1887

Abstract

Several genes involved in the interaction between Sp7 and plants are located on the pRhico plasmid. Here we report the characterization of an Sp7 mutant strain with impairment of the pRhico-located gene . This gene encodes an inner-membrane component of an ATP-binding cassette (ABC) transporter with similarity to transporters involved in surface polysaccharide export. Indeed, SDS-PAGE revealed that LPS synthesis is affected in the mutant. No significant differences were observed between wild-type and mutant strains in exopolysaccharide (EPS) amount; however, several differences were observed between them in EPS monosaccharide composition, and only wild-type colonies stained positively with Congo red. Microscopy revealed that mutant cells are longer and thinner, and exhibit several differences in their cell surface relative to the wild-type. The mutant was more resistant to oxidative stress, starvation, desiccation, heat and osmotic shock than the wild-type. In contrast, the mutant was more susceptible than the wild-type to UV radiation and saline stress. The strains also differed in their susceptibility to different antibiotics. Differences between the strains were also observed in their outer-membrane protein composition. No differences were observed between strains in their ability to attach to sweet corn roots and seeds, and to promote growth under the tested conditions. As LPS plays an important role in cell envelope structural integrity, we propose that the pleiotropic phenotypic changes observed in the mutant are due to its altered LPS relative to the wild-type.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.021824-0
2009-03-01
2020-01-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/3/791.html?itemId=/content/journal/micro/10.1099/mic.0.021824-0&mimeType=html&fmt=ahah

References

  1. Albersheim, P., Nevins, D. J., English, P. D. & Karr, A. ( 1967; ). A method for the analysis of sugars in plant cell-wall polysaccharides by gas-liquid chromatography. Carbohydr Res 5, 340–345.[CrossRef]
    [Google Scholar]
  2. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J. ( 1997; ). Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25, 3389–3402.[CrossRef]
    [Google Scholar]
  3. Arunakumari, A., Lamm, R. B. & Neyra-Estens, C. A. ( 1992; ). Changes in cell surface properties of azospirilla in relation to cell pleomorphism and aggregation. Symbiosis 13, 291–305.
    [Google Scholar]
  4. Bahat-Samet, E., Castro-Sowinski, S. & Okon, Y. ( 2004; ). Arabinose content of extracellular polysaccharide plays a role in cell aggregation of Azospirillum brasilense. FEMS Microbiol Lett 237, 195–203.
    [Google Scholar]
  5. Bastarrachea, F., Zamudio, M. & Rivas, R. ( 1988; ). Non-encapsulated mutants of Azospirillum brasilense and Azospirillum lipoferum. Can J Microbiol 34, 24–29.[CrossRef]
    [Google Scholar]
  6. Bliss, J. M., Garon, C. F. & Silver, R. P. ( 1996; ). Polysialic acid export in Escherichia coli Kl: the role of KpsT, the ATP-binding component of an ABC transporter, in chain translocation. Glycobiology 6, 445–452.[CrossRef]
    [Google Scholar]
  7. Brink, B. A., Miller, J., Carlson, R. W. & Noel, K. D. ( 1990; ). Expression of Rhizobium leguminosarum CFN42 genes for lipopolysaccharide in strains derived from different R. leguminosarum soil isolates. J Bacteriol 172, 548–555.
    [Google Scholar]
  8. Bryan, L. E., O'Hara, K. & Wong, S. ( 1984; ). Lipopolysaccharide changes in impermeability-type aminoglycoside resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother 26, 250–255.[CrossRef]
    [Google Scholar]
  9. Burdman, S., Jurkevitch, E., Schwatsburd, B., Hampel, M. & Okon, Y. ( 1998; ). Aggregation in Azospirillum brasilense: effects of chemical and physical factors and involvement of extracellular components. Microbiology 144, 1989–1999.[CrossRef]
    [Google Scholar]
  10. Burdman, S., Jurkevitch, E., Schwartsburd, B. & Okon, Y. ( 1999; ). Involvement of outer membrane proteins in aggregation of Azospirillum brasilense. Microbiology 145, 1145–1152.[CrossRef]
    [Google Scholar]
  11. Burdman, S., De Mot, R., Vanderleyden, J., Okon, Y. & Jurkevitch, E. ( 2000a; ). Identification and characterization of the omaA gene encoding the major outer membrane protein of Azospirillum brasilense. DNA Seq 11, 225–237.
