Identification and characterization of a periplasmic trilactone esterase, Cee, revealed unique features of ferric enterobactin acquisition in Campylobacter

Molecular Microbiology

Volumn 87, Issue 3, 2013, Pages 594-608

  Zeng, Ximin ^a   Mo, Yiming ^a   Xu, Fuzhou ^a,b   Lin, Jun ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

^b INSTITUTE OF PLANT AND ENVIRONMENT PROTECTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; BACTERIAL PROTEIN; CAMPYLOBACTER ENTEROBACTIN ESTERASE; ENTEROCHELIN; ENZYME ANTIBODY; ESTERASE; LACTONE; PROTEIN CEE ANTIBODY; PROTEIN CFRA; PROTEIN CFRB; PROTEIN IROD; PROTEIN IROE; PROTEIN KINASE FES; UNCLASSIFIED DRUG;

ANTIBODY SPECIFICITY; ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BIOASSAY; CAMPYLOBACTER JEJUNI; CATALYSIS; COMPARATIVE GENOMIC ANALYSIS; CONTROLLED STUDY; CYTOPLASM; ENZYME ANALYSIS; ENZYME LOCALIZATION; ENZYME PURIFICATION; ENZYME STRUCTURE; GENE SEQUENCE; GENETIC MANIPULATION; GENOMICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOBLOTTING; IRON METABOLISM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN HYDROLYSIS; PROTEIN STRUCTURE; SCAVENGING SYSTEM; SEQUENCE HOMOLOGY; THIN LAYER CHROMATOGRAPHY;

CAMPYLOBACTER JEJUNI; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CHROMATOGRAPHY, THIN LAYER; ENTEROBACTIN; ESTERASES; GENOME, BACTERIAL; HYDROLYSIS; KINETICS; LACTONES; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PERIPLASMIC PROTEINS; SEQUENCE ANALYSIS, DNA;

CAMPYLOBACTER; CAMPYLOBACTER COLI; CAMPYLOBACTER JEJUNI; NEGIBACTERIA;

EID: 84873056868     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12118     Document Type: Article

References (50)

