IroT/mavN, a new iron-regulated gene involved in Legionella pneumophila virulence against amoebae and macrophages

Environmental Microbiology

Volumn 17, Issue 4, 2015, Pages 1338-1350

  Portier, Emilie ^a   Zheng, Huaixin ^b   Sahr, Tobias ^c   Burnside, Denise M ^b   Mallama, Celeste ^b   Buchrieser, Carmen ^c   Cianciotto, Nicholas P ^b   Héchard, Yann ^a  

^a UNIVERSITÉ DE POITIERS   (France)

^b NORTHWESTERN UNIVERSITY   (United States)

^c INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACANTHAMOEBA CASTELLANII; BACTERIA (MICROORGANISMS); LEGIONELLA PNEUMOPHILA;

BACTERIAL PROTEIN; IRON; MEMBRANE PROTEIN; VIRULENCE FACTOR;

AMOEBA (LIFE CYCLE STAGE); GENETICS; HUMAN; LEGIONELLA PNEUMOPHILA; LEGIONNAIRE DISEASE; MACROPHAGE; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; TRANSPORT AT THE CELLULAR LEVEL; VIRULENCE;

AMOEBA; BACTERIAL PROTEINS; BASE SEQUENCE; BIOLOGICAL TRANSPORT; HUMANS; IRON; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; MACROPHAGES; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; VIRULENCE; VIRULENCE FACTORS;

EID: 84926415727     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12604     Document Type: Article

References (48)

