The secreted pyomelanin pigment of Legionella pneumophila confers ferric reductase activity

Infection and Immunity

Volumn 75, Issue 8, 2007, Pages 4062-4070

  Chatfield, Christa H ^a   Cianciotto, Nicholas P ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FERRIC ION; FERROUS ION; HOMOGENTISIC ACID; IRON; IRON REDUCTASE; PROTEINASE; PYOMELANIN; SIDEROPHORE; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; ENZYME ACTIVITY; GENE IDENTIFICATION; GENE INSERTION; HMGA GENE; LEGIONELLA PNEUMOPHILA; NONHUMAN; PRIORITY JOURNAL;

BACTERIAL PROTEINS; DNA TRANSPOSABLE ELEMENTS; FMN REDUCTASE; GENETIC COMPLEMENTATION TEST; LEGIONELLA PNEUMOPHILA; MELANINS; MOLECULAR WEIGHT; MUTAGENESIS, INSERTIONAL; PEPTIDE HYDROLASES;

EID: 34547647647     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00489-07     Document Type: Article

References (116)

1. Agodi, A., S. Stefani, C. Corsaro, F. Campanile, S. Gribaldo, and G. Sichel. 1996. Study of a melanic pigment of Proteus mirabilis. Res. Microbiol. 147:167-174.
2. Albert-Weissenberger, C., C. Cazalet, and C. Buchrieser. 2007. Legionella pneumophila - a human pathogen that co-evolved with fresh water protozoa. Cell Mol. Life Sci. 64:432-448.
3. Allard, K. A., V. K. Viswanathan, and N. P. Cianciotto. 2006. lbtA and lbtB are required for production of the Legionella pneumophila siderophore legiobactin. J. Bacteriol. 188:1351-1363.
4. Arias-Barrau, E., E. R. Olivera, J. M. Luengo, C. Fernandez, B. Galan, J. L. Garcia, E. Diaz, and B. Minambres. 2004. The homogentisate pathway: a central catabolic pathway involved in the degradation of L- phenylalanine, L-ryrosine, and 3-hydroxyphenylacetate in Pseudomonas putida. J. Bacteriol. 186:5062-5077.
5. Bachman, M. A., and M. S. Swanson. 2004. The LetE protein enhances expression of multiple LetA/LetS-dependent transmission traits by Legionella pneumophila. Infect. Immun. 72:3284-3293.
6. Baine, W. B., and J. K. Rasheed. 1979. Aromatic substrate specificity of browning by cultures of the Legionnaires' disease bacterium. Ann. Intern. Med. 90:619-620.
7. Baine, W. B., J. K. Rasheed, J. C. Feeley, G. W. Gorman, and L. E. Casida. 1978. Effect of supplemental L-tyrosine on pigment production in cultures of the Legionnaires' disease bacterium. Curr. Microbiol. 1:93-94.
8. Bandyopadhyay, P., S. Liu, C. B. Gabbai, Z. Venitelli, and H. M. Steinman. 2007. Environmental mimics and the Lvh type IVA secretion system contribute to virulence-related phenotypes of Legionella pneumophila. Infect. Immun. 75:723-735.
9. Bellinger-Kawahara, C., and M. A. Horwitz. 1990. Complement component C3 fixes selectively to the major outer membrane protein (MOMP) of Legionella pneumophila and mediates phagocytosis of liposome-MOMP complexes by human monocytes. J. Exp. Med. 172:1201-1210.
10. Bender, L., M. Ott, A. Debes, U. Rdest, J. Heesemann, and J. Hacker. 1991. Distribution, expression, and long-range mapping of legiolysin gene (lly)-specific DNA sequences in legionellae. Infect. Immun. 59:3333-3336.
11. Berg, J. D., J. C. Hoff, P. V. Roberts, and A. Matin. 1985. Growth of Legionella pneumophila in continuous culture. Appl. Environ. Microbiol. 49:1534-1537.
12. Byrd, T. F., and M. A. Horwitz. 1989. Interferon gamma-activated human monocytes downregulate transferrin receptors and inhibit the intracellular multiplication of Legionella pneumophila by limiting the availability of iron. J. Clin. Investig. 83:1457-1465.
