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Infection and Immunity, August 2007, p. 4062-4070, Vol. 75, No. 8
0019-9567/07/$08.00+0     doi:10.1128/IAI.00489-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

The Secreted Pyomelanin Pigment of Legionella pneumophila Confers Ferric Reductase Activity{triangledown}

Christa H. Chatfield and Nicholas P. Cianciotto*

Department of Microbiology-Immunology, Northwestern University Medical School, Chicago, Illinois 60611

Received 5 April 2007/ Returned for modification 8 May 2007/ Accepted 18 May 2007

The virulence of Legionella pneumophila is dependent upon its capacity to acquire iron. To identify genes involved in expression of its siderophore, we screened a mutagenized population of L. pneumophila for strains that were no longer able to rescue the growth of a ferrous transport mutant. However, an unusual mutant was obtained that displayed a strong inhibitory effect on the feoB mutant. Due to an insertion in hmgA that encodes homogentisate 1,2-dioxygenase, the mutant secreted increased levels of pyomelanin, the L. pneumophila pigment that is derived from secreted homogentisic acid (HGA). Thus, we hypothesized that L. pneumophila-secreted HGA-melanin has intrinsic ferric reductase activity, converting Fe3+ to Fe2+, but that hyperpigmentation results in excessive reduction of iron that can, in the case of the feoB mutant, be inhibitory to growth. In support of this hypothesis, we demonstrated, for the first time, that wild-type L. pneumophila secretes ferric reductase activity. Moreover, whereas the hyperpigmented mutant had increased secreted activity, an lly mutant specifically impaired for pigment production lacked the activity. Compatible with the nature of HGA-melanins, the secreted ferric reductase activity was positively influenced by the amount of tyrosine in the growth medium, resistant to protease, acid precipitable, and heterogeneous in size. Together, these data represent the first demonstration of pyomelanin-mediated ferric reduction by a pathogenic bacterium.

* Corresponding author. Mailing address: Department of Microbiology-Immunology, Northwestern University Medical School, 320 East Superior Street, Chicago, IL 60611-3010. Phone: (312) 503-0385. Fax: (312) 503-1339. E-mail: n-cianciotto{at}northwestern.edu

{triangledown} Published ahead of print on 4 June 2007.

Editor: D. L. Burns

Infection and Immunity, August 2007, p. 4062-4070, Vol. 75, No. 8
0019-9567/07/$08.00+0     doi:10.1128/IAI.00489-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Allard, K. A., Dao, J., Sanjeevaiah, P., McCoy-Simandle, K., Chatfield, C. H., Crumrine, D. S., Castignetti, D., Cianciotto, N. P. (2009). Purification of Legiobactin and Importance of This Siderophore in Lung Infection by Legionella pneumophila. Infect. Immun. 77: 2887-2895 [Abstract] [Full Text]  
  • Valeru, S. P., Rompikuntal, P. K., Ishikawa, T., Vaitkevicius, K., Sjoling, A., Dolganov, N., Zhu, J., Schoolnik, G., Wai, S. N. (2009). Role of Melanin Pigment in Expression of Vibrio cholerae Virulence Factors. Infect. Immun. 77: 935-942 [Abstract] [Full Text]  
  • Stewart, C. R., Rossier, O., Cianciotto, N. P. (2009). Surface Translocation by Legionella pneumophila: a Form of Sliding Motility That Is Dependent upon Type II Protein Secretion. J. Bacteriol. 191: 1537-1546 [Abstract] [Full Text]  


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