Flagella interact with ionic plant lipids to mediate adherence of pathogenic Escherichia coli to fresh produce plants

Environmental Microbiology

Volumn 16, Issue 7, 2014, Pages 2181-2195

  Rossez, Yannick ^a   Holmes, Ashleigh ^a   Wolfson, Eliza B ^b   Gally, David L ^b   Mahajan, Arvind ^b   Pedersen, Henriette L ^c   Willats, William G T ^c   Toth, Ian K ^a   Holden, Nicola J ^a  

^a SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); ESCHERICHIA; ESCHERICHIA COLI; EUKARYOTA; SPINACIA OLERACEA;

CARRAGEENAN; MEMBRANE LIPID;

ARABIDOPSIS; ARTICLE; BACTERIAL COUNT; BACTERIUM ADHERENCE; CELL MEMBRANE; CHEMISTRY; ESCHERICHIA COLI O157; FLAGELLUM; HOST PATHOGEN INTERACTION; HOST RANGE; METABOLISM; MICROBIOLOGY; OSMOLARITY; SPINACH;

ARABIDOPSIS; BACTERIAL ADHESION; CARRAGEENAN; CELL MEMBRANE; COLONY COUNT, MICROBIAL; ESCHERICHIA COLI O157; FLAGELLA; HOST SPECIFICITY; HOST-PATHOGEN INTERACTIONS; MEMBRANE LIPIDS; OSMOLAR CONCENTRATION; SPINACIA OLERACEA;

EID: 84903767293     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12315     Document Type: Article

References (72)