13. Carreira, A., L. M. Ferreira, and V. Loureiro. 2001. Brown pigments produced by Yarrowia lipolytica result from extracellular accumulation of homogentisic acid. Appl. Environ. Microbiol. 67:3463-3468.
14. Cazalet, C., C. Rusniok, H. Bruggemann, N. Zidane, A. Magnier, L. Ma, M. Tichit, S. Jarraud, C. Bouchier, F. Vandenesch, F. Kunst, J. Etienne, P. Glaser, and C. Buchrieser. 2004. Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat. Genet. 36:1165-1173.
15. Challis, G. L. 2005. A widely distributed bacterial pathway for siderophore biosynthesis independent of nonribosomal peptide synthetases. Chembiochem 6:601-611.
16. Chien, M., I. Morozova, S. Shi, H. Sheng, J. Chen, S. M. Gomez, G. Asamani, K. Hill, J. Nuara, M. Feder, J. Rineer, J. J. Greenberg, V. Steshenko, S. H. Park, B. Zhao, E. Teplitskaya, J. R. Edwards, S. Pampou, A. Georghiou, I. C. Chou, W. Iannuccilli, M. E. Ulz, D. H. Kim, A. Geringer-Sameth, C. Goldsberry, P. Morozov, S. G. Fischer, G. Segal, X. Qu, A. Rzhetsky, P. Zhang, E. Cayanis, P. J. De Jong, J. Ju, S. Kalachikov, H. A. Shuman, and J. J. Russo. 2004. The genomic sequence of the accidental pathogen Legionella pneumophila. Science 305:1966-1968.
17. Cianciotto, N. P. 2007. Iron acquisition by Legionella pneumophila. Biometals 20:323-331.
18. Cianciotto, N. P. 2001. Pathogenicity of Legionella pneumophila. Int. J. Med. Microbiol. 291:331-343.
19. Cianciotto, N. P. 2005. Type II secretion: a protein secretion system for all seasons. Trends Microbiol. 13:581-588.
20. Cianciotto, N. P., P. Cornelis, and C. Baysse. 2005. Impact of the bacterial type I cytochrome c maturation system on different biological processes. Mol. Microbiol. 56:1408-1415.
21. Cianciotto, N. P., and B. S. Fields. 1992. Legionella pneumophila mip gene potentiates intracellular infection of protozoa and human macrophages. Proc. Natl. Acad. Sci. USA 89:5188-5191.
22. Cowart, R. E. 2002. Reduction of iron by extracellular iron reductases: implications for microbial iron acquisition. Arch. Biochem. Biophys. 400: 273-281.
23. Cox, C. D. 1986. Role of pyocyanin in the acquisition of iron from transferrin. Infect. Immun. 52:263-270.
24. Coyne, V. E., and L. al-Harthi. 1992. Induction of melanin biosynthesis in Vibrio cholerae. Appl. Environ. Microbiol. 58:2861-2865.
25. Cubo, M. T., A. M. Buendia-Claveria, J. E. Beringer, and J. E. Ruiz-Sainz. 1988. Melanin production by Rhizobium strains. Appl. Environ. Microbiol. 54:1812-1817.
26. DebRoy, S., V. Aragon, S. Kurtz, and N. P. Cianciotto. 2006. Legionella pneumophila Mip, a surface-exposed peptidylproline cis-trans-isomerase, promotes the presence of phospholipase C-like activity in culture supernatants. Infect. Immun. 74:5152-5160.
27. DebRoy, S., J. Dao, M. Soderberg, O. Rossier, and N. P. Cianciotto. 2006. Legionella pneumophila type II secretome reveals unique exoproteins and a chitinase that promotes bacterial persistence in the lung. Proc. Natl. Acad. Sci. USA 103:19146-19151.
28. Deneer, H. G., V. Healey, and I. Boychuk. 1995. Reduction of exogenous ferric iron by a surface-associated ferric reductase of Listeria spp. Microbiology 141:1985-1992.
29. Denoya, C. D., D. D. Skinner, and M. R. Morgenstern. 1994. A Streptomyces avermitilis gene encoding a 4-hydroxyphenylpyruvic acid dioxygenase-like protein that directs the production of homogentisic acid and an ochronotic pigment in Escherichia coli. J. Bacteriol. 176:5312-5319.