1. Akiba, M., Lin, J., Barton, Y.W., and Zhang, Q. (2006) Interaction of CmeABC and CmeDEF in conferring antimicrobial resistance and maintaining cell viability in Campylobacter jejuni. J Antimicrob Chemother 57: 52-60.
2. Anderson, M.T., and Armstrong, S.K. (2004) The BfeR regulator mediates enterobactin-inducible expression of Bordetella enterobactin utilization genes. J Bacteriol 186: 7302-7311.
3. Aziz, R.K., Bartels, D., Best, A.A., DeJongh, M., Disz, T., Edwards, R.A., etal. (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9: 75.
4. Baumler, A.J., Tsolis, R.M., van der Velden, A.W., Stojiljkovic, I., Anic, S., and Heffron, F. (1996) Identification of a new iron regulated locus of Salmonella typhi. Gene 183: 207-213.
5. Brickman, T.J., and McIntosh, M.A. (1992) Overexpression and purification of ferric enterobactin esterase from Escherichia coli. Demonstration of enzymatic hydrolysis of enterobactin and its iron complex. J Biol Chem 267: 12350-12355.
6. Caza, M., Lepine, F., Milot, S., and Dozois, C.M. (2008) Specific roles of the iroBCDEN genes in virulence of an avian pathogenic Escherichia coli O78 strain and in production of salmochelins. Infect Immun 76: 3539-3549.
7. Chaudhuri, R.R., Loman, N.J., Snyder, L.A., Bailey, C.M., Stekel, D.J., and Pallen, M.J. (2008) xBASE2: a comprehensive resource for comparative bacterial genomics. Nucleic Acids Res 36: D543-D546.
8. Coward, C., van Diemen, P.M., Conlan, A.J., Gog, J.R., Stevens, M., Jones, M.A., and Maskell, D.J. (2008) Competing isogenic Campylobacter strains exhibit variable population structures in vivo. Appl Environ Microbiol 74: 3857-3867.
9. Crossley, R.A., Gaskin, D.J., Holmes, K., Mulholland, F., Wells, J.M., Kelly, D.J., etal. (2007) Riboflavin biosynthesis is associated with assimilatory ferric reduction and iron acquisition by Campylobacter jejuni. Appl Environ Microbiol 73: 7819-7825.
10. Darling, A.C., Mau, B., Blattner, F.R., and Perna, N.T. (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14: 1394-1403.
11. Field, L.H., Headley, V.L., Payne, S.M., and Berry, L.J. (1986) Influence of iron on growth, morphology, outer membrane protein composition, and synthesis of siderophores in Campylobacter jejuni. Infect Immun 54: 126-132.
12. Flo, T.H., Smith, K.D., Sato, S., Rodriguez, D.J., Holmes, M.A., Strong, R.K., etal. (2004) Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 432: 917-921.
13. Fouts, D.E., Mongodin, E.F., Mandrell, R.E., Miller, W.G., Rasko, D.A., Ravel, J., etal. (2005) Major structural differences and novel potential virulence mechanisms from the genomes of multiple Campylobacter species. PLoS Biol 3: e15.
14. Furrer, J.L., Sanders, D.N., Hook-Barnard, I.G., and McIntosh, M.A. (2002) Export of the siderophore enterobactin in Escherichia coli: involvement of a 43 kDa membrane exporter. Mol Microbiol 44: 1225-1234.
15. Hantke, K., Nicholson, G., Rabsch, W., and Winkelmann, G. (2003) Salmochelins, siderophores of Salmonella enterica and uropathogenic Escherichia coli strains, are recognized by the outer membrane receptor IroN. Proc Natl Acad Sci USA 100: 3677-3682.
16. Hofreuter, D., Tsai, J., Watson, R.O., Novik, V., Altman, B., Benitez, M., etal. (2006) Unique features of a highly pathogenic Campylobacter jejuni strain. Infect Immun 74: 4694-4707.
17. Holmes, K., Mulholland, F., Pearson, B.M., Pin, C., McNicholl-Kennedy, J., Ketley, J.M., and Wells, J.M. (2005) Campylobacter jejuni gene expression in response to iron limitation and the role of Fur. Microbiology 151: 243-257.
18. Jeon, B., Wang, Y., Hao, H., Barton, Y.W., and Zhang, Q. (2011) Contribution of CmeG to antibiotic and oxidative stress resistance in Campylobacter jejuni. J Antimicrob Chemother 66: 79-85.
19. Langman, L., Young, I.G., Frost, G.E., Rosenberg, H., and Gibson, F. (1972) Enterochelin system of iron transport in Escherichia coli: mutations affecting ferric-enterochelin esterase. J Bacteriol 112: 1142-1149.
20. Larsen, N.A., Lin, H., Wei, R., Fischbach, M.A., and Walsh, C.T. (2006) Structural characterization of enterobactin hydrolase IroE. Biochemistry 45: 10184-10190.
21. Lefebure, T., Bitar, P.D., Suzuki, H., and Stanhope, M.J. (2010) Evolutionary dynamics of complete Campylobacter pan-genomes and the bacterial species concept. Genome Biol Evol 2: 646-655.
22. Lin, H., Fischbach, M.A., Liu, D.R., and Walsh, C.T. (2005a) In vitro characterization of salmochelin and enterobactin trilactone hydrolases IroD, IroE, and Fes. J Am Chem Soc 127: 11075-11084.
23. Lin, J., Michel, L.O., and Zhang, Q. (2002) CmeABC functions as a multidrug efflux system in Campylobacter jejuni. Antimicrob Agents Chemother 46: 2124-2131.
24. Lin, J., Sahin, O., Michel, L.O., and Zhang, Q. (2003) Critical role of multidrug efflux pump CmeABC in bile resistance and in vivo colonization of Campylobacter jejuni. Infect Immun 71: 4250-4259.
