Induction of a quorum sensing pathway by environmental signals enhances group A streptococcal resistance to lysozyme

Molecular Microbiology

Volumn 97, Issue 6, 2015, Pages 1097-1113

  Chang, Jennifer C ^a   Jimenez, Juan Cristobal ^b   Federle, Michael J ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARBON; LYSOZYME; MANNOSE; MULTIPROTEIN COMPLEX; PHEROMONE; RGG2 PROTEIN; RGG3 PROTEIN; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; METAL;

ARTICLE; BACTERIAL STRAIN; CARBON SOURCE; CELL COMMUNICATION; CONTROLLED STUDY; ENVIRONMENTAL IMPACT; HOST RESISTANCE; NONHUMAN; NUTRIENT AVAILABILITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUORUM SENSING; STREPTOCOCCUS GROUP A; STREPTOCOCCUS PYOGENES; STRESS; ANTIBIOTIC RESISTANCE; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; SIGNAL TRANSDUCTION;

ANTI-INFECTIVE AGENTS; BACTERIAL PROTEINS; DRUG RESISTANCE, BACTERIAL; METALS; MURAMIDASE; PHEROMONES; QUORUM SENSING; SIGNAL TRANSDUCTION; STREPTOCOCCUS PYOGENES;

EID: 84941191990     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13088     Document Type: Article

References (73)