30. Edelstein, P. H. 1981. Improved semiselective medium for isolation of Legionella pneumophila from contaminated clinical and environmental specimens. J. Clin. Microbiol. 14:298-303.
31. Engleberg, N. C., C. Carter, D. R. Weber, N. P. Cianciotto, and B. I. Eisenstein. 1989. DNA sequence of mip, a Legionella pneumophila gene associated with macrophage infectivity. Infect. Immun. 57:1263-1270.
32. Engleberg, N. C., D. J. Drutz, and B. I. Eisenstein. 1984. Cloning and expression of Legionella pneumophila antigens in Escherichia coli. Infect. Immun. 44:222-227.
33. Ernst, R. K., D. A. D'Argenio, J. K. Ichikawa, M. G. Bangera, S. Selgrade, J. L. Burns, P. Hiatt, K. McCoy, M. Brittnacher, A. Kas, D. H. Spencer, M. V. Olson, B. W. Ramsey, S. Lory, and S. I. Miller. 2003. Genome mosaicism is conserved but not unique in Pseudomonas aeruginosa isolates from the airways of young children with cystic fibrosis. Environ. Microbiol. 5:1341-1349.
34. Fang, G. D., V. L. Yu, and R. M. Vickers. 1989. Disease due to the Legionellaceae (other than Legionella pneumophila): historical, microbiological, clinical, and epidemiological review. Medicine 68:116-132.
35. Feeley, J. C., G. W. Gorman, R. E. Weaver, D. C. Mackel, and H. W. Smith. 1978. Primary isolation media for Legionnaires' disease bacterium. J. Clin. Microbiol. 8:320-325.
36. Fernandez-Canon, J. M., and M. A. Penalva. 1995. Molecular characterization of a gene encoding a homogentisate dioxygenase from Aspergillus nidulans and identification of its human and plant homologues. J. Biol. Chem. 270:21199-21205.
37. Fields, B. S., R. F. Benson, and R. E. Besser. 2002. Legionella and Legionnaires' disease: 25 years of investigation. Clin. Microbiol. Rev. 15:506-526.
38. Frases, S., A. Salazar, E. Dadachova, and A. Casadevall. 2007. Cryptococcus neoformans can utilize the bacterial melanin precursor homogentisic acid for fungal melanogenesis. Appl. Environ. Microbiol. 73:615-621.
39. Garduno, R. A., E. Garduno, and P. S. Hoffman. 1998. Surface-associated Hsp60 chaperonin of Legionella pneumophila mediates invasion in a HeLa cell model. Infect. Immun. 66:4602-4610.
40. Gillespie, D. E., S. F. Brady, A. D. Bettermann, N. P. Cianciotto, M. R. Liles, M. R. Rondon, J. Clardy, R. M. Goodman, and J. Handelsman. 2002. Isolation of antibiotics turbomycin A and B from a metagenomic library of soil microbial DNA. Appl. Environ. Microbiol. 68:4301-4306.
41. Gilmour, M. W., K. Bernard, D. M. Tracz, A. B. Olson, C. R. Corbett, T. Burdz, B. Ng, D. Wiebe, G. Broukhanski, P. Boleszczuk, P. Tang, F. Jamieson, G. Van Domselaar, F. A. Plummer, and J. D. Berry. 2007. Molecular typing of a Legionella pneumophila outbreak in Ontario, Canada. J. Med. Microbiol. 56:336-341.
42. Goodwin, P. H., and C. R. Sopher. 1993. Brown pigmentation of Xanthomonas campestris pv. phaseoli associated with homogentisic acid. Can. J. Microbiol. 40:28-34.
43. Grass, G. 2006. Iron transport in Escherichia coli: all has not been said and done. Biometals 19:159-172.
44. Hawkey, P. M., A. McCormick, and R. A. Simpson. 1986. Selective and differential medium for the primary isolation of members of the Proteeae. J. Clin. Microbiol. 23:600-603.
45. Hernandez-Romero, D., F. Solano, and A. Sanchez-Amat. 2005. Polyphenol oxidase activity expression in Ralstonia solanacearum. Appl. Environ. Microbiol. 71:6808-6815.
46. Heuner, K., and M. Steinert. 2003. The flagellum of Legionella pneumophila and its link to the expression of the virulent phenotype. Int. J. Med. Microbiol. 293:133-143.