    [Google Scholar]
  12. Burdman, S., Jurkevitch, E., Soria-Diaz, M. E., Serrano, A. M. G. & Okon, Y. ( 2000b; ). Extracellular polysaccharide composition of Azospirillum brasilense and its relation with cell aggregation. FEMS Microbiol Lett 189, 259–264.[CrossRef]
    [Google Scholar]
  13. Burdman, S., Okon, Y. & Jurkevitch, E. ( 2000c; ). Surface characteristics of Azospirillum brasilense in relation to cell aggregation and attachment to plant roots. Crit Rev Microbiol 26, 91–110.[CrossRef]
    [Google Scholar]
  14. Cava, J. R., Elias, P. M., Turowski, L. D. A. & Noel, K. D. ( 1989; ). Rhizobium leguminosarum CFN42 genetic regions encoding lipopolysaccharide structures essential for complete nodule development on bean plants. J Bacteriol 171, 8–15.
    [Google Scholar]
  15. Chen, J., Lee, S. M. & Mao, Y. ( 2004; ). Protective effect of Escherichia coli O157 : H7 exopolysaccharide colanic acid to osmotic shock and oxidative stress. Int J Food Microbiol 93, 281–286.[CrossRef]
    [Google Scholar]
  16. Chowdhury, S. P., Nagarajan, T., Tripathi, R., Mishra, M. N., Le Rudulier, D. & Tripathi, A. K. ( 2007; ). Strain-specific salt tolerance and osmoregulatory mechanisms in Azospirillum brasilense. FEMS Microbiol Lett 267, 72–79.[CrossRef]
    [Google Scholar]
  17. Creus, C. M., Graziano, M., Casanovas, E. M., Pereyra, M. A., Simontacchi, M., Puntarulo, S., Barassi, C. A. & Lamattina, L. ( 2005; ). Nitric oxide is involved in the Azospirillum brasilense-induced lateral root formation in tomato. Planta 221, 297–303.[CrossRef]
    [Google Scholar]
  18. Croes, C., Van Bastelaere, E., DeClercq, E., Eyers, M., Vanderleyden, J. & Michiels, K. ( 1991; ). Identification and mapping of loci involved in motility, adsorption to wheat roots, colony morphology, and growth in minimal medium on the Azospirillum brasilense Sp7 90-MDa plasmid. Plasmid 26, 83–93.[CrossRef]
    [Google Scholar]
  19. Cuthbertson, L., Powers, J. & Whitfield, C. ( 2005; ). The C-terminal domain of the nucleotide-binding domain protein Wzt determines substrate specificity in the ATP-binding cassette transporter for the lipopolysaccharide O-antigens in Escherichia coli serotypes O8 and O9a. J Biol Chem 280, 30310–30319.[CrossRef]
    [Google Scholar]
  20. Davidson, A. L. ( 2002; ). Mechanism of coupling of transport to hydrolysis in bacterial ATP-binding cassette transporters. J Bacteriol 184, 1225–1233.[CrossRef]
    [Google Scholar]
  21. de Cock, H., Brandenburg, K., Wiese, A., Holst, O. & Seydel, U. ( 1999; ). Non-lamellar structure and negative charges of lipopolysaccharides required for efficient folding of outer membrane protein PhoE of Escherichia coli. J Biol Chem 274, 5114–5119.[CrossRef]
    [Google Scholar]
  22. del Gallo, M., Negi, M. & Neyra, C. A. ( 1989; ). Calcofluor- and lectin-binding exocellular polysaccharides of Azospirillum brasilense and Azospirillum lipoferum. J Bacteriol 171, 3504–3510.
    [Google Scholar]
  23. de Troch, P. ( 1993; ). Bacterial surface polysaccharides in relation to plant interaction: a genetic and chemical study of Azospirillum brasilense. PhD thesis, Katholieke University te Leuven, Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen.
  24. Dische, Z. ( 1962; ). General color reactions. Methods Carbohydr Chem 1, 477–479.
    [Google Scholar]
  25. Dobbelaere, S., Croonenborghs, A., Thys, A., Ptacek, D., Vanderleyden, J., Dutto, P., Lambandera-Gonzalez, C., Caballero-Mellado, J., Aguirre, J. F. & other authors ( 2001; ). Responses of agronomically important crops to inoculation with Azospirillum. Aust J Plant Physiol 28, 871–879.