1. Aisen, P. (1976) The binding and release of iron by transferrin. Birth Defects Orig Artic Ser 12: 81-95.
2. Allard, K.A., Viswanathan, V.K., and Cianciotto, N.P. (2006) lbtA and lbtB are required for production of the Legionella pneumophila siderophore legiobactin. J Bacteriol 188: 1351-1363.
3. Allard, K.A., Dao, J., Sanjeevaiah, P., McCoy-Simandle, K., Chatfield, C.H., Crumrine, D.S., etal. (2009) Purification of Legiobactin and importance of this siderophore in lung infection by Legionella pneumophila. Infect Immun 77: 2887-2895.
4. Andrews, S.C. (2011) Making DNA without iron - induction of a manganese-dependent ribonucleotide reductase in response to iron starvation. Mol Microbiol 80: 286-289.
5. Andrews, S.C., Robinson, A.K., and Rodriguez-Quinones, F. (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27: 215-237.
6. Borella, P., Montagna, M.T., Romano-Spica, V., Stampi, S., Stancanelli, G., Triassi, M., etal. (2004) Legionella infection risk from domestic hot water. Emerg Infect Dis 10: 457-464.
7. Bruggemann, H., Hagman, A., Jules, M., Sismeiro, O., Dillies, M.A., Gouyette, C., etal. (2006) Virulence strategies for infecting phagocytes deduced from the in vivo transcriptional program of Legionella pneumophila. Cell Microbiol 8: 1228-1240.
8. Byrne, B., and Swanson, M.S. (1998) Expression of Legionella pneumophila virulence traits in response to growth conditions. Infect Immun 66: 3029-3034.
9. Cazalet, C., Rusniok, C., Bruggemann, H., Zidane, N., Magnier, A., Ma, L., etal. (2004) Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat Genet 36: 1165-1173.
10. Chatfield, C.H., and Cianciotto, N.P. (2007) The secreted pyomelanin pigment of Legionella pneumophila confers ferric reductase activity. Infect Immun 75: 4062-4070.
11. Chatfield, C.H., Mulhern, B.J., Burnside, D.M., and Cianciotto, N.P. (2011) Legionella pneumophila LbtU acts as a novel, TonB-independent receptor for the legiobactin siderophore. J Bacteriol 193: 1563-1575.
12. Chatfield, C.H., Mulhern, B.J., Viswanathan, V.K., and Cianciotto, N.P. (2012) The major facilitator superfamily-type protein LbtC promotes the utilization of the legiobactin siderophore by Legionella pneumophila. Microbiology 158: 721-735.
13. Chien, M., Morozova, I., Shi, S., Sheng, H., Chen, J., Gomez, S.M., etal. (2004) The genomic sequence of the accidental pathogen Legionella pneumophila. Science 305: 1966-1968.
14. Cianciotto, N.P. (2007) Iron acquisition by Legionella pneumophila. Biometals 20: 323-331.
15. Cirillo, S.L., Lum, J., and Cirillo, J.D. (2000) Identification of novel loci involved in entry by Legionella pneumophila. Microbiology 146 (Part 6): 1345-1359.
16. Dalebroux, Z.D., and Swanson, M.S. (2012) ppGpp: magic beyond RNA polymerase. Nat Rev Microbiol 10: 203-212.
17. Dalebroux, Z.D., Edwards, R.L., and Swanson, M.S. (2009) SpoT governs Legionella pneumophila differentiation in host macrophages. Mol Microbiol 71: 640-658.
18. Declerck, P., Behets, J., van Hoef, V., and Ollevier, F. (2007) Replication of Legionella pneumophila in floating biofilms. Curr Microbiol 55: 435-440.
19. Edwards, R.L., Dalebroux, Z.D., and Swanson, M.S. (2009) Legionella pneumophila couples fatty acid flux to microbial differentiation and virulence. Mol Microbiol 71: 1190-1204.
20. Escolar, L., Perez-Martin, J., and de Lorenzo, V. (1999) Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181: 6223-6229.
21. Fields, B.S., Benson, R.F., and Besser, R.E. (2002) Legionella and Legionnaires' disease: 25 years of investigation. Clin Microbiol Rev 15: 506-526.
22. Hickey, E.K., and Cianciotto, N.P. (1994) Cloning and sequencing of the Legionella pneumophila fur gene. Gene 143: 117-121.
23. Hickey, E.K., and Cianciotto, N.P. (1997) An iron- and fur-repressed Legionella pneumophila gene that promotes intracellular infection and encodes a protein with similarity to the Escherichia coli aerobactin synthetases. Infect Immun 65: 133-143.
24. Huang, L., Boyd, D., Amyot, W.M., Hempstead, A.D., Luo, Z.Q., O'Connor, T.J., etal. (2011) The E Block motif is associated with Legionella pneumophila translocated substrates. Cell Microbiol 13: 227-245.
25. Koide, M., Saito, A., Kusano, N., and Higa, F. (1993) Detection of Legionella spp. in cooling tower water by the polymerase chain reaction method. Appl Environ Microbiol 59: 1943-1946.
26. Leong, J., Neilands, J.B., and Raymond, K.N. (1974) Coordination isomers of biological iron transport compounds. III. (1) Transport of lambda-cis-chromic desferriferrichrome by Ustilago sphaerogena. Biochem Biophys Res Commun 60: 1066-1071.
27. Liles, M.R., Scheel, T.A., and Cianciotto, N.P. (2000) Discovery of a nonclassical siderophore, legiobactin, produced by strains of Legionella pneumophila. J Bacteriol 182: 749-757.
28. Livak, K.J., and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Methods 25: 402-408.
29. Lomma, M., Dervins-Ravault, D., Rolando, M., Nora, T., Newton, H.J., Sansom, F.M., etal. (2010) The Legionella pneumophila F-box protein Lpp2082 (AnkB) modulates ubiquitination of the host protein parvin B and promotes intracellular replication. Cell Microbiol 12: 1272-1291.
30. Magnusson, L.U., Farewell, A., and Nystrom, T. (2005) ppGpp: a global regulator in Escherichia coli. Trends Microbiol 13: 236-242.
31. Molofsky, A.B., and Swanson, M.S. (2004) Differentiate to thrive: lessons from the Legionella pneumophila life cycle. Mol Microbiol 53: 29-40.
32. Py, B., and Barras, F. (2010) Building Fe-S proteins: bacterial strategies. Nat Rev Microbiol 8: 436-446.
33. Ratledge, C., and Dover, L.G. (2000) Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54: 881-941.
34. Reeves, M.W., Pine, L., Hutner, S.H., George, J.R., and Harrell, W.K. (1981) Metal requirements of Legionella pneumophila. J Clin Microbiol 13: 688-695.
35. Reeves, M.W., Pine, L., Neilands, J.B., and Balows, A. (1983) Absence of siderophore activity in Legionella species grown in iron-deficient media. J Bacteriol 154: 324-329.
36. Riemer, J., Hoepken, H.H., Czerwinska, H., Robinson, S.R., and Dringen, R. (2004) Colorimetric ferrozine-based assay for the quantitation of iron in cultured cells. Anal Biochem 331: 370-375.
37. Robey, M., and Cianciotto, N.P. (2002) Legionella pneumophila feoAB promotes ferrous iron uptake and intracellular infection. Infect Immun 70: 5659-5669.
38. Roche, B., Aussel, L., Ezraty, B., Mandin, P., Py, B., and Barras, F. (2013) Iron/sulfur proteins biogenesis in prokaryotes: formation, regulation and diversity. Biochim Biophys Acta 1827: 455-469.
39. Rolando, M., Sanulli, S., Rusniok, C., Gomez-Valero, L., Bertholet, C., Sahr, T., etal. (2013) Legionella pneumophila effector RomA uniquely modifies host chromatin to repress gene expression and promote intracellular bacterial replication. Cell Host Microbe 13: 395-405.
40. Rowbotham, T.J. (1980) Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J Clin Pathol 33: 1179-1183.
41. Sahr, T., Bruggemann, H., Jules, M., Lomma, M., Albert-Weissenberger, C., Cazalet, C., and Buchrieser, C. (2009) Two small ncRNAs jointly govern virulence and transmission in Legionella pneumophila. Mol Microbiol 72: 741-762.
42. Sahr, T., Rusniok, C., Dervins-Ravault, D., Sismeiro, O., Coppee, J.Y., and Buchrieser, C. (2012) Deep sequencing defines the transcriptional map of L. pneumophila and identifies growth phase-dependent regulated ncRNAs implicated in virulence. RNA Biol 9: 503-519.
43. Schaible, U.E., and Kaufmann, S.H. (2004) Iron and microbial infection. Nat Rev Microbiol 2: 946-953.
44. Steinert, M., Hentschel, U., and Hacker, J. (2002) Legionella pneumophila: an aquatic microbe goes astray. FEMS Microbiol Rev 26: 149-162.
45. Vinella, D., Albrecht, C., Cashel, M., and D'Ari, R. (2005) Iron limitation induces SpoT-dependent accumulation of ppGpp in Escherichia coli. Mol Microbiol 56: 958-970.
46. Viswanathan, V.K., Edelstein, P.H., Pope, C.D., and Cianciotto, N.P. (2000) The Legionella pneumophila iraAB locus is required for iron assimilation, intracellular infection, and virulence. Infect Immun 68: 1069-1079.
47. Weinberg, E.D. (1978) Iron and infection. Microbiol Rev 42: 45-66.
48. Zheng, H., Chatfield, C.H., Liles, M.R., and Cianciotto, N.P. (2013) Secreted pyomelanin of Legionella pneumophila promotes bacterial iron uptake and growth under iron-limiting conditions. Infect Immun 81: 4182-4191.