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http://dx.doi.org/10.4014/jmb.0810.574

Regulation of the Edwardsiella tarda Hemolysin Gene and luxS by EthR  

Fang, Wang (Institute of Oceanology, Chinese Academy of Sciences)
Zhang, Min (Institute of Oceanology, Chinese Academy of Sciences)
Hu, Yong-Hua (Institute of Oceanology, Chinese Academy of Sciences)
Zhang, Wei-wei (Institute of Oceanology, Chinese Academy of Sciences)
Sun, Li (Institute of Oceanology, Chinese Academy of Sciences)
Publication Information
Journal of Microbiology and Biotechnology / v.19, no.8, 2009 , pp. 765-773 More about this Journal
Abstract
Edwardsiella tarda is a pathogen with a broad host range that includes human and animals. The E. tarda hemolysin (Eth) system, which comprises EthA and EthB, is a noted virulence element that is widely distributed in pathogenic isolates of E. tarda. Previous study has shown that the expression of ethB is regulated by iron, which suggests the possibility that the ferric uptake regulator (Fur) is involved in the regulation of ethB. The work presented in this report supports the previous findings and demonstrates that ethB expression was decreased under conditions when the E. tarda Fur ($Fur_{Et}$) was overproduced, and enhanced when $Fur_{Et}$ was inactivated. We also identified a second ethB regulator, EthR, which is a transcription regulator of the GntR family. EthR represses ethB expression by direct interaction with the ethB promoter region. In addition to ethB, EthR also modulates, but positively, luxS expression and AI-2 production by binding to the luxS promoter region. The expression of ethR itself is subject to negative autoregulation; interference with this regulation by overexpressing ethR during the process of infection caused (i) drastic changes in ethB and luxS expressions, (ii) vitiation in the tissue dissemination and survival ability of the bacterium, and (iii) significant attenuation of the overall bacterial virulence. These results not only provide new insights into the regulation mechanisms of the Eth hemolysin and LuxS/AI-2 quorum sensing systems but also highlight the importance of these systems in bacterial virulence.
Keywords
Edwardsiella tarda; hemolysin; luxS; RNAi; virulence;
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1 Casali, N., A. M. White, and L. W. Riley. 2006. Regulation of the Mycobacterium tuberculosis mce1 operon. J. Bacteriol. 188: 441-449   DOI   ScienceOn
2 Gebhard, S. and G. M. Cook. 2008. Differential regulation of high-affinity phosphate transport systems of Mycobacterium smegmatis: Identification of PhnF, a repressor of the phnDCE operon. J. Bacteriol. 190: 1335-1343   DOI   ScienceOn
3 Haine, V., A. Sinon, F. Van Steen, S. Rousseau, M. Dozot, P. Lestrate, C. Lambert, J. Letesson, and X. De Bolle. 2005. Systematic targeted mutagenesis of Brucella melitensis 16M reveals a major role for GntR regulators in the control of virulence. Infect. Immun. 73: 5578-5586   DOI   ScienceOn
4 Jaques, S. and L. L. McCarter. 2006. Three new regulators of swarming in Vibrio parahaemolyticus. J. Bacteriol. 188: 2625- 2635   DOI   ScienceOn
5 Livak, K. J. and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the $2^{{-{\bigtriangleup}{\bigtriangleup}}CT}$ method. Methods 25: 402-408   DOI   ScienceOn
6 Srinivasa Rao, P. S., Y. Yamada, and K. Y. Leung. 2003. A major catalase (KatB) that is required for $H_2O_2$ and phagocytemediated killing in Edwardsiella tarda. Microbiology 149: 2635-2644   DOI   ScienceOn