1. Andersson, M.X., Stridh, M.H., Larsson, K.E., Liljenberg, C., and Sandelius, A.S. (2003) Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol. FEBS Lett 537: 128-132.
2. Bardoel, B.W., van der Ent, S., Pel, M.J., Tommassen, J., Pieterse, C.M., van Kessel, K.P., and van Strijp, J.A. (2011) Pseudomonas evades immune recognition of flagellin in both mammals and plants. PLoS Pathog 7: e1002206.
3. Benning, C. (2009) Mechanisms of lipid transport involved in organelle biogenesis in plant cells. Annu Rev Cell Dev Biol 25: 71-91.
4. Benning, C., and Ohta, H. (2005) Three enzyme systems for galactoglycerolipid biosynthesis are coordinately regulated in plants. J Biol Chem 280: 2397-2400.
5. Berger, C.N., Shaw, R.K., Brown, D.J., Mather, H., Clare, S., Dougan, G., etal. (2009) Interaction of Salmonella enterica with basil and other salad leaves. ISME J 3: 261-265.
6. Berger, C.N., Sodha, S.V., Shaw, R.K., Griffin, P.M., Pink, D., Hand, P., and Frankel, G. (2010) Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ Microbiol 12: 2385-2397.
7. Blomfield, I.C., Vaughn, V., Rest, R.F., and Eisenstein, B.I. (1991) Allelic exchange in Escherichia coli using the Bacillus subtilis sacB gene and a temperature-sensitive pSC101 replicon. Mol Microbiol 5: 1447-1457.
8. Buttner, D., and Bonas, U. (2002) Port of entry - the type III secretion translocon. Trends Microbiol 10: 186-192.
9. Campellone, K.G., Robbins, D., and Leong, J.M. (2004) EspFU is a translocated EHEC effector that interacts with Tir and N-WASP and promotes Nck-independent actin assembly. Dev Cell 7: 217-228.
10. Canut, H., Carrasco, A., Galaud, J.P., Cassan, C., Bouyssou, H., Vita, N., etal. (1998) High affinity RGD-binding sites at the plasma membrane of Arabidopsis thaliana links the cell wall. Plant J 16: 63-71.
11. CDC (2012) Multistate outbreak of shiga toxin-producing Escherichia coli O157:H7 infections linked to organic spinach and spring mix blend in Centers for Disease Control and Prevention.
12. Chacon-Lopez, A., Ibarra-Laclette, E., Sanchez-Calderon, L., Gutierrez-Alanis, D., and Herrera-Estrella, L. (2011) Global expression pattern comparison between low phosphorus insensitive 4 and WT Arabidopsis reveals an important role of reactive oxygen species and jasmonic acid in the root tip response to phosphate starvation. Plant Signal Behav 6: 382-392.
13. Chevalier, F., and Rossignol, M. (2011) Proteomic analysis of Arabidopsis thaliana ecotypes with contrasted root architecture in response to phosphate deficiency. J Plant Physiol 168: 1885-1890.
14. Chinchilla, D., Bauer, Z., Regenass, M., Boller, T., and Felix, G. (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18: 465-476.
15. Dormann, P., Hoffmann-Benning, S., Balbo, I., and Benning, C. (1995) Isolation and characterization of an Arabidopsis mutant deficient in the thylakoid lipid digalactosyl diacylglycerol. Plant Cell 7: 1801-1810.
16. Duan, Q., Zhou, M., Zhu, X., Yang, Y., Zhu, J., Bao, W., etal. (2013) Flagella from F18+ Escherichia coli play a role in adhesion to pig epithelial cell lines. Microb Pathog 55: 32-38.
17. Eaves-Pyles, T.D., Wong, H.R., Odoms, K., and Pyles, R.B. (2001) Salmonella flagellin-dependent proinflammatory responses are localized to the conserved amino and carboxyl regions of the protein. J Immunol 167: 7009-7016.
18. Erdem, A.L., Avelino, F., Xicohtencatl-Cortes, J., and Giron, J.A. (2007) Host protein binding and adhesive properties of H6 and H7 flagella of attaching and effacing Escherichia coli. J Bacteriol 189: 7426-7435.
19. Essigmann, B., Guler, S., Narang, R.A., Linke, D., and Benning, C. (1998) Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. PNAS 95: 1950-1955.
20. Estelle, M., and Somerville, C. (1987) Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology. Mol Gel Genet 206: 200-206.
21. Felix, G., Duran, J.D., Volko, S., and Boller, T. (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18: 265-276.
22. Geldner, N., Denervaud-Tendon, V., Hyman, D.L., Mayer, U., Stierhof, Y.D., and Chory, J. (2009) Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J 59: 169-178.
23. Giron, J.A., Torres, A.G., Freer, E., and Kaper, J.B. (2002) The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol Microbiol 44: 361-379.
24. Gomez-Gomez, L., and Boller, T. (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5: 1003-1011.
25. Gorski, L., Palumbo, J.D., and Mandrell, R.E. (2003) Attachment of Listeria monocytogenes to radish tissue is dependent upon temperature and flagellar motility. Appl Environ Microbiol 69: 258-266.
