.Y.M., and Burne, R.A. (2003) Characterization of Streptococcus mutans strains deficient in EIIABMan of the sugar phosphotransferase system. Appl Environ Microbiol 69: 4760–4769.
2. Abranches, J., Candella, M.M., Wen, Z.T., Baker, H.V., and Burne, R.A. (2006) Different roles of EIIABMan and EIIGlc in regulation of energy metabolism, biofilm development, and competence in Streptococcus mutans. J Bacteriol 188: 3748–3756.
3. Aké, F.M.D., Joyet, P., Deutscher, J., and Milohanic, E. (2011) Mutational analysis of glucose transport regulation and glucose-mediated virulence gene repression in Listeria monocytogenes. Mol Microbiol 81: 274–293.
4. Barriere, C., Veiga-da-Cunha, M., Pons, N., Guedon, E., van Hijum, S.A., Kok, J., et al. (2005) Fructose utilization in Lactococcus lactis as a model for low-GC gram-positive bacteria: its regulator, signal, and DNA-binding site. J Bacteriol 187: 3752–3761.
5. Bertram, R., Rigali, S., Wood, N., Lulko, A.T., Kuipers, O.P., and Titgemeyer, F. (2011) Regulon of the N-acetylglucosamine utilization regulator NagR in Bacillus subtilis. J Bacteriol 193: 3525–3536.
6. Bidossi, A., Mulas, L., Decorosi, F., Colomba, L., Ricci, S., Pozzi, G., et al. (2012) A functional genomics approach to establish the complement of carbohydrate transporters in Streptococcus pneumoniae. PLoS One 7: e33320.
7. Bricker, A., and Camilli, A. (1999) Transformation of a type 4 encapsulated strain of Streptococcus pneumoniae. FEMS Microbiol Lett 172: 131–135.
8. Buckwalter, C.M., and King, S.J. (2012) Pneumococcal carbohydrate transport: food for thought. Trends Microbiol 20: 517–522.
9. Burnaugh, A.M., Frantz, L.J., and King, S.J. (2008) Growth of Streptococcus pneumoniae on human glycoconjugates is dependent upon the sequential activity of bacterial exoglycosidases. J Bacteriol 190: 221–230.
10. Carvalho, S.M., Kloosterman, T.G., Kuipers, O.P., and Neves, A.R. (2011) CcpA ensures optimal metabolic fitness of Streptococcus pneumoniae. PLoS One 6: e26707.
11. Chapuy-Regaud, S., Ogunniyi, A.D., Diallo, N., Huet, Y., Desnottes, J.F., Paton, J.C., et al. (2003) RegR, a global LacI/GalR family regulator, modulates virulence and competence in Streptococcus pneumoniae. Infect Immun 71: 2615–2625.
12. Cheng, W., Wang, L., Jiang, Y.L., Bai, X.H., Chu, J., Li, Q., et al. (2012) Structural insights into the substrate specificity of Streptococcus pneumoniae β(1,3)-galactosidase BgaC. J Biol Chem 287: 22910–22918.
13. Dalia, A.B., Standish, A.J., and Weiser, J.N. (2010) Three surface exoglycosidases from Streptococcus pneumoniae, NanA, BgaA, and StrH, promote resistance to opsonophagocytic killing by human neutrophils. Infect Immun 78: 2108–2116.
14. Deutscher, J., Francke, C., and Postma, P.W. (2006) How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol Mol Biol Rev 70: 939–1031.
15. Fleming, E., Lazinski, D.W., and Camilli, A. (2015) Carbon catabolite repression by seryl phosphorylated HPr is essential to Streptococcus pneumoniae in carbohydrate rich environments. Mol Microbiol 97: 360–380.
16. Halfmann, A., Kovács, M., Hakenbeck, R., and Brückner, R. (2007) Identification of the genes directly controlled by the response regulator CiaR in Streptococcus pneumoniae: five out of 15 promoters drive expression of small non-coding RNAs. Mol Microbiol 66: 110–126.
17. Halfmann, A., Schnorpfeil, A., Müller, M., Marx, P., Günzler, U., Hakenbeck, R., and Brückner, R. (2011) Activity of the two-component regulatory system CiaRH in Streptococcus pneumoniae R6. J Mol Microbiol Biotechnol 20: 96–104.
18. Hava, D.L., and Camilli, A. (2002) Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. Mol Microbiol 45: 1389–1405.
19. Hava, D.L., LeMieux, J., and Camilli, A. (2003) From nose to lung: the regulation behind Streptococcus pneumoniae virulence factors. Mol Microbiol 50: 1103–1110.
20. Horton, R.M., Cai, Z.L., Ho, S.N., and Pease, L.R. (1990) Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 8: 528–535.
21. Iyer, R., and Camilli, A. (2007) Sucrose metabolism contributes to in vivo fitness of Streptococcus pneumoniae. Mol Microbiol 66: 1–13.
