TCA cycle activity in Staphylococcus aureus is essential for iron-regulated synthesis of staphyloferrin A, but not staphyloferrin B: The benefit of a second citrate synthase

Molecular Microbiology

Volumn 92, Issue 4, 2014, Pages 824-839

  Sheldon, Jessica R ^a   Marolda, Cristina L ^a   Heinrichs, David E ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; CITRATE SYNTHASE; CITRIC ACID; GLUCOSE; LACTIC ACID; SIDEROPHORE; STAPHYLOFERRIN; STAPHYLOFERRIN A; STAPHYLOFERRIN B; UNCLASSIFIED DRUG; CULTURE MEDIUM; IRON; ORNITHINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CITRIC ACID CYCLE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; ANALOGS AND DERIVATIVES; CHEMISTRY; CULTURE MEDIUM; ENZYMOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

STAPHYLOCOCCUS AUREUS;

CITRATE (SI)-SYNTHASE; CITRATES; CITRIC ACID CYCLE; CULTURE MEDIA; GLUCOSE; IRON; ORNITHINE; SIDEROPHORES; STAPHYLOCOCCUS AUREUS;

EID: 84899946485     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12593     Document Type: Article

References (63)

1. Adams, B.D., Lazova, R., Andrews, N.C., and Milstone, L.M. (2005) Iron in skin of mice with three etiologies of systemic iron overload. J Invest Dermatol 125: 1200-1205.
2. American Diabetes Association (2013) Standards of medical care in diabetes - 2013. Diabetes Care 36 (Suppl. 1): S11-S66.
3. Aruoma, O.I., Reilly, T., MacLaren, D., and Halliwell, B. (1988) Iron, copper and zinc concentrations in human sweat and plasma; the effect of exercise. Int J Clin Chem 177: 81-87.
4. Bae, T., and Schneewind, O. (2006) Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid 55: 58-63.
5. Bae, T., Banger, A.K., Wallace, A., Glass, E.M., Aslund, F., Schneewind, O., and Missiakas, D.M. (2004) Staphylococcus aureus virulence genes identified by bursa aurealis mutagenesis and nematode killing. Proc Natl Acad Sci USA 101: 12312-12317.
6. Bateman, B.T., Donegan, N.P., Jarry, T.M., Palma, M., and Cheung, A.L. (2001) Evaluation of a tetracycline-inducible promoter in Staphylococcus aureus in vitro and in vivo and its application in demonstrating the role of sigB in microcolony formation. Infect Immun 69: 7851-7857.
7. Beamish, M.R., Jobbins, K., and Cavill, I. (1971) The cellular distribution of transferrin-bound iron in the skin. Br J Dermatol 85: 49-51.
8. Beasley, F.C., and Heinrichs, D.E. (2010) Siderophore-mediated iron acquisition in the staphylococci. J Inorg Biochem 104: 282-288.
9. Beasley, F.C., Vinés, E.D., Grigg, J.C., Zheng, Q., Liu, S., Lajoie, G.A., etal. (2009) Characterization of staphyloferrin A biosynthetic and transport mutants in Staphylococcus aureus. Mol Microbiol 72: 947-963.
10. Beasley, F.C., Cheung, J., and Heinrichs, D.E. (2011) Mutation of L-2, 3-diaminopropionic acid synthase genes blocks staphyloferrin B synthesis in Staphylococcus aureus. BMC Microbiol 11: 199.
11. Beasley, F.C., Marolda, C.L., Cheung, J., Buac, S., and Heinrichs, D.E. (2011) Staphylococcus aureus transporters Hts, Sir, and Sst capture iron liberated from human transferrin by staphyloferrin A, staphyloferrin B, and catecholamine stress hormones, respectively, and contribute to virulence. Infect Immun 79: 2345-2355.
12. Cassat, J.E., and Skaar, E.P. (2012) Metal ion acquisition in Staphylococcus aureus: overcoming nutritional immunity. Semin Immunopathol 34: 215-235.
13. Cheung, J., Beasley, F.C., Liu, S., Lajoie, G.A., and Heinrichs, D.E. (2009) Molecular characterization of staphyloferrin B biosynthesis in Staphylococcus aureus. Mol Microbiol 74: 594-608.
14. Cheung, J., Murphy, M.E.P., and Heinrichs, D.E. (2012) Discovery of an iron-regulated citrate synthase in Staphylococcus aureus. Chem Biol 19: 1568-1578.
15. Cohen, S., Sweeney, H.M., and Leitner, F. (1967) Relation between iron uptake, pH of growth medium, and penicillinase formation in Staphylococcus aureus. J Bacteriol 93: 1227-1235.
16. Collins, F., and Lascelles, J. (1962) The effect of growth conditions on oxidative and dehydrogenase activity in Staphylococcus aureus. J Gen Microbiol 29: 531-535.
17. Cotton, J.L., Tao, J., and Balibar, C.J. (2009) Identification and characterization of the Staphylococcus aureus gene cluster coding for staphyloferrin A. Biochemistry (Mosc) 48: 1025-1035.