26. Grant, J., Wendelboe, A.M., Wendel, A., Jepson, B., Torres, P., Smelser, C., and Rolfs, R.T. (2008) Spinach-associated Escherichia coli O157:H7 outbreak, Utah and New Mexico, 2006. Emerg Infect Dis 14: 1633-1636.
27. Hartel, H., Dormann, P., and Benning, C. (2000) DGD1-independent biosynthesis of extraplastidic galactolipids after phosphate deprivation in Arabidopsis. PNAS 97: 10649-10654.
28. Hayashi, T., Makino, K., Ohnishi, M., Kurokawa, K., Ishii, K., Yokoyama, K., etal. (2001) Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12. DNA Res 8: 11-22.
29. He, S.Y. (1997) Hrp-controlled interkingdom protein transport: learning from flagellar assembly? Trends Microbiol 5: 489-495.
30. Holden, N., Pritchard, L., and Toth, I. (2009) Colonization outwith the colon: plants as an alternative environmental reservoir for human pathogenic enterobacteria. FEMS Microbiol Rev 33: 689-703.
31. Ibrahim, G.F., Fleet, G.H., Lyons, M.J., and Walker, R.A. (1985) Method for the isolation of highly purified Salmonella flagellins. J Clin Microbiol 22: 1040-1044.
32. Iguchi, A., Thomson, N.R., Ogura, Y., Saunders, D., Ooka, T., Henderson, I.R., etal. (2009) Complete genome sequence and comparative genome analysis of enteropathogenic Escherichia coli O127:H6 strain E2348/69. J Bacteriol 191: 347-354.
33. Jeter, C., and Matthysse, A.G. (2005) Characterization of the binding of diarrheagenic strains of E.coli to plant surfaces and the role of curli in the interaction of the bacteria with alfalfa sprouts. Mol Plant Microbe Interact 18: 1235-1242.
34. Jiao, G., Yu, G., Zhang, J., and Ewart, H.S. (2011) Chemical structures and bioactivities of sulfated polysaccharides from marine algae. Mar Drugs 9: 196-223.
35. Jouhet, J., Marechal, E., Baldan, B., Bligny, R., Joyard, J., and Block, M.A. (2004) Phosphate deprivation induces transfer of DGDG galactolipid from chloroplast to mitochondria. J Cell Biol 167: 863-874.
36. Kaper, J.B., Nataro, J.P., and Mobley, H.L. (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2: 123-140.
37. Karlova, R., Boeren, S., Russinova, E., Aker, J., Vervoort, J., and de Vries, S. (2006) The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE1 protein complex includes BRASSINOSTEROID-INSENSITIVE1. Plant Cell 18: 626-638.
38. Kunst, L., and Samuels, L. (2009) Plant cuticles shine: advances in wax biosynthesis and export. Curr Opin Plant Biol 12: 721-727.
39. Lahteenmaki, K., Westerlund, B., Kuusela, P., and Korhonen, T.K. (1993) Immobilization of plasminogen on Escherichia coli flagella. FEMS Microbiol Lett 106: 309-314.
40. Lombard, J., Lopez-Garcia, P., and Moreira, D. (2012) The early evolution of lipid membranes and the three domains of life. Nat Rev Microbiol 10: 507-515.
41. Luck, S.N., Badea, L., Bennett-Wood, V., Robins-Browne, R., and Hartland, E.L. (2006) Contribution of FliC to epithelial cell invasion by enterohemorrhagic Escherichia coli O113:H21. Infect Immun 74: 6999-7004.
42. Mahajan, A., Currie, C.G., Mackie, S., Tree, J., McAteer, S., McKendrick, I., etal. (2009) An investigation of the expression and adhesin function of H7 flagella in the interaction of Escherichia coli O157:H7 with bovine intestinal epithelium. Cell Microbiol 11: 121-137.
43. Michel, G., Nyval-Collen, P., Barbeyron, T., Czjzek, M., and Helbert, W. (2006) Bioconversion of red seaweed galactans: a focus on bacterial agarases and carrageenases. Appl Microbiol Biotechnol 71: 23-33.
44. Moran, A.P., Gupta, A., and Joshi, L. (2011) Sweet-talk: role of host glycosylation in bacterial pathogenesis of the gastrointestinal tract. Gut 60: 1412-1425.
45. Murashige, T., and Skoog, F. (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15: 473-497.
46. Nakamura, Y. (2013) Phosphate starvation and membrane lipid remodeling in seed plants. Prog Lipid Res 52: 43-50.
47. Namba, K., Yamashita, I., and Vonderviszt, F. (1989) Structure of the core and central channel of bacterial flagella. Nature 342: 648-654.
48. Narise, T., Kobayashi, K., Baba, S., Shimojima, M., Masuda, S., Fukaki, H., and Ohta, H. (2010) Involvement of auxin signaling mediated by IAA14 and ARF7/19 in membrane lipid remodeling during phosphate starvation. Plant Mol Biol 72: 533-544.
49. Neidhardt, F.C., Bloch, P.L., and Smith, D.F. (1974) Culture medium for enterobacteria. J Bacteriol 119: 736-747.
50. Okazaki, Y., Otsuki, H., Narisawa, T., Kobayashi, M., Sawai, S., Kamide, Y., etal. (2013) A new class of plant lipid is essential for protection against phosphorus depletion. Nat Commun 4: 1510.