1. Abranches, J., Chen, Y.Y., and Burne, R.A. (2003) Characterization of Streptococcus mutans strains deficient in EIIAB Man of the sugar phosphotransferase system. Appl Environ Microbiol 69: 4760-4769.
2. Aggarwal, C., Jimenez, J.C., Nanavati, D., and Federle, M.J. (2014) Multiple length peptide-pheromone variants produced by Streptococcus pyogenes directly bind Rgg proteins to confer transcriptional regulation. J Biol Chem 289: 22427-22436.
3. Aggarwal, C., Jimenez, J.C., Lee, H., Chlipala, G.E., Ratia, K., and Federle, M.J. (2015) Identification of quorum-sensing inhibitors disrupting signaling between rgg and short hydrophobic peptides in streptococci. MBio 6: e00393-15.
4. Almengor, A.C., Kinkel, T.L., Day, S.J., and McIver, K.S. (2007) The catabolite control protein CcpA binds to Pmga and influences expression of the virulence regulator Mga in the Group A streptococcus. J Bacteriol 189: 8405-8416.
5. Bates, C.S., Montanez, G.E., Woods, C.R., Vincent, R.M., and Eichenbaum, Z. (2003) Identification and characterization of a Streptococcus pyogenes operon involved in binding of hemoproteins and acquisition of iron. Infect Immun 71: 1042-1055.
6. Bates, C.S., Toukoki, C., Neely, M.N., and Eichenbaum, Z. (2005) Characterization of MtsR, a new metal regulator in group A streptococcus, involved in iron acquisition and virulence. Infect Immun 73: 5743-5753.
7. Berkelman, R.L., Martin, D., Graham, D.R., Mowry, J., Freisem, R., Weber, J.A., etal. (1982) Streptococcal wound infections caused by a vaginal carrier. JAMA 247: 2680-2682.
8. Bidossi, A., Mulas, L., Decorosi, F., Colomba, L., Ricci, S., Pozzi, G., etal. (2012) A functional genomics approach to establish the complement of carbohydrate transporters in Streptococcus pneumoniae. PLoS ONE 7: e33320.
9. Buckwalter, C.M., and King, S.J. (2012) Pneumococcal carbohydrate transport: food for thought. Trends Microbiol 20: 517-522.
10. 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.
11. Chang, J.C., LaSarre, B., Jimenez, J.C., Aggarwal, C., and Federle, M.J. (2011) Two group A streptococcal peptide pheromones act through opposing Rgg regulators to control biofilm development. PLoS Pathog 7: e1002190.
12. Chaussee, M.S., Ajdic, D., and Ferretti, J.J. (1999) The rgg gene of Streptococcus pyogenes NZ131 positively influences extracellular SPE B production. Infect Immun 67: 1715-1722.
13. Chaussee, M.S., Sylva, G.L., Sturdevant, D.E., Smoot, L.M., Graham, M.R., Watson, R.O., and Musser, J.M. (2002) Rgg influences the expression of multiple regulatory loci to coregulate virulence factor expression in Streptococcus pyogenes. Infect Immun 70: 762-770.
14. Cochu, A., Vadeboncoeur, C., Moineau, S., and Frenette, M. (2003) Genetic and biochemical characterization of the phosphoenolpyruvate:glucose/mannose phosphotransferase system of Streptococcus thermophilus. Appl Environ Microbiol 69: 5423-5432.
15. Cole, J.N., Aziz, R.K., Kuipers, K., Timmer, A.M., Nizet, V., and van Sorge, N.M. (2012) A conserved UDP-glucose dehydrogenase encoded outside the hasABC operon contributes to capsule biogenesis in group A Streptococcus. J Bacteriol 194: 6154-6161.
16. Cook, L.C., LaSarre, B., and Federle, M.J. (2013) Interspecies communication among commensal and pathogenic streptococci. MBio 4: e00382-13.
17. Davis, K.M., and Weiser, J.N. (2011) Modifications to the peptidoglycan backbone help bacteria to establish infection. Infect Immun 79: 562-570.
18. Dei, M., Di Maggio, F., Di Paolo, G., and Bruni, V. (2010) Vulvovaginitis in childhood. Best Pract Res Clin Obstet Gynaecol 24: 129-137.
19. Deutscher, J., Ake, F.M., Derkaoui, M., Zebre, A.C., Cao, T.N., Bouraoui, H., etal. (2014) The bacterial phosphoenolpyruvate:carbohydrate phosphotransferase system: regulation by protein phosphorylation and phosphorylation-dependent protein-protein interactions. Microbiol Mol Biol Rev 78: 231-256.
20. Durmaz, R., Durmaz, B., Bayraktar, M., Ozerol, I.H., Kalcioglu, M.T., Aktas, E., and Cizmeci, Z. (2003) Prevalence of group A streptococcal carriers in asymptomatic children and clonal relatedness among isolates in Malatya, Turkey. J Clin Microbiol 41: 5285-5287.
21. Freter, R. (1983) Mechanisms that control the microflora in the large intestine. In Human Intestinal Microflora in Health and Disease. Hentges, D.J. (ed.). New York: Academic Press, pp. 33-54.
22. Gauthier, L., Bourassa, S., Brochu, D., and Vadeboncoeur, C. (1990) Control of sugar utilization in oral streptococci. Properties of phenotypically distinct 2-deoxyglucose-resistant mutants of Streptococcus salivarius. Oral Microbiol Immunol 5: 352-359.
23. Gera, K., Le, T., Jamin, R., Eichenbaum, Z., and McIver, K.S. (2014) The phosphoenolpyruvate phosphotransferase system in group A Streptococcus acts to reduce streptolysin S activity and lesion severity during soft tissue infection. Infect Immun 82: 1192-1204.
24. Gorke, B., and Stulke, J. (2008) Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 6: 613-624.
