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Cyclic AMP-receptor protein activates aerobactin receptor IutA expression in Vibrio vulnificus

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Abstract

The ferrophilic bacterium Vibrio vulnificus can utilize the siderophore aerobactin of Escherichia coli for iron acquisition via its specific receptor IutA. This siderophore piracy by V. vulnificus may contribute to its survival and proliferation, especially in mixed bacterial environments. In this study, we examined the effects of glucose, cyclic AMP (cAMP), and cAMP-receptor protein (Crp) on iutA expression in V. vulnificus. Glucose dose-dependently repressed iutA expression. A mutation in cya encoding adenylate cyclase required for cAMP synthesis severely repressed iutA expression, and this change was recovered by in trans complementing cya or the addition of exogenous cAMP. Furthermore, a mutation in crp encoding Crp severely repressed iutA expression, and this change was recovered by complementing crp. Accordingly, glucose deprivation under iron-limited conditions is an environmental signal for iutA expression, and Crp functions as an activator that regulates iutA expression in response to glucose availability.

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References

  • Andrews, S.C., Robinson, A.K., and Rodriguez-Quinones, F. 2003. Bacterial iron homeostasis. FEMS Microbiol. Rev. 27, 215–237.

    Article  PubMed  CAS  Google Scholar 

  • Aso, H., Miyoshi, S., Nakao, H., Okamoto, K., and Yamamoto, S. 2002. Induction of an outer membrane protein of 78 kDa in Vibrio vulnificus in the presence of desferrioxamine B under iron-limiting conditions. FEMS Microbiol. Lett. 212, 65–70.

    Article  PubMed  CAS  Google Scholar 

  • Choi, M.H., Sun, H.Y., Park, R.Y., Kim, C.M., Bai Y.H., Kim, Y.R., Rhee, J.H., and Shin, S.H. 2006. Effect of the crp mutation on the utilization of transferrin-bound iron by Vibrio vulnificus. FEMS Microbiol. Lett. 257, 285–292.

    Article  PubMed  CAS  Google Scholar 

  • Deutscher, J. 2008. The mechanisms of carbon catabolite repression in bacteria. Curr. Opin. Microbiol. 11, 87–93.

    Article  PubMed  CAS  Google Scholar 

  • Ditta, G., Stanfield, S., Corbin, D., and Helinski, D.R. 1980. Broad host range cloning system for Gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc. Natl. Acad. Sci. USA 27, 7347–7351.

    Article  Google Scholar 

  • Hantke, K. 2001. Iron and metal regulation in bacteria. Curr. Opin. Microbiol. 4, 172–177.

    Article  PubMed  CAS  Google Scholar 

  • Jones, M.K. and Oliver J.D. 2009. Vibrio vulnificus: disease and pathogenesis. Infect. Immun. 77, 1723–1733.

    Article  PubMed  CAS  Google Scholar 

  • Kim, C.M., Chung, Y.Y., and Shin, S.H. 2009. Iron differentially regulates gene expression and extracellular secretion of Vibrio vulnificus cytolysin-hemolysin. J. Infect. Dis. 200, 582–589.

    Article  PubMed  CAS  Google Scholar 

  • Kim, S.Y., Lee, S.E., Kim, Y.R., Kim, C.M., Ryu, P.Y., Choy, H.E., Chung, S.S., and Rhee, J.H. 2003. Regulation of Vibrio vulnificus virulence by LuxS quorum-sensing system. Mol. Microbiol. 48, 1647–1664.

    Article  PubMed  CAS  Google Scholar 

  • Kim, C.M., Park, R.Y., Choi, M.H., Sun, H.Y., and Shin, S.H. 2007. Ferrophilic characteristics of Vibrio vulnificus and potential usefulness of iron chelation therapy. J. Infect. Dis. 195, 90–99.

    Article  PubMed  CAS  Google Scholar 

  • Kim, C.M., Park, R.Y., Park, J.H., Sun, H.Y., Bai, Y.H., Ryu, P.Y., Kim, S.Y., Rhee J.H., and Shin, S.H. 2006. Vibrio vulnificus vulnibactin, but not metalloprotease VvpE, is essentially required for iron-uptake from holotransferrin. Biol. Pharm. Bull. 29, 911–918.

    Article  PubMed  CAS  Google Scholar 

  • Kim, C.M., Park, Y.J., and Shin, S.H. 2007. A widespread deferoxamine-mediated iron-uptake system in Vibrio vulnificus. J. Infect. Dis. 196, 1537–1545.

    Article  PubMed  CAS  Google Scholar 

  • Kim, C.M. and Shin, S.H. 2011. Modulation of iron-uptake systems by a mutation of luxS encoding an autoinducer-2 synthase in Vibrio vulnificus. Biol. Pharm. Bull. 34, 632–637.

    Article  PubMed  CAS  Google Scholar 

  • Leong, S.A. and Neilands, J.B. 1982. Siderophore production by phytopathogenic microbial species. Arch. Biochem. Biophys. 218, 351–359.

    Article  PubMed  CAS  Google Scholar 

  • Lesic, B., Foulon, J., and Carniel, E. 2002. Comparison of the effect of deferiprone versus deferoxamine on growth and virulence of Yersinia enterocolitica. Antimicrob. Agents Chemother. 46, 1741–1745.