47. Hickey, E. K., and N. P. Cianciotto. 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.
48. Hodgson, D. A., P. Shaw, and L. Shapiro. 1984. Isolation and genetic analysis of Caulobacter mutants defective in cell shape and membrane lipid synthesis. Genetics 108:809-826.
49. Hoffman, P. S., M. Ripley, and R. Weeratna. 1992. Cloning and nucleotide sequence of a gene (ompS) encoding the major outer membrane protein of Legionella pneumophila. J. Bacteriol. 174:914-920.
50. Homuth, M., P. Valentin-Weigand, M. Rohde, and G. F. Gerlach. 1998. Identification and characterization of a novel extracellular ferric reductase from Mycobacterium paratuberculosis. Infect. Immun. 66:710-716.
51. Jacobson, E. S., and J. D. Hong. 1997. Redox buffering by melanin and Fe(II) in Cryptococcus neoformans. J. Bacteriol. 179:5340- 5346.
52. James, B. W., W. S. Mauchline, P. J. Dennis, and C. W. Keevil. 1997. A study of iron acquisition mechanisms of Legionella pneumophila grown in chemostat culture. Curr. Microbiol. 34:238-243.
53. Johnson, W., L. Varner, and M. Poch. 1991. Acquisition of iron by Legionella pneumophila: role of iron reductase. Infect. Immun. 59:2376-2381.
54. Jung, W. H., A. Sham, R. White, and J. W. Kronstad. 2006. Iron regulation of the major virulence factors in the AIDS-associated pathogen Cryptococcus neoformans. PLoS Biol. 4:2282-2295.
55. Kotob, S. I., S. L. Coon, E. J. Quintero, and R. M. Weiner. 1995. Homogentisic acid is the primary precursor of melanin synthesis in Vibrio cholerae, a Hyphomonas strain, and Shewanella colwelliana. Appl. Environ. Microbiol. 61:1620-1622.
56. Kuroki, H., H. Miyamoto, K. Fukuda, H. Iihara, Y. Kawamura, M. Ogawa, Y. Wang, T. Ezaki, and H. Taniguchi. 2006. Legionella impletisoli sp. nov. and Legionella yabuuchiae sp. nov., isolated from soils contaminated with industrial wastes in Japan. Syst. Appl. Microbiol. 30:273-279.
57. Laguna, R. K., E. A. Creasey, Z. Li, N. Valtz, and R. R. Isberg. 2006. A Legionella pneumophila-translocated substrate that is required for growth within macrophages and protection from host cell death. Proc. Natl. Acad. Sci. USA 103:18745-18750.
58. Lagunas-Munoz, V. H., N. Cabrera-Valladares, F. Bolivar, G. Gosset, and A. Martinez. 2006. Optimum melanin production using recombinant Escherichia coli. J. Appl. Microbiol. 101:1002-1008.
59. La Scola, B., R. J. Birtles, G. Greub, T. J. Harrison, R. M. Ratcliff, and D. Raoult. 2004. Legionella drancourtii sp. nov., a strictly intracellular amoebal pathogen. Int. J. Syst. Evol. Microbiol. 54:699-703.
60. Liles, M. R., T. Aber Scheel, and N. P. Cianciotto. 2000. Discovery of a nonclassical siderophore, legiobactin, produced by strains of Legionella pneumophila. J. Bacteriol. 182:749-757.
61. Liles, M. R., V. K. Viswanathan, and N. P. Cianciotto. 1998. Identification and temperature regulation of Legionella pneumophila genes involved in type IV pilus biogenesis and type II protein secretion. Infect. Immun. 66:1776-1782.
62. Mampel, J., T. Spirig, S. S. Weber, J. A. Haagensen, S. Molin, and H. Hilbi. 2006. Planktonic replication is essential for biofilm formation by Legionella pneumophila in a complex medium under static and dynamic flow conditions. Appl. Environ. Microbiol. 72:2885-2895.
63. Michiels, J., T. Van Soom, I. D'Hooghe, B. Dombrecht, T. Benhassine, P. de Wilde, and J. Vanderleyden. 1998. The Rhizobium etli rpoN locus: DNA sequence analysis and phenotypical characterization of rpoN, ptsN, and ptsA mutants. J. Bacteriol. 180:1729-1740.
