Growth promotion of the opportunistic human pathogen, Staphylococcus lugdunensis, by heme, hemoglobin, and coculture with Staphylococcus aureus

MicrobiologyOpen

Volumn 3, Issue 2, 2014, Pages 182-195

  Brozyna, Jeremy R ^a   Sheldon, Jessica R ^a   Heinrichs, David E ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Heme; Hemoglobin; Iron acquisition; Staphylococci; Staphyloferrins

Indexed keywords

ABC TRANSPORTER; HEME; HEMOGLOBIN; HTSA TRANSPORTER; HTSB TRANSPORTER; HTSC TRANSPORTER; SIDEROPHORE; SIRA TRANSPORTER; SIRB TRANSPORTER; SIRC TRANSPORTER; STAPHYLOFERRIN A; STAPHYLOFERRIN B; UNCLASSIFIED DRUG; CARRIER PROTEIN; IRON;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; COCULTURE; CONTROLLED STUDY; GENE CLUSTER; GENE LOCUS; IRON METABOLISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEQUENCE ANALYSIS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS LUGDUNENSIS; STAPHYLOFERRIN A GENE; STAPHYLOFERRIN B GENE; GENE DELETION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

GENE DELETION; HEME; HEMOGLOBINS; IRON; MEMBRANE TRANSPORT PROTEINS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS LUGDUNENSIS;

EID: 84898008478     PISSN: None     EISSN: 20458827     Source Type: Journal    
DOI: 10.1002/mbo3.162     Document Type: Article

References (50)