22. Iyer, R., Baliga, N.S., and Camilli, A. (2005) Catabolite control protein a (CcpA) contributes to virulence and regulation of sugar metabolism in Streptococcus pneumoniae. J Bacteriol 187: 8340–8349.
23. Jahreis, K., Pimentel-Schmitt, E.F., Brückner, R., and Titgemeyer, F. (2008) Ins and outs of glucose transport systems in eubacteria. FEMS Microbiol Rev 32: 891–907.
24. Jeong, J.K., Kwon, O., Lee, Y.M., Oh, D.B., Lee, J.M., Kim, S., et al. (2009) Characterization of the Streptococcus pneumoniae BgaC protein as a novel surface beta-galactosidase with specific hydrolysis activity for the Galbeta1-3GlcNAc moiety of oligosaccharides. J Bacteriol 191: 3011–3023.
25. Kaufman, G.E., and Yother, J. (2007) CcpA-dependent and -independent control of beta-galactosidase expression in Streptococcus pneumoniae occurs via regulation of an upstream phosphotransferase system-encoding operon. J Bacteriol 189: 5183–5192.
26. Kawai, Y., Moriya, S., and Ogasawara, N. (2003) Identification of a protein, YneA, responsible for cell division suppression during the SOS response in Bacillus subtilis. Mol Microbiol 47: 1113–1122.
27. King, S.J. (2010) Pneumococcal modification of host sugars: a major contributor to colonization of the human airway? Mol Oral Microbiol 25: 15–24.
28. King, S.J., Hippe, K.R., Gould, J.M., Bae, D., Peterson, S., Cline, R.T., et al. (2004) Phase variable desialylation of host proteins that bind to Streptococcus pneumoniae in vivo and protect the airway. Mol Microbiol 54: 159–171.
29. King, S.J., Hippe, K.R., and Weiser, J.N. (2006) Deglycosylation of human glycoconjugates by the sequential activities of exoglycosidases expressed by Streptococcus pneumoniae. Mol Microbiol 59: 961–974.
30. Kloosterman, T.G., Bijlsma, J.J.E., Kok, J., and Kuipers, O.P. (2006) To have neighbour's fare: extending the molecular toolbox for Streptococcus pneumoniae. Microbiology 152: 351–359.
31. Lamblin, G., Degroote, S., Perini, J.M., Delmotte, P., Scharfman, A., Davril, M., et al. (2001) Human airway mucin glycosylation: a combinatory of carbohydrate determinants which vary in cystic fibrosis. Glycoconj J 18: 661–684.
32. Lau, G.W., Haataja, S., Lonetto, M., Kensit, S.E., Marra, A., Bryant, A.P., et al. (2001) A functional genomic analysis of type 3 Streptococcus pneumoniae virulence. Mol Microbiol 40: 555–571.
33. Leprohon, P., Gingras, H., Ouennane, S., Moineau, S., and Ouellette, M. (2015) A genomic approach to understand interactions between Streptococcus pneumoniae and its bacteriophages. BMC Genomics 16: 972.
34. Limoli, D.H., Sladek, J.A., Fuller, L.A., Singh, A.K., and King, S.J. (2011) BgaA acts as an adhesin to mediate attachment of some pneumococcal strains to human epithelial cells. Microbiology 157: 2369–2381.
35. Lorca, G., Chung, Y., and Barabote, R. (2005) Catabolite repression and activation in Bacillus subtilis: dependency on CcpA, HPr, and HprK. J Bacteriol 187: 7826–7839.
36. Mahdi, L.K., Ebrahimie, E., Adelson, D.L., Paton, J.C., and Ogunniyi, A.D. (2013) A transcription factor contributes to pathogenesis and virulence in Streptococcus pneumoniae. PLoS One 8: e70862.
37. Mahdi, L.K., Deihimi, T., Zamansani, F., Fruzangohar, M., Adelson, D.L., Paton, J.C., et al. (2014) A functional genomics catalogue of activated transcription factors during pathogenesis of pneumococcal disease. BMC Genomics 15: 769.
38. Marion, C., Aten, A.E., Woodiga, S.A., and King, S.J. (2011) Identification of an ATPase, MsmK, which energizes multiple carbohydrate ABC transporters in Streptococcus pneumoniae. Infect Immun 79: 4193–4200.
39. Marx, P., Nuhn, M., Kovács, M., Hakenbeck, R., and Brückner, R. (2010) Identification of genes for small non-coding RNAs that belong to the regulon of the two-component regulatory system CiaRH in Streptococcus. BMC Genomics 11: 661.
40. Mascher, T., Zahner, D., Merai, M., Balmelle, N., de Saizieu, A.B., and Hakenbeck, R. (2003) The Streptococcus pneumoniae cia regulon: CiaR target sites and transcription profile analysis. Society 185: 60–70.