64. Milcamps, A., and F. J. de Bruijn. 1999. Identification of a novel nutrient-deprivation-induced Sinorhizobium meliloti gene (hmgA) involved in the degradation of tyrosine. Microbiology 145:935-947.
65. Molmeret, M., M. Horn, M. Wagner, M. Santic, and Y. Abu Kwaik. 2005. Amoebae as training grounds for intracellular bacterial pathogens. Appl. Environ. Microbiol. 71:20-28.
66. Molofsky, A. B., L. M. Shetron-Rama, and M. S. Swanson. 2005. Components of the Legionella pneumophila flagellar regulon contribute to multiple virulence traits, including lysosome avoidance and macrophage death. Infect. Immun. 73:5720-5734.
67. Murata, T., A. Delprato, A. Ingmundson, D. K. Toomre, D. G. Lambright, and C. R. Roy. 2006. The Legionella pneumophila effector protein DrrA is a Rab1 guanine nucleotide-exchange factor. Nat. Cell Biol. 8:971-977.
68. Naylor, J., and N. P. Cianciotto. 2004. Cytochrome c maturation proteins are critical for in vivo growth of Legionella pneumophila. FEMS Microbiol. Lett. 241:249-256.
69. Nevin, K. P., and D. R. Lovley. 2002. Mechanisms for accessing insoluble Fe(III) oxide during dissimilatory Fe(III) reduction by Geothrix fermentans. Appl. Environ Microbiol. 68:2294-2299.
70. Nosanchuk, J. D., and A. Casadevall. 2003. The contribution of melanin to microbial pathogenesis. Cell. Microbiol. 5:203-223.
71. Nosanchuk, J. D., and A. Casadevall. 2006. Impact of melanin on microbial virulence and clinical resistance to antimicrobial compounds. Antimicrob. Agents Chemother. 50:3519-3528.
72. Nyhus, K. J., A. T. Wilborn, and E. S. Jacobson. 1997. Ferric iron reduction by Cryptococcus neoformans. Infect. Immun. 65:434-438.
73. O'Connell, W. A., E. K. Hickey, and N. P. Cianciotto. 1996. A Legionella pneumophila gene that promotes hemin binding. Infect. Immun. 64:842-848.
74. Orrison, L. H., W. B. Cherry, C. B. Fliermans, S. B. Dees, L. K. McDougal, and D. J. Dodd. 1981. Characteristics of environmental isolates of Legionella pneumophila. Appl. Environ. Microbiol. 42:109-115.
75. Page, W. J., and S. Shivprasad. 1995. Iron binding to Azotobacter salinestris melanin, iron mobilization and uptake mediated by siderophores. Biometals 8:59-64.
76. Park, M. Y., K. S. Ko, H. K. Lee, M. S. Park, and Y. H. Kook. 2003. Legionella busanensis sp. nov., isolated from cooling tower water in Korea. Int. J. Syst. Evol. Microbiol. 53:77-80.
77. Pavan, M. E., S. L. Abbott, J. Zorzopulos, and J. M. Janda. 2000. Aeromonas salmonicida subsp. pectinolytica subsp. nov., a new pectinase-positive subspecies isolated from a heavily polluted river. Int. J. Syst. Evol. Microbiol. 50:1119-1124.
78. Pine, L., J. R. George, M. W. Reeves, and W. K. Harrell. 1979. Development of a chemically defined liquid medium for growth of Legionella pneumophila. J. Clin. Microbiol. 9:615-626.
79. Plonka, P. M., and M. Grabacka. 2006. Melanin synthesis in microorganisms - biotechnological and medical aspects. Acta Biochim. Pol. 53:429-443.
80. Poch, M. T., and W. Johnson. 1993. Ferric reductases of Legionella pneumophila. Biometals 6:107-114.
81. Pope, C. D., W. O'Connell, and N. P. Cianciotto. 1996. Legionella pneumophila mutants that are defective for iron acquisition and assimilation and intracellular infection. Infect. Immun. 64:629-636.
82. Reeves, M. W., L. Pine, S. H. Hutner, J. R. George, and W. K. Harrell. 1981. Metal requirements of Legionella pneumophila. J. Clin. Microbiol. 13:688-695.