1. Anguera, I., A. Del Río, J. M. Miró, X. Matínez-Lacasa, F. Marco, J. R. Gumá, et al. 2005. Staphylococcus lugdunensis infective endocarditis: description of 10 cases and analysis of native valve, prosthetic valve, and pacemaker lead endocarditis clinical profiles. Heart 91:e10.
2. Arias, M., D. Tena, M. Apellániz, M. P. Asensio, P. Caballero, C. Hernández, et al. 2010. Skin and soft tissue infections caused by Staphylococcus lugdunensis: report of 20 cases. Scand. J. Infect. Dis. 42:879-884.
3. Bae, T., and O. Schneewind. 2006. Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid 55:58-63.
4. Beasley, F. C., and D. E. Heinrichs. 2010. Siderophore-mediated iron acquisition in the staphylococci. J. Inorg. Biochem. 104:282-288.
5. Beasley, F. C., E. D. Vines, J. C. Grigg, Q. Zheng, S. Liu, G. A. Lajoie, et al. 2009. Characterization of staphyloferrin A biosynthetic and transport mutants in Staphylococcus aureus. Mol. Microbiol. 72:947-963.
6. Beasley, F. C., J. Cheung, and D. E. Heinrichs. 2011a. Mutation of l-2, 3-diaminopropionic acid synthase genes blocks staphyloferrin B synthesis in Staphylococcus aureus. BMC Microbiol. 11:199.
7. Beasley, F. C., C. L. Marolda, J. Cheung, S. Buac, and D. E. Heinrichs. 2011b. 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.
8. Bellamy, R., and T. Barkham. 2002. Staphylococcus lugdunensis infection sites: predominance of abscesses in the pelvic girdle region. Clin. Infect. Dis. 35:E32-E34.
9. Bieber, L., and G. Kahlmeter. 2010. Staphylococcus lugdunensis in several niches of the normal skin flora. Clin. Microbiol. Infect. 16:385-388.
10. Böcher, S., B. Tønning, R. L. Skov, and J. Prag. 2009. Staphylococcus lugdunensis, a common cause of skin and soft tissue infections in the community. J. Clin. Microbiol. 47:946-950.
11. Cheung, J., F. C. Beasley, S. Liu, G. A. Lajoie, and D. E. Heinrichs. 2009. Molecular characterization of staphyloferrin B biosynthesis in Staphylococcus aureus. Mol. Microbiol. 74:594-608.
12. Corrigan, R. M., and T. J. Foster. 2009. An improved tetracycline-inducible expression vector for Staphylococcus aureus. Plasmid 61:126-129.
13. Cotton, J. L., J. Tao, and C. J. Balibar. 2009. Identification and characterization of the Staphylococcus aureus gene cluster coding for staphyloferrin A. Biochemistry 48:1025-1035.
14. Dale, S. E. 2004. Involvement of SirABC in iron-siderophore import in Staphylococcus aureus. J. Bacteriol. 186:8356-8362.
15. Edwards, A. M., R. C. Massey, and S. R. Clarke. 2012. Molecular mechanisms of Staphylococcus aureus nasopharyngeal colonization. Mol. Oral Microbiol. 27:1-10.
16. Frank, K. L., J. L. Del Pozo, and R. Patel. 2008. From clinical microbiology to infection pathogenesis: how daring to be different works for Staphylococcus lugdunensis. Clin. Microbiol. Rev. 21:111-133.
17. Freney, J., Y. Brun, M. Bes, H. Meugnier, F. Grimont, P. A. D. Grimont, et al. 1988. Staphylococcus lugdunensis sp. nov. and Staphylococcus schleiferi sp. nov., two species from human clinical specimens. Int. J. Syst. Bacteriol. 38:168-172.
18. Gomme, P. T., K. B. McCann, and J. Bertolini. 2005. Transferrin: structure, function and potential therapeutic actions. Drug Discov. Today 10:267-273.
19. Grigg, J. C., J. Cheung, D. E. Heinrichs, and M. E. Murphy. 2010a. Specificity of staphyloferrin B recognition by the SirA receptor from Staphylococcus aureus. J. Biol. Chem. 285:34579-34588.
20. Grigg, J. C., J. D. Cooper, J. Cheung, D. E. Heinrichs, and M. E. Murphy. 2010b. The Staphylococcus aureus siderophore receptor HtsA undergoes localized conformational changes to enclose staphyloferrin A in an arginine-rich binding pocket. J. Biol. Chem. 285:11162-11171.
21. Grigg, J. C., G. Ukpabi, C. F. M. Gaudin, and M. E. P. Murphy. 2010c. Structural biology of heme binding in the Staphylococcus aureus Isd system. J. Inorg. Biochem. 104:341-348.
22. Haag, H., H.-P. Fiedler, J. Meiwes, H. Drechsel, G. Jung, and H. Zähner. 1994. Isolation and biological characterization of staphyloferrin B, a compound with siderophore activity from staphylococci. FEMS Microbiol. Lett. 115:125-130.
23. Haley, K. P., E. M. Janson, S. Heilbronner, T. J. Foster, and E. P. Skaar. 2011. Staphylococcus lugdunensis IsdG liberates iron from host heme. J. Bacteriol. 193:4749-4757.
24. Hammer, N. D., and E. P. Skaar. 2011. Molecular mechanisms of Staphylococcus aureus iron acquisition. Annu. Rev. Microbiol. 65:129-147.
25. Heilbronner, S., M. T. G. Holden, A. van Tonder, J. A. Geoghegan, T. J. Foster, J. Parkhill, et al. 2011. Genome sequence of Staphylococcus lugdunensis N920143 allows identification of putative colonization and virulence factors. FEMS Microbiol. Lett. 322:60-67.