    [Google Scholar]
  26. El'Garch, F., Jeannot, K., Hocquet, D., Llanes-Barakat, C. & Plésiat, P. ( 2007; ). Cumulative effects of several nonenzymatic mechanisms on the resistance of Pseudomonas aeruginosa to aminoglycosides. Antimicrob Agents Chemother 51, 1016–1021.[CrossRef]
    [Google Scholar]
  27. Fedonenko, Y. P., Zatonsky, G. V., Konnova, S. A., Zdorovenko, E. L. & Ignatov, V. V. ( 2002; ). Structure of the O-specific polysaccharide of the lipopolysaccharide of Azospirillum brasilense Sp245. Carbohydr Res 337, 869–872.[CrossRef]
    [Google Scholar]
  28. Feng, L., Senchenkova, S. N., Yang, J., Shashkov, A. S., Tao, J., Guo, H., Cheng, J., Ren, Y., Knirel, Y. A. & other authors ( 2004; ). Synthesis of the heteropolysaccharide O antigen of Escherichia coli O52 requires an ABC transporter: structural and genetic evidence. J Bacteriol 186, 4510–4519.[CrossRef]
    [Google Scholar]
  29. Figurski, D. H. & Helinski, D. R. ( 1979; ). Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A 76, 1648–1652.[CrossRef]
    [Google Scholar]
  30. Galindo Blaha, C. A. & Schrank, I. S. ( 2003; ). An Azospirillum brasilense Tn5 mutant with modified stress response and impaired in flocculation. Antonie Van Leeuwenhoek 83, 35–43.[CrossRef]
    [Google Scholar]
  31. Godowski, P. J. ( 2005; ). A smooth operator for LPS responses. Nat Immunol 6, 544–546.[CrossRef]
    [Google Scholar]
  32. Guo, D., Bowden, M. G., Pershad, R. & Kaplan, H. B. ( 1996; ). The Myxococcus xanthus rfbABC operon encodes an ABC transporter homolog required for O-antigen biosynthesis and multicellular development. J Bacteriol 178, 1631–1639.
    [Google Scholar]
  33. Hartman, A., Prabhu, S. R. & Galinski, E. A. ( 1991; ). Osmotolerance of diazotrophic rhizosphere bacteria. Plant Soil 137, 105–109.[CrossRef]
    [Google Scholar]
  34. Herschkovitz, Y., Lerner, A., Davidov, Y., Okon, Y. & Jurkevitch, E. ( 2005; ). Azospirillum brasilense does not affect population structure of specific rhizobacterial communities of inoculated maize (Zea mays). Environ Microbiol 7, 1847–1852.[CrossRef]
    [Google Scholar]
  35. Hirai, K., Aoyama, H., Irikura, T., Iyobe, S. & Mitsuhashi, S. ( 1986; ). Differences in susceptibility to quinolones of outer membrane mutants of Salmonella typhimurium and Escherichia coli. Antimicrob Agents Chemother 29, 535–538.[CrossRef]
    [Google Scholar]
  36. Holguin, G., Patten, C. L. & Glick, B. R. ( 1999; ). Genetics and molecular biology of Azospirillum. Biol Fertility Soils 29, 10–23.[CrossRef]
    [Google Scholar]
  37. Holmström, C. & Kjelleberg, S. ( 1999; ). Marine Pseudoalteromonas species are associated with higher organisms and produce biologically active extracellular agents. FEMS Microbiol Ecol 30, 285–293.[CrossRef]
    [Google Scholar]
  38. Jofré, E., Fischer, S., Rivarola, V., Balegno, H. & Mori, G. ( 1998; ). Saline stress affects the attachment of Azospirillum brasilense Cd to maize and wheat roots. Can J Microbiol 44, 416–422.[CrossRef]
    [Google Scholar]
  39. Jofré, E., Lagares, A. & Mori, G. ( 2004; ). Disruption of dTDP-rhamnose biosynthesis modifies lipopolysaccharide core, exopolysaccharide production, and root colonization in Azospirillum brasilense. FEMS Microbiol Lett 231, 267–275.[CrossRef]
    [Google Scholar]
  40. Kadouri, D., Burdman, S., Jurkevitch, E. & Okon, Y. ( 2002; ). Identification and isolation of genes involved in poly(β-hydroxybutyrate) biosynthesis in Azospirillum brasilense and characterization of phbC mutant. Appl Environ Microbiol 68, 2943–2949.[CrossRef]
    [Google Scholar]
  41. Kadouri, D., Jurkevitch, E. & Okon, Y. ( 2003; ). Involvement of the reserve material poly-β-hydroxybutyrate in Azospirillum brasilense stress endurance and root colonization. Appl Environ Microbiol 69, 3244–3250.[CrossRef]
    [Google Scholar]
  42. Katupitiya, S., Millet, J., Vesk, M., Viccars, L., Zeman, A., Lidong, Z., Elmerich, C. & Kennedy, I. R. ( 1995; ). A mutant of Azospirillum brasilense Sp7 impaired in flocculation with a modified colonization pattern and superior nitrogen fixation in association with wheat. Appl Environ Microbiol 61, 1987–1995.