7 Tan, Y. P., J. Zheng, S. L. Tung, I. Rosenshine, and K. Y. Leung. 2005. Role of type III secretion in Edwardsiella tarda virulence. Microbiology 151: 2301-2313   DOI   ScienceOn
8 Gorelik, M., V. V. Lunin, T. Skarina, and A. Savchenko. 2006. Structural characterization of GntR/HutC family signaling domain. Protein Sci. 15: 1506-1511   DOI   ScienceOn
9 Miller, J. H. 1972. Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
10 Janda, J. M. and S. L. Abbott. 1993. Expression of an ironregulated hemolysin by Edwardsiella tarda. FEMS Microbiol. Lett. 111: 275-280   DOI   PUBMED   ScienceOn
11 Banks, A. S. 1992. A puncture wound complicated by infection with Edwardsiella tarda. J. Am. Pediatr. Med. Assoc. 82: 529- 531   DOI   PUBMED   ScienceOn
12 Fujita, Y., T. Fujita, Y. Miwa, J. I. Nihashi, and Y. Aratani. 1986. Organization and transcription of the gluconate operon, gnt, of Bacillus subtilis. J. Biol. Chem. 261: 13744-13753   PUBMED
13 Hillerich, B. and J. Westpheling. 2006. A new GntR family transcriptional regulator in Streptomyces coelicolor is required for morphogenesis and antibiotic production and controls transcription of an ABC transporter in response to carbon source. J. Bacteriol. 188: 7477-7487   DOI   ScienceOn
14 Schauder, S., K. Shokat, M. G. Surette, and B. L. Bassler. 2001. The LuxS family of bacterial autoinducers: Biosynthesis of a novel quorum-sensing signal molecule. Mol. Microbiol. 41: 463-476   DOI   ScienceOn
15 Janda, J. M., S. L. Abott, S. Kroshe-Bystrom, W. K. W. Cheng, C. Powers, R. P. Kokka, and K. Tamura. 1991. Pathogenic properties of Edwardsiella species. J. Clin. Microbiol. 29: 1977-2001
16 Hoskisson, P. A., S. Rigali, K. Fowler, K. C. Findlay, and M. J. Buttner. 2006. DevA, a GntR-like transcriptional regulator required for development in Streptomyces coelicolor. J. Bacteriol. 188: 5014-5023   DOI   ScienceOn
17 Hirono, I., N. Tange, and T. Aoki. 1997. Iron regulated hemolysin gene from Edwardsiella tarda. Mol. Microbiol. 24: 851-856   DOI   ScienceOn
18 Vendeville, A., K. Winzer, K. Heurlier, C. M. Tang, and K. R. Hardie. 2005. Making 'sense' of metabolism: Autoinducer-2, LuxS and pathogenic bacteria. Nat. Rev. Microbiol. 3: 383-396   DOI   ScienceOn
19 Fineran, P. C., L. Everson, H. Slater, and G. P. C. Salmond. 2005. A GntR family transcriptional regulator (PigT) controls gluconate-mediated repression and defines a new, independent pathway for regulation of the tripyrrole antibiotic, prodigiosin, in Serratia. Microbiology 151: 3833-3845   DOI   ScienceOn
20 Surette, M. G. and B. L. Bassler. 1999. Regulation of autoinducer production in Salmonella typhimurium. Mol. Microbiol. 31: 585-595   DOI   ScienceOn
21 Rigali, S., H. Nothaft, E. E. Noens, M. Schlicht, S. Colson, M. Muller, et al. 2006. The sugar phosphotransferase system of Streptomyces coelicolor is regulated by the GntR-family regulator DasR and links N-acetylglucosamine metabolism to the control of development. Mol. Microbiol. 61: 1237-1251   DOI   ScienceOn
22 Sun, L., J. vanderSpek, and J. R. Murphy. 1998. Isolation and characterization of iron-independent positive dominant mutants of Diphtheria toxin repressor, DtxR. Proc. Natl. Acad. Sci. U.S.A. 95: 14985-14990   DOI   ScienceOn
23 Wiethaus, J., B. Schubert, Y. Pfander, F. Narberhaus, and B. Masepohl. 2008. The GntR-like regulator TauR activates expression of taurine utilization genes in Rhodobacter capsulatus. J. Bacteriol. 190: 487-493   DOI   ScienceOn