18. Dale, S.E., Doherty-Kirby, A., Lajoie, G., and Heinrichs, D.E. (2004a) Role of siderophore biosynthesis in virulence of Staphylococcus aureus: identification and characterization of genes involved in production of a siderophore. Infect Immun 72: 29-37.
19. Dale, S.E., Sebulsky, M.T., and Heinrichs, D.E. (2004b) Involvement of SirABC in iron-siderophore import in Staphylococcus aureus. J Bacteriol 186: 8356-8362.
20. DeLeo, F.R., Otto, M., Kreiswirth, B.N., and Chambers, H.F. (2010) Community-associated meticillin-resistant Staphylococcus aureus. Lancet 375: 1557-1568.
21. Diekema, D.J., Pfaller, M.A., Schmitz, F.J., Smayevsky, J., Bell, J., Jones, R.N., and Beach, M. (2001) Survey of infections due to Staphylococcus species: frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacific region for the SENTRY Antimicrobial Surveillance Program, 1997-1999. Clin Infect Dis 32 (Suppl. 2): S114-S132.
22. Drechsel, H., Freund, S., Nicholson, G., Haag, H., Jung, O., Zahner, H., and Jung, G. (1993) Purification and chemical characterization of staphyloferrin B, a hydrophilic siderophore from staphylococci. Biometals 6: 185-192.
23. Duthie, E.S., and Lorenz, L.L. (1952) Staphylococcal coagulase; mode of action and antigenicity. J Gen Microbiol 6: 95-107.
24. von Eiff, C., Peters, G., and Heilmann, C. (2002) Pathogenesis of infections due to coagulase-negative staphylococci. Lancet Infect Dis 2: 677-685.
25. Forslind, B. (2000) The skin barrier: analysis of physiologically important elements and trace elements. Acta Derm Venereol Suppl (Stockh) 208: 46-52.
26. Friedman, D.B., Stauff, D.L., Pishchany, G., Whitwell, C.W., Torres, V.J., and Skaar, E.P. (2006) Staphylococcus aureus redirects central metabolism to increase iron availability. PLoS Pathog 2: e87.
27. Gaballa, A., Antelmann, H., Aguilar, C., Khakh, S.K., Song, K.B., Smaldone, G.T., and Helmann, J.D. (2008) The Bacillus subtilis iron-sparing response is mediated by a Fur-regulated small RNA and three small, basic proteins. Proc Natl Acad Sci USA 105: 11927-11932.
28. Gomme, P.T., McCann, K.B., and Bertolini, J. (2005) Transferrin: structure, function and potential therapeutic actions. Drug Discov Today 10: 267-273.
29. Gordon, R.J., and Lowy, F.D. (2008) Pathogenesis of methicillin-resistant Staphylococcus aureus infection. Clin Infect Dis 46 (Suppl. 5): S350-S359.
30. Guerinot, M.L. (1994) Microbial iron transport. Annu Rev Microbiol 48: 743-772.
31. Haag, H., Fiedler, H.P., Meiwes, J., Drechsel, H., Jung, G., and Zähner, H. (1994) Isolation and biological characterization of staphyloferrin B, a compound with siderophore activity from staphylococci. FEMS Microbiol Lett 115: 125-130.
32. Hantke, K. (2001) Iron and metal regulation in bacteria. Curr Opin Microbiol 4: 172-177.
33. Hood, M.I., and Skaar, E.P. (2012) Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol 10: 525-537.
34. Jin, S., and Sonenshein, A.L. (1994) Identification of two distinct Bacillus subtilis citrate synthase genes. J Bacteriol 176: 4669-4679.
35. Kobylarz, M.J., Grigg, J.C., Takayama, S.J., Rai, D.K., Heinrichs, D.E., and Murphy, M.E. (2014) Synthesis of L-2, 3-diaminopropionic acid, a siderophore and antibiotic precursor. Chem Biol 21: 379-388.
36. Konetschny-Rapp, S., Jung, G., Meiwes, J., and Zahner, H. (1990) Staphyloferrin A: a structurally new siderophore from staphylococci. Eur J Biochem 191: 65-74.
37. Kreiswirth, B.N., Löfdahl, S., Betley, M.J., O'Reilly, M., Schlievert, P.M., Bergdoll, M.S., and Novick, R.P. (1983) The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305: 709-712.
38. Krismer, B., Liebeke, M., Janek, D., Nega, M., Rautenberg, M., Hornig, G., etal. (2014) Nutrient limitation governs Staphylococcus aureus metabolism and niche adaptation in the human nose. PLoS Pathog 10: e1003862.
39. Lan, L., Cheng, A., Dunman, P.M., Missiakas, D., and He, C. (2010) Golden Pigment Production and Virulence Gene Expression Are Affected by Metabolisms in Staphylococcus aureus. J Bacteriol 192: 3068-3077.
40. Lindsay, J.A., Riley, T.V., and Mee, B.J. (1994) Production of siderophore by coagulase-negative staphylococci and its relation to virulence. Eur J Clin Microbiol Infect Dis 13: 1063-1066.