25. Graham, M.R., Virtaneva, K., Porcella, S.F., Barry, W.T., Gowen, B.B., Johnson, C.R., etal. (2005) Group A Streptococcus transcriptome dynamics during growth in human blood reveals bacterial adaptive and survival strategies. Am J Pathol 166: 455-465.
26. Graham, M.R., Virtaneva, K., Porcella, S.F., Gardner, D.J., Long, R.D., Welty, D.M., etal. (2006) Analysis of the transcriptome of group A Streptococcus in mouse soft tissue infection. Am J Pathol 169: 927-942.
27. Hammerstrom, T.G., Horton, L.B., Swick, M.C., Joachimiak, A., Osipiuk, J., and Koehler, T.M. (2015) Crystal structure of Bacillus anthracis virulence regulator AtxA and effects of phosphorylated histidines on multimerization and activity. Mol Microbiol 95: 426-441.
28. Hanks, T.S., Liu, M., McClure, M.J., Fukumura, M., Duffy, A., and Lei, B. (2006) Differential regulation of iron- and manganese-specific MtsABC and heme-specific HtsABC transporters by the metalloregulator MtsR of group A Streptococcus. Infect Immun 74: 5132-5139.
29. Hoffmann, S. (1985) The throat carrier rate of group A and other beta hemolytic streptococci among patients in general practice. Acta Pathol Microbiol Immunol Scand [B] 93: 347-351.
30. Hollands, A., Aziz, R.K., Kansal, R., Kotb, M., Nizet, V., and Walker, M.J. (2008) A naturally occurring mutation in ropB suppresses SpeB expression and reduces M1T1 group A streptococcal systemic virulence. PLoS ONE 3: e4102.
31. Hondorp, E.R., Hou, S.C., Hause, L.L., Gera, K., Lee, C.E., and McIver, K.S. (2013) PTS phosphorylation of Mga modulates regulon expression and virulence in the group A streptococcus. Mol Microbiol 88: 1176-1193.
32. Hood, M.I., and Skaar, E.P. (2012) Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol 10: 525-537.
33. Hoover, S.E., Perez, A.J., Tsui, H.C., Sinha, D., Smiley, D.L., DiMarchi, R.D., etal. (2015) A new quorum-sensing system (TprA/PhrA) for Streptococcus pneumoniae D39 that regulates a lantibiotic biosynthesis gene cluster. Mol Microbiol doi: 10.1111/mmi.13029.
34. Howell-Adams, B., and Seifert, H.S. (2000) Molecular models accounting for the gene conversion reactions mediating gonococcal pilin antigenic variation. Mol Microbiol 37: 1146-1158.
35. Janulczyk, R., Pallon, J., and Bjorck, L. (1999) Identification and characterization of a Streptococcus pyogenes ABC transporter with multiple specificity for metal cations. Mol Microbiol 34: 596-606.
36. Janulczyk, R., Ricci, S., and Bjorck, L. (2003) MtsABC is important for manganese and iron transport, oxidative stress resistance, and virulence of Streptococcus pyogenes. Infect Immun 71: 2656-2664.
37. Kehl-Fie, T.E., and Skaar, E.P. (2010) Nutritional immunity beyond iron: a role for manganese and zinc. Curr Opin Chem Biol 14: 218-224.
38. Keim, N.L., Levin, R.J., and Havel, P.J. (2005) Carbohydrates. In Modern Nutrition in Health and Disease. Shils, M.E., Ross, A.C., Caballero, B., and Cousins, R.J. (eds). Baltimore: Lippincott, Williams, and Wilkins, pp. 62-82.
39. King, S.J. (2010) Pneumococcal modification of host sugars: a major contributor to colonization of the human airway? Mol Oral Microbiol 25: 15-24.
40. Kizy, A.E., and Neely, M.N. (2009) First Streptococcus pyogenes signature-tagged mutagenesis screen identifies novel virulence determinants. Infect Immun 77: 1854-1865.
41. Kovacs, M., Halfmann, A., Fedtke, I., Heintz, M., Peschel, A., Vollmer, W., etal. (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.
42. Kristian, S.A., Datta, V., Weidenmaier, C., Kansal, R., Fedtke, I., Peschel, A., etal. (2005) D-alanylation of teichoic acids promotes group a streptococcus antimicrobial peptide resistance, neutrophil survival, and epithelial cell invasion. J Bacteriol 187: 6719-6725.
43. Lasarre, B., Aggarwal, C., and Federle, M.J. (2013) Antagonistic Rgg regulators mediate quorum sensing via competitive DNA binding in Streptococcus pyogenes. MBio 3: e00333-12.
44. LaSarre, B., Chang, J.C., and Federle, M.J. (2013) Redundant group a streptococcus signaling peptides exhibit unique activation potentials. J Bacteriol 195: 4310-4318.
45. Le Breton, Y., Mistry, P., Valdes, K.M., Quigley, J., Kumar, N., Tettelin, H., and McIver, K.S. (2013) Genome-wide identification of genes required for fitness of group A Streptococcus in human blood. Infect Immun 81: 862-875.
46. Lei, B., Liu, M., Voyich, J.M., Prater, C.I., Kala, S.V., DeLeo, F.R., and Musser, J.M. (2003) Identification and characterization of HtsA, a second heme-binding protein made by Streptococcus pyogenes. Infect Immun 71: 5962-5969.
47. Lortie, L.A., Pelletier, M., Vadeboncoeur, C., and Frenette, M. (2000) The gene encoding IIAB(Man)L in Streptococcus salivarius is part of a tetracistronic operon encoding a phosphoenolpyruvate: mannose/glucose phosphotransferase system. Microbiology 146 (Part 3): 677-685.
48. Lyon, W.R., Gibson, C.M., and Caparon, M.G. (1998) A role for trigger factor and an rgg-like regulator in the transcription, secretion and processing of the cysteine proteinase of Streptococcus pyogenes. EMBO J 17: 6263-6275.
