YkgM and ZinT proteins are required for maintaining intracellular zinc concentration and producing curli in enterohemorrhagic Escherichia coli (EHEC) O157:H7 under zinc deficient conditions

International Journal of Food Microbiology

Volumn 149, Issue 2, 2011, Pages 159-170

  Lim, Jeesun ^a   Lee, Kang Mu ^a   Kim, So Hyun ^a   Kim, Younghoon ^b   Kim, Sae Hun ^b   Park, Woojun ^b   Park, Sungsu ^a  

^a Ewha Womans University   (South Korea)

^b Korea University   (South Korea)

Author keywords

Biofilm; Escherichia coli O157:H7; YkgM gene; Zinc; ZinT gene

Indexed keywords

BACTERIAL PROTEIN; CSGA PROTEIN; CURLI PROTEIN; MUTANT PROTEIN; UNCLASSIFIED DRUG; YKGM PROTEIN; ZINC ION; ZINT PROTEIN;

ARTICLE; BIOFILM; BIOSYNTHESIS; CULTURE MEDIUM; EPITHELIUM CELL; ESCHERICHIA COLI; MASS SPECTROMETRY; NONHUMAN; PLANKTON; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; WILD TYPE; ZINC DEFICIENCY;

BACTERIAL PROTEINS; BIOFILMS; ESCHERICHIA COLI O157; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION; PLANKTON; ZINC;

ESCHERICHIA COLI;

EID: 79960847681     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2011.06.017     Document Type: Article

References (45)