41. Malachowa, N., Whitney, A.R., Kobayashi, S.D., Sturdevant, D.E., Kennedy, A.D., Braughton, K.R., etal. (2011) Global changes in Staphylococcus aureus gene expression in human blood. PLoS ONE 6: e18617.
42. Meiwes, J., Fiedler, H.P., Haag, H., Zahner, H., Konetschny-Rapp, S., and Jung, G. (1990) Isolation and characterization of staphyloferrin A, a compound with siderophore activity from Staphylococcus hyicus DSM 20459. FEMS Microbiol Lett 55: 201-205.
43. Peng, H.L., Novick, R.P., Kreiswirth, B., Kornblum, J., and Schlievert, P. (1988) Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus. J Bacteriol 170: 4365-4372.
44. Psychogios, N., Hau, D.D., Peng, J., Guo, A.C., Mandal, R., Bouatra, S., etal. (2011) The human serum metabolome. PLoS ONE 6: e16957.
45. Ratledge, C. (2007) Iron metabolism and infection. Food Nutr Bull 28: S515-S523.
46. Ratledge, C., and Dover, L.G. (2000) Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54: 881-941.
47. Richardson, A.R., Libby, S.J., and Fang, F.C. (2008) A nitric oxide-inducible lactate dehydrogenase enables Staphylococcus aureus to resist innate immunity. Science 319: 1672-1676.
48. Rogers, K.L., Fey, P.D., and Rupp, M.E. (2009) Coagulase-negative staphylococcal infections. Infect Clin North Am 23: 73-98.
49. Schaible, U.E., and Kaufmann, S.H. (2004) Iron and microbial infection. Nat Rev Microbiol 2: 946-953.
50. Sebulsky, M.T., Speziali, C.D., Shilton, B.H., Edgell, D.R., and Heinrichs, D.E. (2004) FhuD1, a ferric hydroxamate-binding lipoprotein in Staphylococcus aureus: a case of gene duplication and lateral transfer. J Biol Chem 279: 53152-53159.
51. Seidl, K., Müller, S., Francois, P., Kriebitzsch, C., Schrenzel, J., Engelmann, S., etal. (2009) Effect of a glucose impulse on the CcpA regulon in Staphylococcus aureus. BMC Microbiol 9: 95.
52. Seidl, K., Müller, S., François, P., Kriebitzsch, C., Schrenzel, J., Engelmann, S., etal. (2009) Effect of a glucose impulse on the CcpA regulon in Staphylococcus aureus. BMC Microbiol 9: 95.
53. Sheldon, J.R., and Heinrichs, D.E. (2012) The iron-regulated staphylococcal lipoproteins. Front Cell Infect Microbiol 2: 41.
54. Smaldone, G.T., Revelles, O., Gaballa, A., Sauer, U., Antelmann, H., and Helmann, J.D. (2012) A global investigation of the Bacillus subtilis iron-sparing response identifies major changes in metabolism. J Bacteriol 194: 2594-2605.
55. Somerville, G.A., and Powers, R. (2014) Growth and preparation of Staphylococcus epidermidis for NMR metabolomic analysis. Methods Mol Biol 1106: 71-91.
56. Somerville, G.A., and Proctor, R.A. (2013) Cultivation conditions and the diffusion of oxygen into culture media: the rationale for the flask-to-medium ratio in microbiology. BMC Microbiol 13: 9.
57. Somerville, G.A., Chaussee, M.S., Morgan, C.I., Fitzgerald, J.R., Dorward, D.W., Reitzer, L.J., and Musser, J.M. (2002) Staphylococcus aureus aconitase inactivation unexpectedly inhibits post-exponential-phase growth and enhances stationary-phase survival. Infect Immun 70: 6373-6382.
58. Somerville, G.A., Saïd-Salim, B., Wickman, J.M., Raffel, S.J., Kreiswirth, B.N., and Musser, J.M. (2003) Correlation of acetate catabolism and growth yield in Staphylococcus aureus: implications for host-pathogen interactions. Infect Immun 71: 4724-4732.
59. Strasters, K.C., and Winkler, K.C. (1963) Carbohydrate metabolism of Staphylococcus aureus. J Gen Microbiol 33: 213-229.
60. Torres, V.J., Attia, A.S., Mason, W.J., Hood, M.I., Corbin, B.D., Beasley, F.C., etal. (2010) Staphylococcus aureus fur regulates the expression of virulence factors that contribute to the pathogenesis of pneumonia. Infect Immun 78: 1618-1628.
61. Wiltshire, M.D., and Foster, S.J. (2001) Identification and analysis of Staphylococcus aureus components expressed by a model system of growth in serum. Infect Immun 69: 5198-5202.
62. Wolfe, A.J. (2005) The acetate switch. Microbiol Mol Biol Rev 69: 12-50.
63. Xiong, A., Singh, V.K., Cabrera, G., and Jayaswal, R.K. (2000) Molecular characterization of the ferric-uptake regulator, fur, from Staphylococcus aureus. Microbiology 146: 659-668.