24 Miyazaki, T. and N. Kaige. 1985. Comparative histopathology of edwardsiellosis in fishes. Fish Pathol. 20: 219-227   DOI
25 Zhang, W. and L. Sun. 2007. Cloning, characterization and molecular application of a beta-agarase gene from Vibrio sp. strain V134. Appl. Environ. Microbiol. 73: 2825-2831   DOI   ScienceOn
26 Murray, E. L. and T. Conway. 2005. Multiple regulators control expression of the Entner-Doudoroff aldolase (Eda) of Escherichia coli. J. Bacteriol. 187: 991-1000   DOI   ScienceOn
27 Rigali, S., A. Derouaux, F. Giannotta, and J. Dusart. 2002. Subdivision of the helix-turn-helix GntR family of bacterial regulators in FadR, HutC, MocR and YtrA sub-families. J. Biol. Chem. 277: 12507-12515   DOI   ScienceOn
28 Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual, 2nd Ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
29 Hamza, I., S. Chauhan, R. Hassett, and M. R. O'Brian. 1998. The bacterial Irr protein is required for coordination of heme biosynthesis with iron availability. J. Biol. Chem. 273: 21669- 21674   DOI   ScienceOn
30 Wang, F., S. Cheng, K. Sun, and L. Sun. 2008. Molecular analysis of the fur (ferric uptake regulator) gene of a pathogenic Edwardsiella tarda strain. J. Microbiol. 46: 350-355   DOI   ScienceOn
31 Zheng, J. and K. Y. Leung. 2007. Dissection of a type VI secretion system in Edwardsiella tarda. Mol. Microbiol. 66: 1192-1206   DOI   ScienceOn
32 Winzer, K., K. R. Hardie, N. Burgess, N. Doherty, D. Kirke, M. T. Holden, et al. 2002. LuxS: Its role in central metabolism and the in vitro synthesis of 4-hydroxy-5-methyl-3(2H)-furanone. Microbiology 148: 909-922   DOI   PUBMED   ScienceOn
33 Hanssler, E., T. Muller, N. Jessberger, A. Volzke, J. Plassmeier, J. Kalinowski, R. Kramer, and A. Burkovski. 2007. FarR, a putative regulator of amino acid metabolism in Corynebacterium glutamicum. Appl. Microbiol. Biotechnol. 76: 625-632   DOI   ScienceOn
34 Slaven, E. M., F. A. Lopez, S. M. Hart, and C. V. Sanders. 2001. Myonecrosis caused by Edwardsiella tarda: A case report and case series of extraintestinal E. tarda infections. Clin. Infect. Dis. 32: 1430-1433   DOI   ScienceOn
35 Zhang, M., K. Sun, and L. Sun. 2008. Regulation of autoinducer 2 production and luxS expression in a pathogenic Edwardsiella tarda strain. Microbiology 154: 2060-2069   DOI   PUBMED   ScienceOn
36 Lin, J. W., H. C. Lu, H. Y. Chen, and S. F. Weng. 1997. The pkI gene encoding pyruvate kinase I links to the luxZ gene which enhances bioluminescence of the lux operon from Photobacterium leiognathi. Biochem. Biophys. Res. Commun. 239: 228-234   DOI   ScienceOn
37 Frunzke, J., V. Engels, S. Hasenbein, C. Gatgens, and M. Bott. 2008. Co- rdinated regulation of gluconate catabolism and glucose uptake in orynebacterium glutamicum by two functionally equivalent transcriptional egulators, GntR1 and GntR2. Mol. Microbiol. 190: 1335-1343
38 Kalivoda, K. A., S. M. Steenbergen, E. R. Vimr, and J. Plumbridge. 2003. Regulation of sialic acid catabolism by the DNA binding protein NanR in Escherichia coli. J. Bacteriol. 185: 4806-4815   DOI   ScienceOn
39 Hantke, K. 2001. Iron and metal regulation in bacteria. Curr. Opin. Microbiol. 4: 172-177   DOI   PUBMED   ScienceOn
40 Ullah, M. A. and T. Arai. 1983. Pathological activities of the naturally occurring strains of Edwardsiella tarda. Fish Pathol. 18: 65-70   DOI
41 Reizer, A., J. Deutscher, M. H. Saier, and J. Reizer. 1991. Analysis of the gluconate (gnt) operon of Bacillus subtilis. Mol. Microbiol. 5: 1081-1089   DOI   ScienceOn