    Article  PubMed  CAS  Google Scholar 

  • Litwin, C.M. and Byrne, B.L. 1998. Cloning and characterization of an outer membrane protein of Vibrio vulnificus required for haem utilization: regulation of expression and determination of the gene sequence. Infect. Immun. 66, 3134–3141.

    PubMed  CAS  Google Scholar 

  • Litwin, C.M. and Calderwood, S.B. 1993. Cloning and genetic analysis of the Vibrio vulnificus fur gene and construction of a fur mutant by in vivo marker exchange. J. Bacteriol. 175, 706–715.

    PubMed  CAS  Google Scholar 

  • Litwin, C.M. and Quackenbush, J. 2001. Characterization of a Vibrio vulnificus LysR homologue, HupR, which regulates expression of the haem uptake outer membrane protein, HupA. Microb. Pathog. 31, 295–307.

    Article  PubMed  CAS  Google Scholar 

  • Litwin, C.M., Rayback, T.W., and Skinner, J. 1996. Role of catechol siderophore synthesis in Vibrio vulnificus virulence. Infect. Immun. 64, 2834–2838.

    PubMed  CAS  Google Scholar 

  • McGee, K., Horstedt, P., and Milton, D.L. 1996. Identification and characterization of additional flagellin genes from Vibrio anguillarum. J. Bacteriol. 178, 5188–5198.

    PubMed  CAS  Google Scholar 

  • Miller, J.H. 1992. A short course in bacterial genetics: a laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, N.Y., USA.

    Google Scholar 

  • Miller, V.L. and Mekalanos, J.J. 1988. A novel suicide vector and its use in construction of insertion mutations: Osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170, 2575–2583.

    PubMed  CAS  Google Scholar 

  • Oh, M.H., Lee, S.M., Lee, D.H., and Choi, S.H. 2009. Regulation of the Vibrio vulnificus hupA gene by temperature alteration and cyclic AMP receptor protein and evaluation of its role in virulence. Infect. Immun. 77, 1208–1215.

    Article  PubMed  CAS  Google Scholar 

  • Reddy, G.P., Hayat, U., Abeygunawardana, C., Fox, C., Wright, A.C., Raneval, D.R.Jr., Bush, C.A., and Morris, J.G.Jr. 1992. Purification and determination of the structure of capsular polysaccharide of Vibrio vulnificus M06-24/O. J. Bacteriol. 174, 2620–2630.

    PubMed  CAS  Google Scholar 

  • Schubert, S., Fischer, D., and Heesemann, J. 1999. Ferric enterochelin transport in Yersinia enterocolitica: Molecular and evolutionary aspects. J. Bacteriol. 181, 6387–6395.

    PubMed  CAS  Google Scholar 

  • Sebulsky, M.T., Hohnstein, D., Hunter, M.D., and Heinrichs, D.E. 2000. Identification and characterization of a membrane permease involved in iron-hydroxamate transport in Staphylococcus aureus. J. Bacteriol. 182, 4394–4400.

    Article  PubMed  CAS  Google Scholar 

  • Stookey, L.I. 1970. Ferrozine-a new spectrophotometric reagent for iron. Anal. Chem. 42, 779–781.

    Article  CAS  Google Scholar 

  • Takata, T., Takata, N., Naka, A., Moon, Y.H., Nakao, H., Ionue, Y., Narimatsu, S., and Yamamoto, S. 2005. Identification of an AraC-like regulator gene required for induction of the 78-kDa ferrioxamine B receptor in Vibrio vulnificus. FEMS Microbiol. Lett. 249, 309–314.

    Article  PubMed  Google Scholar 

  • Tanabe, T., Naka, A., Aso, H., Nakao, H., Narimatsu, S., Inoue, Y., Ono, T., and Yamamoto, S. 2005. A novel aerobactin utilization cluster in Vibrio vulnificus with a gene involved in the transcription regulation of the iutA homologue. Microbiol. Immunol. 49, 823–834.

    PubMed  CAS  Google Scholar 

  • Webster, A.C.D. and Litwin, C.M. 2000. Cloning and characterization of vuuA, a gene encoding Vibrio vulnificus ferric vulnibactin receptor. Infect. Immun. 68, 526–534.

    Article  PubMed  CAS  Google Scholar 

  • Weinberg, E.D. 2000. Microbial pathogens with impaired ability to acquire host iron. BioMetals 13, 85–89.

    Article  PubMed  CAS  Google Scholar 

  • Wright, A.C., Simpson, L.M., and Oliver, J.D. 1981. Role of iron in the pathogenesis of Vibrio vulnificus infections. Infect. Immun. 34, 503–507.

    PubMed  CAS  Google Scholar 

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Correspondence to Sung-Heui Shin.

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These authors contributed equally to this work.

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Kim, CM., Kim, SJ. & Shin, SH. Cyclic AMP-receptor protein activates aerobactin receptor IutA expression in Vibrio vulnificus . J Microbiol. 50, 320–325 (2012). https://doi.org/10.1007/s12275-012-2056-y

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