51. Paton, A.W., and Paton, J.C. (1998) Detection and characterization of Shiga toxigenic Escherichia coli by using multiplex PCR assays for stx1, stx2, eaeA, enterohemorrhagic E.coli hlyA, rfbO111, and rfbO157. J Clin Microbiol 36: 598-602.
52. Pedersen, H.L., Fangel, J.U., McCleary, B., Ruzanski, C., Rydahl, M.G., Ralet, M.C., etal. (2012) Versatile high resolution oligosaccharide microarrays for plant glycobiology and cell wall research. J Biol Chem 287: 39429-39438.
53. Peret, B., Clement, M., Nussaume, L., and Desnos, T. (2011) Root developmental adaptation to phosphate starvation: better safe than sorry. Trends Plant Sci 16: 442-450.
54. Reid, S.D., Selander, R.K., and Whittam, T.S. (1999) Sequence diversity of flagellin (fliC) alleles in pathogenic Escherichia coli. J Bacteriol 181: 153-160.
55. Riley, M., Abe, T., Arnaud, M.B., Berlyn, M.K., Blattner, F.R., Chaudhuri, R.R., etal. (2006) Escherichia coli K-12: a cooperatively developed annotation snapshot-2005. Nucleic Acids Res 34: 1-9.
56. Roy, K., Hilliard, G.M., Hamilton, D.J., Luo, J., Ostmann, M.M., and Fleckenstein, J.M. (2009) Enterotoxigenic Escherichia coli EtpA mediates adhesion between flagella and host cells. Nature 457: 594-598.
57. Saldana, Z., Sanchez, E., Xicohtencatl-Cortes, J., Puente, J.L., and Giron, J.A. (2011a) Surface structures involved in plant stomata and leaf colonization by Shiga-toxigenic Escherichia coli O157:H7. Front Microbiol 2: 119.
58. Saldana, Z., Sanchez, E., Xicohtencatl-Cortes, J., Puente, J.L., and Giron, J.A. (2011b) Surface structures involved in plant stomata and leaf colonization by shiga-toxigenic Escherichia coli O157:H7. Front Microbiol 2: 119.
59. Shaw, R.K., Berger, C.N., Feys, B., Knutton, S., Pallen, M.J., and Frankel, G. (2008) Enterohemorrhagic Escherichia coli exploits EspA filaments for attachment to salad leaves. Appl Environ Microbiol 74: 2908-2914.
60. Shaw, R.K., Berger, C.N., Pallen, M.J., Sjoeling, A., and Frankel, G. (2011) Flagella mediate attachment of enterotoxigenic Escherichia coli to fresh salad leaves. Environ Microbiol Rep 3: 112-117.
61. Smith, K.D., Andersen-Nissen, E., Hayashi, F., Strobe, K., Bergman, M.A., Barrett, S.L., etal. (2003) Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat Immunol 4: 1247-1253.
62. Somerville, C., Bauer, S., Brininstool, G., Facette, M., Hamann, T., Milne, J., etal. (2004) Toward a systems approach to understanding plant cell walls. Science 306: 2206-2211.
63. Troge, A., Scheppach, W., Schroeder, B.O., Rund, S.A., Heuner, K., Wehkamp, J., etal. (2012) More than a marine propeller - the flagellum of the probiotic Escherichia coli strain Nissle 1917 is the major adhesin mediating binding to human mucus. Int J Med Microbiol 302: 304-314.
64. Wang, R.F., and Kushner, S.R. (1991) Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100: 195-199.
65. Wang, Z., and Benning, C. (2011) Arabidopsis thaliana polar glycerolipid profiling by thin layer chromatography (TLC) coupled with gas-liquid chromatography (GLC). J Vis Exp 49: 2518.
66. Wei, H.L., Chakravarthy, S., Worley, J.N., and Collmer, A. (2012) Consequences of flagellin export through the type III secretion system of Pseudomonas syringae reveal a major difference in the innate immune systems of mammals and the model plant Nicotiana benthamiana. Cell Microbiol 15: 601-618.
67. Wendel, A.M., Johnson, D.H., Sharapov, U., Grant, J., Archer, J.R., Monson, T., etal. (2009) Multistate outbreak of Escherichia coli O157:H7 infection associated with consumption of packaged spinach, August-September 2006: the Wisconsin investigation. Clin Infect Dis 48: 1079-1086.
68. Wright, K.M., Chapman, S., McGeachy, K., Humphris, S., Campbell, E., Toth, I.K., and Holden, N.J. (2013) The endophytic lifestyle of Escherichia coli O157:H7: quantification and internal localization in roots. Phytopathology 103: 333-340.
69. Xicohtencatl-Cortes, J., Sanchez Chacon, E., Saldana, Z., Freer, E., and Giron, J.A. (2009) Interaction of Escherichia coli O157: H7 with leafy green produce. J Food Prot 72: 1531-1537.
70. Xu, X., McAteer, S.P., Tree, J.J., Shaw, D.J., Wolfson, E.B., Beatson, S.A., etal. (2012) Lysogeny with Shiga toxin 2-encoding bacteriophages represses type III secretion in enterohemorrhagic Escherichia coli. PLoS Pathog 8: e1002672.
71. Yonekura, K., Maki, S., Morgan, D.G., DeRosier, D.J., Vonderviszt, F., Imada, K., and Namba, K. (2000) The bacterial flagellar cap as the rotary promoter of flagellin self-assembly. Science 290: 2148-2152.
72. Yu, B., Xu, C., and Benning, C. (2002) Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. Proc Natl Acad Sci U S A 99: 5732-5737.