26. Heilbronner, S., F. Hanses, I. R. Monk, P. Speziale, and T. J. Foster. 2013. Sortase A promotes virulence in experimental Staphylococcus lugdunensis endocarditis. Microbiology 159:2141-2152.
27. Herchline, T. E., and L. W. Ayers. 1991. Occurrence of Staphylococcus lugdunensis in consecutive clinical cultures and relationship of isolation to infection. J. Clin. Microbiol. 29:419-421.
28. Hood, M. I., and E. P. Skaar. 2012. Nutritional immunity: transition metals at the pathogen-host interface. Nat. Rev. Microbiol. 10:525-537.
29. Kleiner, E., A. B. Monk, G. L. Archer, and B. A. Forbes. 2010. Clinical significance of Staphylococcus lugdunensis isolated from routine cultures. Clin. Infect. Dis. 51:801-803.
30. Kreiswirth, B., S. Lofdahl, M. J. Bentley, M. O'Reilly, P. M. Schlievert, M. S. Bergdoll, et al. 1983. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305:709-712.
31. Lee, C. Y., and J. J. Iandolo. 1986. Lysogenic conversion of staphylococcal lipase is caused by insertion of the bacteriophage L54a genome into the lipase structural gene. J. Bacteriol. 166:385-391.
32. Mazmanian, S. K., H. Ton-That, K. Su, and O. Schneewind. 2002. An iron-regulated sortase anchors a class of surface protein during Staphylococcus aureus pathogenesis. Proc. Natl Acad. Sci. USA 99:2293-2298.
33. Mazmanian, S. K., E. P. Skaar, A. H. Gaspar, M. Humayun, P. Gornicki, J. Jelenska, et al. 2003. Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299:906-909.
34. Meiwes, J., H. P. Fiedler, H. Haag, H. Zahner, S. Konetschny-Rapp, and G. Jung. 1990. Isolation and characterization of staphyloferrin A, a compound with siderophore activity from Staphylococcus hyicus DSM 20459. FEMS Microbiol. Lett. 55:201-205.
35. Monk, I.R., I. M. Shah, M. Xu, M. W. Tan, and T. J. Foster. 2012. Transforming the untransformable: application of direct transformation to manipulate genetically Staphylococcus aureus and Staphylococcus epidermidis. mBio 3:e00277-11.
36. Peng, H. L., R. P. Novick, B. Kreiswirth, J. Kornblum, and P. Schlievert. 1988. Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus. J. Bacteriol. 170:4365-4372.
37. Pishchany, G., and E. P. Skaar. 2012. Taste for blood: hemoglobin as a nutrient source for pathogens. PLoS Pathog. 8:e1002535.
38. Ratledge, C., and L. G. Dover. 2000. Iron metabolism in pathogenic bacteria. Annu. Rev. Microbiol. 54:881-941.
39. Rosenstein, R., and F. Götz. 2013. What distinguishes highly pathogenic Staphylococci from medium- and non-pathogenic? Curr. Top. Microbiol. Immunol. 358:33-89.
40. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular cloning. A laboratory manual. 2nd ed.Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
41. Schwyn, B., and J. B. Neilands. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160:47-56.
42. Sebulsky, M. T., D. Hohnstein, M. D. Hunter, and D. E. Heinrichs. 2000. Identification and characterization of a membrane permease involved in iron-hydroxamate transport in Staphylococcus aureus. J. Bacteriol. 182:4394-4400.
43. Sebulsky, M. T., C. D. Speziali, B. H. Shilton, D. R. Edgell, and D. E. Heinrichs. 2004. FhuD1, a ferric hydroxamate-binding lipoprotein in Staphylococcus aureus: a case of gene duplication and lateral transfer. J. Biol. Chem. 279:53152-53159.
44. Skaar, E. P., and O. Schneewind. 2004. Iron-regulated surface determinants (Isd) of Staphylococcus aureus: stealing iron from heme. Microbes Infect. 6:390-397.
45. Sotutu, V., J. Carapetis, J. Wilkinson, A. Davis, and N. Curtis. 2002. The "surreptitious Staphylococcus": Staphylococcus lugdunensis endocarditis in a child. Pediatr. Infect. Dis. J. 21:984-986.
46. Speziali, C. G., S. E. Dale, J. A. Henderson, E. D. Vines, and D. E. Heinrichs. 2006. Requirement of Staphylococcus aureus ATP-binding cassette ATPase FhuC for iron-restricted growth and evidence that it functions with more than one iron transporter. J. Bacteriol. 188:2048-2055.
47. Szabados, F., Y. Nowotny, L. Marlinghaus, M. Korte, S. Neumann, M. Kaase, et al. 2011. Occurrence of genes of putative fibrinogen binding proteins and hemolysins, as well as of their phenotypic correlates in isolates of S. lugdunensis of different origins. BMC Res. Notes 4:113.
48. Tse, H., H. W. Tsoi, S. P. Leung, S. K. P. Lau, P. C. Y. Woo, and K. Y. Yuen. 2010. Complete genome sequence of Staphylococcus lugdunensis strain HKU09-01. J. Bacteriol. 192:1471-1472.
49. Winterbourn, C. C., B. M. McGrath, and R. W. Carrell. 1976. Reactions involving superoxide and normal and unstable haemoglobins. Biochem. J. 155:493-502.
50. Zapotoczna, M., S. Heilbronner, P. Speziale, and T. J. Foster. 2012. Iron-regulated surface determinant (Isd) proteins of Staphylococcus lugdunensis. J. Bacteriol. 194:6453-6467.