83. Reeves, M. W., L. Pine, J. B. Neilands, and A. Balows. 1983. Absence of siderophore activity in Legionella species grown in iron-deficient media. J. Bacteriol. 154:324-329.
84. Ridenour, D. A., S. L. Cirillo, S. Feng, M. M. Samrakandi, and J. D. Cirillo. 2003. Identification of a gene that affects the efficiency of host cell infection by Legionella pneumophila in a temperature-dependent fashion. Infect. Immun. 71:6256-6263.
85. Ristroph, J. D., K. W. Hedlund, and S. Gowda. 1981. Chemically defined medium for Legionella pneumophila growth. J. Clin. Microbiol. 13:115-119.
86. Robey, M., and N. P. Cianciotto. 2002. Legionella pneumophila feoAB promotes ferrous iron uptake and intracellular infection. Infect. Immun. 70: 5659-5669.
87. Rossier, O., and N. P. Cianciotto. 2005. The Legionella pneumophila tatB gene facilitates secretion of phospholipase C, growth under iron-limiting conditions, and intracellular infection. Infect. Immun. 73:2020-2032.
88. Rossier, O., S. Starkenburg, and N. P. Cianciotto. 2004. Legionella pneumophila type II protein secretion promotes virulence in the A/J mouse model of Legionnaires' disease pneumonia. Infect. Immun. 72:310-321.
89. Ruebush, S. S., S. L. Brantley, and M. Tien. 2006. Reduction of soluble and insoluble iron forms by membrane fractions of Shewanella oneidensis grown under aerobic and anaerobic conditions. Appl. Environ. Microbiol. 72: 2925-2935.
90. Ruzafa, C., A. Sanchez-Amat, and F. Solano. 1995. Characterization of the melanogenic system in Vibrio cholerae, ATCC 14035. Pigment Cell Res. 8:147-152.
91. Sambrook, J., E. F. Fritsch, and T. Maniatis (ed.). 1989. Molecular cloning: a laboratory manual, 2nd ed., vol. Cold Spring Harbor Laboratory Press, Plainview, NY.
92. Sanchez-Amat, A., C. Ruzafa, and F. Solano. 1998. Comparative tyrosine degradation in Vibrio cholerae strains. The strain ATCC 14035 as a prokaryotic melanogenic model of homogentisate-releasing cell. Comp. Biochem. Physiol. B 119:557-562.
93. Sauer, J. D., J. G. Shannon, D. Howe, S. F. Hayes, M. S. Swanson, and R. A. Heinzen. 2005. Specificity of Legionella pneumophila and Coxiella burnetii vacuoles and versatility of Legionella pneumophila revealed by coinfection. Infect. Immun. 73:4494-4504.
94. Scazzocchio, C. 1997. Alkaptonuria: from humans to moulds and back. Trends Genet. 13:125-127.
95. Shohdy, N., J. A. Efe, S. D. Emr, and H. A. Shuman. 2005. Pathogen effector protein screening in yeast identifies Legionella factors that interfere with membrane trafficking. Proc. Natl. Acad. Sci. USA 102:4866-4871.
96. Starkenburg, S. R., J. M. Casey, and N. P. Cianciotto. 2004. Siderophore activity among members of the Legionella genus. Curr. Microbiol. 49:203-207.
97. Steinert, M., H. Engelhard, M. Flugel, E. Wintermeyer, and J. Hacker. 1995. The Lly protein protects Legionella pneumophila from light but does not directly influence its intracellular survival in Hartmannella vermiformis. Appl. Environ. Microbiol. 61:2428-2430.
98. Steinert, M., M. Flugel, M. Schuppler, J. H. Helbig, A. Supriyono, P. Proksch, and P. C. Luck. 2001. The Lly protein is essential for p-hydroxyphenylpyruvate dioxygenase activity in Legionella pneumophila. FEMS Microbiol. Lett. 203:41-47.
99. Stone, B. J., and Y. Abu Kwaik. 1998. Expression of multiple pili by Legionella pneumophila: identification and characterization of a type IV pilin gene and its role in adherence to mammalian and protozoan cells. Infect. Immun. 66:1768-1775.