41. Monzon, M.E., Casalino-Matsuda, S.M., and Forteza, R.M. (2006) Identification of glycosaminoglycans in human airway secretions. Am J Respir Cell Mol Biol 34: 135–141.
42. Moye, Z.D., Burne, R.A., and Zeng, L. (2014a) Uptake and metabolism of N-acetylglucosamine and glucosamine by Streptococcus mutans. Appl Environ Microbiol 80: 5053–5067.
43. Moye, Z.D., Zeng, L., and Burne, R.A. (2014b) Modification of gene expression and virulence traits in Streptococcus mutans in response to carbohydrate availability. Appl Environ Microbiol 80: 972–985.
44. van Opijnen, T., and Camilli, A. (2012) A fine scale phenotype-genotype virulence map of a bacterial pathogen. Genome Res 22: 2541–2551.
45. Rosenow, C., Maniar, M., and Trias, J. (1999) Regulation of the alpha-galactosidase activity in Streptococcus pneumoniae: characterization of the raffinose utilization system. Genome Res 9: 1189–1197.
46. Shainheit, M.G., Valentino, M.D., Gilmore, M.S., and Camilli, A. (2015) Mutations in pneumococcal cpsE generated via in vitro serial passaging reveal a potential mechanism of reduced encapsulation utilized by a conjunctival isolate. J Bacteriol 197: 1781–1791.
47. Singh, A.K., Pluvinage, B., Higgins, M.A., Dalia, A.B., Woodiga, S.A., Flynn, M., et al. (2014) Unravelling the multiple functions of the architecturally intricate Streptococcus pneumoniae β-galactosidase, BgaA. PLoS Pathog 10: e1004364.
48. Tettelin, H., Nelson, K.E., Paulsen, I.T., Eisen, J.A., Read, T.D., Peterson, S., et al. (2001) Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293: 498–506.
49. Vadeboncoeur, C., and Gauthier, L. (1987) The phosphoenolpyruvate: sugar phosphotransferase system of Streptococcus salivarius. Identification of a IIIManL protein. Can J Microbiol 33: 118–122.
50. Vadeboncoeur, C., and Pelletier, M. (1997) The phosphoenolpyruvate:sugar phosphotransferase system of oral streptococci and its role in the control of sugar metabolism. FEMS Microbiol Rev 19: 187–207.
51. Vadeboncoeur, C., Bourgeau, G., Mayrand, D., and Trahan, L. (1983) Control of sugar utilization in the oral bacteria Streptococcus salivarius and Streptococcus sanguis by the phosphoenolpyruvate: glucose phosphotransferase system. Arch Oral Biol 28: 123–131.
52. Vadeboncoeur, C., Frenette, M., and Lortie, L. (2000) Regulation of the pts operon in low G+C gram-positive bacteria. J Mol Microbiol Biotechnol 2: 483–490.
53. Warner, J.B., and Lolkema, J.S. (2003) CcpA-dependent carbon catabolite repression in bacteria. Microbiol Mol Biol Rev 67: 475–490.
54. Wen, Z.T., Browngardt, C., and Burne, R.A. (2001) Characterization of two operons that encode components of fructose-specific enzyme II of the sugar:phosphotransferase system of Streptococcus mutans. FEMS Microbiol Lett 205: 337–342.
55. Weng, L., Biswas, I., and Morrison, D.A. (2009) A self-deleting Cre-lox-ermAM Cassette, CHESHIRE, for marker-less gene deletion in Streptococcus pneumoniae. J Microbiol Methods 79: 353.
56. White, R. (1968) Control of amino sugar metabolism in Escherichia coli and isolation of mutants unable to degrade amino sugars. Biochem J 106: 847–858.
57. Yesilkaya, H., Manco, S., Kadioglu, A., Terra, V.S., and Andrew, P.W. (2008) The ability to utilize mucin affects the regulation of virulence gene expression in Streptococcus pneumoniae. FEMS Microbiol Lett 278: 231–235.
58. Yesilkaya, H., Spissu, F., Carvalho, S.M., Terra, V.S., Homer, K.A., Benisty, R., et al. (2009) Pyruvate formate lyase is required for pneumococcal fermentative metabolism and virulence. Infect Immun 77: 5418–5427.
59. Zähner, D., and Hakenbeck, R. (2000) The Streptococcus pneumoniae beta-galactosidase is a surface protein. J Bacteriol 182: 5919–5921.
60. Zeng, L., and Burne, R.A. (2008) Multiple sugar: phosphotransferase system permeases participate in catabolite modification of gene expression in Streptococcus mutans. Mol Microbiol 70: 197–208.
61. Zúñiga, M., Comas, I., Linaje, R., Monedero, V., Yebra, M.J., Esteban, C.D., et al. (2005) Horizontal gene transfer in the molecular evolution of mannose PTS transporters. Mol Biol Evol 22: 1673–1685.