25. Lin, J., Akiba, M., Sahin, O., and Zhang, Q. (2005b) CmeR functions as a transcriptional repressor for the multidrug efflux pump CmeABC in Campylobacter jejuni. Antimicrob Agents Chemother 49: 1067-1075.
26. Miethke, M., and Marahiel, M.A. (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71: 413-451.
27. Miethke, M., Hou, J., and Marahiel, M.A. (2011) The siderophore-interacting protein YqjH acts as a ferric reductase in different iron assimilation pathways of Escherichia coli. Biochemistry 50: 10951-10964.
28. Miller, C.E., Rock, J.D., Ridley, K.A., Williams, P.H., and Ketley, J.M. (2008) Utilization of lactoferrin-bound and transferrin-bound iron by Campylobacter jejuni. J Bacteriol 190: 1900-1911.
29. Miller, C.E., Williams, P.H., and Ketley, J.M. (2009) Pumping iron: mechanisms for iron uptake by Campylobacter. Microbiology 155: 3157-3165.
30. Naikare, H., Palyada, K., Panciera, R., Marlow, D., and Stintzi, A. (2006) Major role for FeoB in Campylobacter jejuni ferrous iron acquisition, gut colonization, and intracellular survival. Infect Immun 74: 5433-5444.
31. O'Brien, I.G., Cox, G.B., and Gibson, F. (1971) Enterochelin hydrolysis and iron metabolism in Escherichia coli. Biochim Biophys Acta 237: 537-549.
32. Olson, C.K., Ethelberg, S., Pelt, W.V., and Tauxe, R.V. (2008) Epidemiology of Campylobacter jejuni infections in industrialized nations. In Campylobacter. Nachamkin, I., Szymanski, C.M., and Blaser, M.J. (eds). Washington, DC: ASM Press, pp. 163-189.
33. Palyada, K., Threadgill, D., and Stintzi, A. (2004) Iron acquisition and regulation in Campylobacter jejuni. J Bacteriol 186: 4714-4729.
34. Parkhill, J., Wren, B.W., Mungall, K., Ketley, J.M., Churcher, C., Basham, D., etal. (2000) The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403: 665-668.
35. Pickett, C.L., Auffenberg, T., Pesci, E.C., Sheen, V.L., and Jusuf, S.S. (1992) Iron acquisition and hemolysin production by Campylobacter jejuni. Infect Immun 60: 3872-3877.
36. Raffatellu, M., George, M.D., Akiyama, Y., Hornsby, M.J., Nuccio, S.P., Paixao, T.A., etal. (2009) Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe 5: 476-486.
37. Raymond, K.N., Dertz, E.A., and Kim, S.S. (2003) Enterobactin: an archetype for microbial iron transport. Proc Natl Acad Sci USA 100: 3584-3588.
38. Rees, J.H., Soudain, S.E., Gregson, N.A., and Hughes, R.A. (1995) Campylobacter jejuni infection and Guillain-Barre syndrome. N Engl J Med 333: 1374-1379.
39. Richardson, P.T., and Park, S.F. (1995) Enterochelin acquisition in Campylobacter coli: characterization of components of a binding-protein-dependent transport system. Microbiology 141 (Part 12): 3181-3191.
40. Rissman, A.I., Mau, B., Biehl, B.S., Darling, A.E., Glasner, J.D., and Perna, N.T. (2009) Reordering contigs of draft genomes using the Mauve aligner. Bioinformatics 25: 2071-2073.
41. Stintzi, A., Vliet, A.H.M.V., and Ketley, J.M. (2008) Iron metabolism, transport, and regulation. In Campylobacter. Nachamkin, I., Szymanski, C.M., and Blaser, M.J. (eds). Washington, DC: ASM Press, pp. 591-610.
42. Takeda, K., Sato, J., Goto, K., Fujita, T., Watanabe, T., Abo, M., etal. (2010) Escherichia coli ferredoxin-NADP+ reductase and oxygen-insensitive nitroreductase are capable of functioning as ferric reductase and of driving the Fenton reaction. Biometals 23: 727-737.
43. Voelkerding, K.V., Dames, S.A., and Durtschi, J.D. (2009) Next-generation sequencing: from basic research to diagnostics. Clin Chem 55: 641-658.
44. Wang, Y., and Taylor, D.E. (1990) Chloramphenicol resistance in Campylobacter coli: nucleotide sequence, expression, and cloning vector construction. Gene 94: 23-28.
45. Xu, F., Zeng, X., Haigh, R.D., Ketley, J.M., and Lin, J. (2010) Identification and characterization of a new ferric enterobactin receptor, CfrB, in Campylobacter. J Bacteriol 192: 4425-4435.
46. Yao, R., Alm, R.A., Trust, T.J., and Guerry, P. (1993) Construction of new Campylobacter cloning vectors and a new mutational cat cassette. Gene 130: 127-130.
47. Yeom, J., Jeon, C.O., Madsen, E.L., and Park, W. (2009) Ferredoxin-NADP+ reductase from Pseudomonas putida functions as a ferric reductase. J Bacteriol 191: 1472-1479.
48. Zaar, A., Gescher, J., Eisenreich, W., Bacher, A., and Fuchs, G. (2004) New enzymes involved in aerobic benzoate metabolism in Azoarcus evansii. Mol Microbiol 54: 223-238.
49. Zeng, X., Xu, F., and Lin, J. (2009) Molecular, antigenic, and functional characteristics of ferric enterobactin receptor CfrA in Campylobacter jejuni. Infect Immun 77: 5437-5448.
50. Zhu, M., Valdebenito, M., Winkelmann, G., and Hantke, K. (2005) Functions of the siderophore esterases IroD and IroE in iron-salmochelin utilization. Microbiology 151: 2363-2372.