1. 2+ uptake system ZnuABC is required for bacterial zinc homeostasis in intracellular environments and contributes to the virulence of Salmonella enterica. Infection and Immunity 2007, 75:5867-5876.
2. Beloin C., Valle J., Latour-Lambert P., Faure P., Kzreminski M., Balestrino D., Haagensen J.A., Molin S., Prensier G., Arbeille B., Ghigo J.M. Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Molecular Microbiology 2004, 51:659-674.
3. Benov L.T., Fridovich I. Escherichia coli expresses a copper- and zinc-containing superoxide dismutase. The Journal of Biological Chemistry 1994, 269:25310-25314.
4. Brown P.K., Dozois C.M., Nickerson C.A., Zuppardo A., Terlonge J., Curtiss R. MlrA, a novel regulator of curli (AgF) and extracellular matrix synthesis by Escherichia coli and Salmonella enterica serovar Typhimurium. Molecular Microbiology 2001, 41:349-363.
5. 2+. Sensors and Actuators B 2009, 137:597-602.
6. Cormack B.P., Valdivia R.H., Falkow S. FACS-optimized mutants of the green fluorescent protein (GFP). Gene 1996, 173:33-38.
7. Crane J.K., Naeher T.M., Shulgina I., Zhu C., Boedeker E.C. Effect of zinc in enteropathogenic Escherichia coli infection. Infection and Immunity 2007, 75:5974-5984.
8. Domka J., Lee J., Bansal T., Wood T.K. Temporal gene-expression in Escherichia coli K-12 biofilms. Environmental Microbiology 2007, 9:332-346.
9. Gabbianelli R., Scotti R., Ammendola S., Petrarca P., Nicolini L., Battistoni A. Role of ZnuABC and ZinT in Escherichia coli O157:H7 zinc acquisition and interaction with epithelial cells. BMC Microbiology 2011, 11:36.
10. Gabriel S.E., Helmann J.D. Contributions of Zur-controlled ribosomal proteins to growth under zinc starvation conditions. Journal of Bacteriology 2009, 191:6116-6122.
11. Garrido M.E., Bosch M., Medina R., Lagostera M., Perez de Rozas A.M., Badiola I., Barbe J. The high affinity zinc-uptake system ZnuABC is under control of the iron-uptake regulator (fur) gene in the animal pathogen Pasteurella multocida. FEMS Microbiology Letters 2002, 221:31-37.
12. Graham A.I., Hunt S., Stokes S.L., Bramall N., Bunch J., Cox A.G., McLeod C.W., Poole R.K. Severe zinc depletion of Escherichia coli: roles for high affinity zinc binding by ZinT, zinc transport and zinc-independent proteins. The Journal of Biological Chemistry 2009, 284:18377-18389.
13. Gualdi L., Tagliabue L., Bertagnoli S., Ierano T., De Castro C., Landini P. Cellulose modulates biofilm formation by counteracting curli-mediated colonization of solid surfaces in Escherichia coli. Microbiology 2008, 154:2017-2024.
14. Gunasekera T.S., Herre A.H., Crowder M.W. Absence of ZnuABC-mediated zinc uptake affects virulence-associated phenotypes of uropathogenic Escherichia coli CFT073 under Zn(II)-depleted conditions. FEMS Microbiology Letter 2009, 300:36-41.
15. Hemm M.R., Paul B.J., Miranda-Ríos J., Zhang A., Soltanzad N., Storx G. Small stress response proteins in Escherichia coli: proteins missed by classical proteomics studies. Journal of Bacteriology 2010, 192:46-58.
16. Ho T.D., Davis B.M., Ritchie J.M., Waldor M.K. Type 2 secretion promotes enterohemorrhagic Escherichia coli adherence and intestinal colonization. Infection and Immunity 2008, 76:1858-1865.
17. Hwang B.K., Lee W.N., Yeon K.M., Park P.K., Lee C.H., Chang I.S., Drews A., Kraume M. Correlating TMP increases with microbial characteristics in the bio-cake on the membrane surface in a membrane bioreactor. Environmental Science and Technology 2008, 42:3963-3968.
18. Justice S.S., Hunstad D.A., Cegelski L., Hultgren S.J. Morphological plasticity as a bacterial survival strategy. Nature Reviews Microbiology 2008, 6:162-168.
19. Kershaw C.J., Brown N.L., Hobman J.L. Zinc dependence of zinT (yodA) mutants and binding of zinc, cadmium and mercury by ZinT. Biochemical and Biophysical Research Communications 2007, 364:66-71.
20. Kikuchi T., Mizunoe Y., Takade A., Naito S., Yoshida S. Curli fibers are required for development of biofilm architecture in Escherichia coli K-12 and enhance bacterial adherence to human uroepithelial cells. Microbiology and Immunology 2005, 49:875-884.
21. Kim S., Watanabe K., Shirahata T., Watarai M. Zinc uptake system (znuA locus) of Brucella bortus is essential for intracellular survival and virulence in mice. The Journal of Veterinary Medical Science 2004, 66:1059-1063.
22. Kim Y.H., Lee Y., Kim S., Yeom J., Yeom S., Kim B.S., Oh S., Park S., Jeon C.O., Park W. The role of periplasmic antioxidant enzymes (superoxide dismutase and thiol peroxidase) of the Shiga toxin-producing Escherichia coli O157:H7 in the formation of biofilms. Proteomics 2006, 6:6181-6193.