100. Tanaka, T., L. Yan, and J. G. Burgess. 2003. Microbulbifer arenaceous sp. nov., a new endolithic bacterium isolated from the inside of red sandstone. Curr. Microbiol. 47:412-416.
101. Turick, C. E., F. Caccavo, Jr., and L. S. Tisa. 2003. Electron transfer from Shewanella algae BrY to hydrous ferric oxide is mediated by cell-associated melanin. FEMS Microbiol. Lett. 220:99-104.
102. Turick, C. E., L. S. Tisa, and F. Caccavo, Jr. 2002. Melanin production and use as a soluble electron shuttle for Fe(III) oxide reduction and as a terminal electron acceptor by Shewanella algae BrY. Appl. Environ. Microbiol. 68:2436-2444.
103. Vartivarian, S. E., and R. E. Cowart. 1999. Extracellular iron reductases: identification of a new class of enzymes by siderophore-producing microorganisms. Arch. Biochem. Biophys. 364:75-82.
104. Vickers, R. M., and V. L. Yu. 1984. Clinical laboratory differentiation of Legionellaceae family members with pigment production and fluorescence on media supplemented with aromatic substrates. J. Clin. Microbiol. 19: 583-587.
105. Vincent, C. D., and J. P. Vogel. 2006. The Legionella pneumophila IcmS-LvgA protein complex is important for Dot/Icm-dependent intracellular growth. Mol. Microbiol. 61:596-613.
106. Viswanathan, V. K., P. H. Edelstein, C. D. Pope, and N. P. Cianciotto. 2000. The Legionella pneumophila iraAB locus is required for iron assimilation, intracellular infection, and virulence. Infect. Immun. 68:1069-1079.
107. Viswanathan, V. K., S. Kurtz, L. L. Pedersen, Y. Abu-Kwaik, K. Krcmarik, S. Mody, and N. P. Cianciotto. 2002. The cytochrome c maturation locus of Legionella pneumophila promotes iron assimilation and intracellular infection and contains a strain-specific insertion sequence element. Infect. Immun. 70:1842-1852.
108. Wagner, C., A. S. Khan, T. Kamphausen, B. Schmausser, C. Unal, U. Lorenz, G. Fischer, J. Hacker, and M. Steinert. 2007. Collagen binding protein Mip enables Legionella pneumophila to transmigrate through a barrier of NCI-H292 lung epithelial cells and extracellular matrix. Cell. Microbiol. 9:450-462.
109. Warren, W. J., and R. D. Miller. 1979. Growth of Legionnaires disease bacterium (Legionella pneumophila) in chemically defined medium. J. Clin. Microbiol. 10:50-55.
110. Weiner, R. M. 1997. Biopolymers from marine prokaryotes. Trends Biotechnol. 15:390-394.
111. Weiner, R. M., A. M. Segall, and R. R. Colwell. 1985. Characterization of a marine bacterium associated with Crassostrea virginica (the Eastern oyster). Appl. Environ. Microbiol. 49:83-90.
112. Wiater, L. A., A. B. Sadosky, and H. A. Shuman. 1994. Mutagenesis of Legionella pneumophila using Tn903 dlllacZ: identification of a growth-phase-regulated pigmentation gene. Mol. Microbiol. 11:641-653.
113. Wintermeyer, E., M. Flugel, M. Ott, M. Steinert, U. Rdest, K. H. Mann, and J. Hacker. 1994. Sequence determination and mutational analysis of the lly locus of Legionella pneumophila. Infect. Immun. 62:1109-1117.
114. Wintermeyer, E., U. Rdest, B. Ludwig, A. Debes, and J. Hacker. 1991. Characterization of legiolysin (lly), responsible for haemolytic activity, colour production and fluorescence of Legionella pneumophila. Mol. Microbiol. 5:1135-1143.
115. Zughaier, S. M., H. C. Ryley, and S. K. Jackson. 1999. A melanin pigment purified from an epidemic strain of Burkholderia cepacia attenuates monocyte respiratory burst activity by scavenging superoxide anion. Infect. Immun. 67:908-913.
116. Zusman, T., O. Gal-Mor, and G. Segal. 2002. Characterization of a Legionella pneumophila relA insertion mutant and roles of RelA and RpoS in virulence gene expression. J. Bacteriol. 184:67-75.