This Article Full Text Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Reprints and Permissions Copyright Information Books from ASM Press MicrobeWorld Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Reverchon, S. Articles by Nasser, W. Search for Related Content PubMed PubMed Citation Articles by Reverchon, S. Articles by Nasser, W.

Characterization of Indigoidine Biosynthetic Genes in Erwinia chrysanthemi and Role of This Blue Pigment in Pathogenicity

Unité de Microbiologie et Génétique CNRS-INSA-UCB UMR 5122, INSA, 69621 Villeurbanne Cedex,¹ Laboratoire de Pathologie Végétale, UMR 217 INRA/INA P-G/Université Paris 6, 75231 Paris Cedex 05, France²

Received 22 June 2001/ Accepted 29 October 2001

In the plant-pathogenic bacterium Erwinia chrysanthemi production of pectate lyases, the main virulence determinant, is modulated by a complex network involving several regulatory proteins. One of these regulators, PecS, also controls the synthesis of a blue pigment identified as indigoidine. Since production of this pigment is cryptic in the wild-type strain, E. chrysanthemi ind mutants deficient in indigoidine synthesis were isolated by screening a library of Tn5-B21 insertions in a pecS mutant. These ind mutations were localized close to the regulatory pecS-pecM locus, immediately downstream of pecM. Sequence analysis of this DNA region revealed three open reading frames, indA, indB, and indC, involved in indigoidine biosynthesis. No specific function could be assigned to IndA. In contrast, IndB displays similarity to various phosphatases involved in antibiotic synthesis and IndC reveals significant homology with many nonribosomal peptide synthetases (NRPS). The IndC product contains an adenylation domain showing the signature sequence DAWCFGLI for glutamine recognition and an oxidation domain similar to that found in various thiazole-forming NRPS. These data suggest that glutamine is the precursor of indigoidine. We assume that indigoidine results from the condensation of two glutamine molecules that have been previously cyclized by intramolecular amide bond formation and then dehydrogenated. Expression of ind genes is strongly derepressed in the pecS background, indicating that PecS is the main regulator of this secondary metabolite synthesis. DNA band shift assays support a model whereby the PecS protein represses indA and indC expression by binding to indA and indC promoter regions. The regulatory link, via pecS, between indigoidine and virulence factor production led us to explore a potential role of indigoidine in E. chrysanthemi pathogenicity. Mutants impaired in indigoidine production were unable to cause systemic invasion of potted Saintpaulia ionantha. Moreover, indigoidine production conferred an increased resistance to oxidative stress, indicating that indigoidine may protect the bacteria against the reactive oxygen species generated during the plant defense response.

This article has been cited by other articles:

• Hussain, M. B. B. M., Zhang, H.-B., Xu, J.-L., Liu, Q., Jiang, Z., Zhang, L.-H. (2008). The Acyl-Homoserine Lactone-Type Quorum-Sensing System Modulates Cell Motility and Virulence of Erwinia chrysanthemi pv. zeae. J. Bacteriol. 190: 1045-1053 [Abstract] [Full Text]  
• Lawrenz, M. B., Miller, V. L. (2007). Comparative Analysis of the Regulation of rovA from the Pathogenic Yersiniae. J. Bacteriol. 189: 5963-5975 [Abstract] [Full Text]  
• Takahashi, H., Kumagai, T., Kitani, K., Mori, M., Matoba, Y., Sugiyama, M. (2007). Cloning and Characterization of a Streptomyces Single Module Type Non-ribosomal Peptide Synthetase Catalyzing a Blue Pigment Synthesis. J. Biol. Chem. 282: 9073-9081 [Abstract] [Full Text]  
• Wei, K., Tang, D.-J., He, Y.-Q., Feng, J.-X., Jiang, B.-L., Lu, G.-T., Chen, B., Tang, J.-L. (2007). hpaR, a Putative marR Family Transcriptional Regulator, Is Positively Controlled by HrpG and HrpX and Involved in the Pathogenesis, Hypersensitive Response, and Extracellular Protease Production of Xanthomonas campestris Pathovar campestris. J. Bacteriol. 189: 2055-2062 [Abstract] [Full Text]  
• Krin, E., Chakroun, N., Turlin, E., Givaudan, A., Gaboriau, F., Bonne, I., Rousselle, J.-C., Frangeul, L., Lacroix, C., Hullo, M.-F., Marisa, L., Danchin, A., Derzelle, S. (2006). Pleiotropic Role of Quorum-Sensing Autoinducer 2 in Photorhabdus luminescens.. Appl. Environ. Microbiol. 72: 6439-6451 [Abstract] [Full Text]  
• Venkatesh, B., Babujee, L., Liu, H., Hedley, P., Fujikawa, T., Birch, P., Toth, I., Tsuyumu, S. (2006). The Erwinia chrysanthemi 3937 PhoQ Sensor Kinase Regulates Several Virulence Determinants.. J. Bacteriol. 188: 3088-3098 [Abstract] [Full Text]  
• Beck, D. L., Boettner, D. R., Dragulev, B., Ready, K., Nozaki, T., Petri, W. A. Jr. (2005). Identification and Gene Expression Analysis of a Large Family of Transmembrane Kinases Related to the Gal/GalNAc Lectin in Entamoeba histolytica. Eukaryot Cell 4: 722-732 [Abstract] [Full Text]  
• Brencic, A., Winans, S. C. (2005). Detection of and Response to Signals Involved in Host-Microbe Interactions by Plant-Associated Bacteria. Microbiol. Mol. Biol. Rev. 69: 155-194 [Abstract] [Full Text]  
• Wilkinson, S. P., Grove, A. (2004). HucR, a Novel Uric Acid-responsive Member of the MarR Family of Transcriptional Regulators from Deinococcus radiodurans. J. Biol. Chem. 279: 51442-51450 [Abstract] [Full Text]  
• Rouanet, C., Reverchon, S., Rodionov, D. A., Nasser, W. (2004). Definition of a Consensus DNA-binding Site for PecS, a Global Regulator of Virulence Gene Expression in Erwinia chrysanthemi and Identification of New Members of the PecS Regulon. J. Biol. Chem. 279: 30158-30167 [Abstract] [Full Text]  
• Hugouvieux-Cotte-Pattat, N., Shevchik, V. E., Nasser, W. (2002). PehN, a Polygalacturonase Homologue with a Low Hydrolase Activity, Is Coregulated with the Other Erwinia chrysanthemi Polygalacturonases. J. Bacteriol. 184: 2664-2673 [Abstract] [Full Text]