49. Ma, Y., Bryant, A.E., Salmi, D.B., McIndoo, E., and Stevens, D.L. (2009) vfr, a novel locus affecting cysteine protease production in Streptococcus pyogenes. J Bacteriol 191: 3189-3194.
50. McKee, W.M., Di Caprio, J.M., Roberts, C.E., Jr, and Sherris, J.C. (1966) Anal carriage as the probable source of a streptococcal epidemic. Lancet 2: 1007-1009.
51. Martin, J.M., Green, M., Barbadora, K.A., and Wald, E.R. (2004) Group A streptococci among school-aged children: clinical characteristics and the carrier state. Pediatrics 114: 1212-1219.
52. Mashburn-Warren, L., Morrison, D.A., and Federle, M.J. (2010) A novel double-tryptophan peptide pheromone controls competence in Streptococcus spp. via an Rgg regulator. Mol Microbiol 78: 589-606.
53. Mashburn-Warren, L., Morrison, D.A., and Federle, M.J. (2012) The cryptic competence pathway in Streptococcus pyogenes is controlled by a peptide pheromone. J Bacteriol 194: 4589-4600.
54. Mogielnicki, N.P., Schwartzman, J.D., and Elliott, J.A. (2000) Perineal group A streptococcal disease in a pediatric practice. Pediatrics 106: 276-281.
55. Montanez, G.E., Neely, M.N., and Eichenbaum, Z. (2005) The streptococcal iron uptake (Siu) transporter is required for iron uptake and virulence in a zebrafish infection model. Microbiology 151: 3749-3757.
56. Moye, Z.D., Burne, R.A., and Zeng, L. (2014) Uptake and metabolism of N-acetylglucosamine and glucosamine by Streptococcus mutans. Appl Environ Microbiol 80: 5053-5067.
57. Ng, K.M., Ferreyra, J.A., Higginbottom, S.K., Lynch, J.B., Kashyap, P.C., Gopinath, S., etal. (2013) Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502: 96-99.
58. Perez-Miranda, S., Cabirol, N., George-Tellez, R., Zamudio-Rivera, L.S., and Fernandez, F.J. (2007) O-CAS, a fast and universal method for siderophore detection. J Microbiol Methods 70: 127-131.
59. van de Rijn, I., and Kessler, R.E. (1980) Growth characteristics of group A streptococci in a new chemically defined medium. Infect Immun 27: 444-448.
60. Schwyn, B., and Neilands, J.B. (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160: 47-56.
61. Shaikh, N., Leonard, E., and Martin, J.M. (2010) Prevalence of streptococcal pharyngitis and streptococcal carriage in children: a meta-analysis. Pediatrics 126: e557-e564.
62. Shelburne, S.A., 3rd, Sumby, P., Sitkiewicz, I., Granville, C., DeLeo, F.R., and Musser, J.M. (2005) Central role of a bacterial two-component gene regulatory system of previously unknown function in pathogen persistence in human saliva. Proc Natl Acad Sci USA 102: 16037-16042.
63. Shelburne, S.A., 3rd, Keith, D., Horstmann, N., Sumby, P., Davenport, M.T., Graviss, E.A., etal. (2008) A direct link between carbohydrate utilization and virulence in the major human pathogen group A Streptococcus. Proc Natl Acad Sci USA 105: 1698-1703.
64. Shelburne, S.A., 3rd, Olsen, R.J., Makthal, N., Brown, N.G., Sahasrabhojane, P., Watkins, E.M., etal. (2011) An amino-terminal signal peptide of Vfr protein negatively influences RopB-dependent SpeB expression and attenuates virulence in Streptococcus pyogenes. Mol Microbiol 82: 1481-1495.
65. Siegel, S.J., Roche, A.M., and Weiser, J.N. (2014) Influenza promotes pneumococcal growth during coinfection by providing host sialylated substrates as a nutrient source. Cell Host Microbe 16: 55-67.
66. Sobel, J.D., Funaro, D., and Kaplan, E.L. (2007) Recurrent group A streptococcal vulvovaginitis in adult women: family epidemiology. Clin Infect Dis 44: e43-e45.
67. Stulke, J., Arnaud, M., Rapoport, G., and Martin-Verstraete, I. (1998) PRD-a protein domain involved in PTS-dependent induction and carbon catabolite repression of catabolic operons in bacteria. Mol Microbiol 28: 865-874.
68. Terra, V.S., Homer, K.A., Rao, S.G., Andrew, P.W., and Yesilkaya, H. (2010) Characterization of novel beta-galactosidase activity that contributes to glycoprotein degradation and virulence in Streptococcus pneumoniae. Infect Immun 78: 348-357.
69. Tong, H., Zeng, L., and Burne, R.A. (2011) The EIIABMan phosphotransferase system permease regulates carbohydrate catabolite repression in Streptococcus gordonii. Appl Environ Microbiol 77: 1957-1965.
70. Toukoki, C., Gold, K.M., McIver, K.S., and Eichenbaum, Z. (2010) MtsR is a dual regulator that controls virulence genes and metabolic functions in addition to metal homeostasis in the group A Streptococcus. Mol Microbiol 76: 971-989.
71. Verstraelen, H., Verhelst, R., Vaneechoutte, M., and Temmerman, M. (2011) Group A streptococcal vaginitis: an unrecognized cause of vaginal symptoms in adult women. Arch Gynecol Obstet 284: 95-98.
72. Virtaneva, K., Porcella, S.F., Graham, M.R., Ireland, R.M., Johnson, C.A., Ricklefs, S.M., etal. (2005) Longitudinal analysis of the group A Streptococcus transcriptome in experimental pharyngitis in cynomolgus macaques. Proc Natl Acad Sci USA 102: 9014-9019.
73. Weinberg, E.D. (1975) Nutritional immunity. Host's attempt to withold iron from microbial invaders. JAMA 231: 39-41.