23. Kim Y.H., Oh S., Park S., Kim S.H. Transcriptome analysis for interaction between Enterohemorrahgic Escherichia coli (EHEC) O157:H7 attachment and intestinal epithelial HT-29 cells. International Journal of Food Microbiology 2009, 131:224-232.
24. Kitagawa M., Ara T., Arifuzzaman M., Ioka-Nakamichi T., Inamoto E., Toyonaga H., Mori H. Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Research 2005, 12:291-299.
25. Lee K.M., Kim W.S., Lim J., Nam S., Youn M., Nam S.W., Kim Y., Kim S.H., Park W., Park S. Antipathogenic properties of green tea polyphenol epigallocatechin gallate at concentrations below the MIC against enterohemorrhagic Escherichia coli O157:H7. Journal of Food Protection 2009, 72:325-331.
26. Lim J., Lee K.M., Kim S.H., Nam S.W., Oh Y.J., Yun H.S., Jo W., Oh S., Kim S.H., Park S. Nanoscale characterization of Escherichia coli biofilm formed under laminar flow using atomic force microscopy (AFM) and scanning electron microscopy (SEM). Bulletin of the Korean Chemical Society 2008, 29:2114-2118.
27. Ma Q., Wood T.K. OmpA influences Escherichia coli biofilm formation by repressing cellulose production through the CpxRA two-component system. Environmental Microbiology 2009, 11:2735-2746.
28. Makarova K.S., Ponomarev V.A., Koonin E.V. Two C or not two C: recurrent disruption of Zn-ribbons, gene duplication, lineage-specific gene loss, and horizontal gene transfer in evolution of bacterial ribosomal proteins. Genome Biology 2001, 2. RESEARCH 0033.
29. May T., Okabe S. Escherichia coli harboring a natural IncF conjugative F plasmid develops complex mature biofilms by stimulating synthesis of colanic acid and curli. Journal of Bacteriology 2008, 190:7479-7490.
30. Miller V.L., Mekalanos J.J. 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. Journal of Bacteriology 1988, 170:2575-2583.
31. O'Connor T.R., Graves R.J., de Murcia G., Castaing B., Laval J. Fpg protein of Escherichia coli is a zinc finger protein whose cysteine residues have a structural and/or functional role. The Journal of Biological Chemistry 1993, 268:9063-9070.
32. O'Toole G., Kaplan H.B., Kolter R. Biofilm formation as microbial development. Annual Review of Microbiology 2000, 54:49-79.
33. Outten C.E., O'Halloran T.V. Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 2001, 292:2488-2492.
34. Oka A., Sugisaki H., Takanami M. Nucleotide sequence of the kanamycin resistance transposon Tn903. Journal of Molecular Biology 1981, 147:217-226.
35. Park S., Worobo R.W., Durst R.A. Escherichia coli O157:H7 as an emerging foodborne pathogen: a literature review. Critical Reviews in Food Science and Nutrition 1999, 39:481-502.
36. Petrarca P., Ammendola S., Pasquali P., Battistoni A. The Zur-regulated ZinT protein is an auxiliary component of the high-affinity ZnuABC zinc transporter that facilitates metal recruitment during severe zinc shortage. Journal of Bacteriology 2010, 192:1553-1564.
37. Philippe N., Alcaraz J.P., Coursange E., Geiselmann J., Schneider D. Improvement of pCVD442, a suicide plasmid for gene allele exchange in bacteria. Plasmid 2004, 51:246-255.
38. Ryu J.H., Beuchat L.R. Biofilm formation by Escherichia coli O157:H7 on stainless steel: effect of exopolysaccharide and curli production on its resistance to chlorine. Applied and Environmental Microbiology 2005, 71:247-254.
39. Sabri M., Houle S., Dozois C.M. Roles of the extraintestinal pathogenic Escherichia coli ZnuACB and ZupT zinc transporters during urinary tract infection. Infection and Immunity 2009, 77:1155-1164.
40. Scrutton M.C., Wu C.W., Goldthwait D.A. The presence and possible role of zinc in RNA polymerase obtained from Escherichia coli. Proceedings of the National Academy of Science of the United States of America 1971, 68:2497-2501.
41. Schaible U.E., Kaufmann S.H. Iron and microbial infection. Nature Reviews Microbiology 2004, 2:946-953.
42. Sigdel T.K., Easton J.A., Crowder M.W. Transcriptional response of Escherichia coli to TPEN. Journal of Bacteriology 2006, 188:6709-6713.
43. Van Houdt R., Michiels C.W. Role of bacterial cell surface structures in Escherichia coli biofilm formation. Research in Microbiology 2005, 156:626-633.
44. Xia Y., Whitesides G.M. Soft lithography. Annual Review of Materials Science 1998, 28:153-184.
45. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 1985, 33:103-119.