    [Google Scholar]
  43. Katzy, E. I., Matora, L. Y., Serebrennikova, O. B. & Scheludko, A. V. ( 1998; ). Involvement of a 120-Mda plasmid of Azospirillum brasilense Sp245 in the production of lipopolysaccharides. Plasmid 40, 73–83.[CrossRef]
    [Google Scholar]
  44. Kenne, L. & Lindberg, B. ( 1983; ). Bacterial polysaccharides. In The Polysaccharides, pp. 287–365. Edited by G. O. Aspinall. Orlando, FL: Academic Press.
  45. Koebnik, R., Locher, K. P. & Van Gelder, P. ( 2000; ). Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37, 239–257.[CrossRef]
    [Google Scholar]
  46. Konnova, O. N., Burygin, G. L., Fedonenko, Y. P., Matora, L. Y., Pankin, K. E., Konnova, S. A. & Ignatov, V. V. ( 2006; ). Chemical composition and immunochemical characteristics of the lipopolysaccharide of nitrogen fixing rhizobacterium Azospirillum brasilense Cd. Mikrobiologiia 75, 383–388 (in Russian).
    [Google Scholar]
  47. Konnova, O. N., Boiko, A. S., Burygin, G. L., Fedorenko, Y. P., Matora, L. Y., Konnova, S. A. & Ignatov, V. V. ( 2008; ). Chemical and serological studies of liposaccharides of bacteria of the genus Azospirillum. Mikrobiologiia 77, 350–357.
    [Google Scholar]
  48. Kustos, I., Tóth, V., Kocsis, B., Kerepesi, I. & Emo dy, L. & Kilár, F. ( 2000a; ). Capillary electrophoretic analysis of wild type and mutant Proteus penneri outer membrane proteins. Electrophoresis 21, 3020–3027.[CrossRef]
    [Google Scholar]
  49. Kustos, I., Tóth, V., Kilár, F., Kocsis, B. & Emody, L. ( 2000b; ). Effect of spontaneous and induced mutations on outer membrane proteins and lipopolysaccharides of Proteus penneri strain 357. In Genes and Proteins Underlying Microbial Urinary Tract Virulence – Basic Aspects and Applications, pp. 177–181. Edited by L. Emoődy, T. Pál, J. Hacker & G. Blum-Oehler. New York: Springer.
  50. Kyte, J. & Doolittle, R. F. ( 1982; ). A simple method for displaying the hydropathic character of a protein. J Mol Biol 157, 105–132.[CrossRef]
    [Google Scholar]
  51. Laemmli, U. K. ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.[CrossRef]
    [Google Scholar]
  52. Lerner, A., Herschkovitz, Y., Baudoin, E., Nazaret, S., Moenne-Loccoz, Y., Okon, Y. & Jurkevitch, E. ( 2006; ). Effect of Azospirillum brasilense inoculation on rhizobacterial communities analyzed by denaturing gradient gel electrophoresis and automated ribosomal intergenic spacer analysis. Soil Biol Biochem 38, 1212–1218.[CrossRef]
    [Google Scholar]
  53. Lüderitz, O., Freudenberg, M. A., Galanos, C., Lehmann, V., Rietschel, E. Th. & Shaw, D. H. ( 1982; ). Lipopolysaccharides of Gram-negative bacteria. Curr Top Membr Transp 17, 79–151.
    [Google Scholar]
  54. Mao, Y., Doyle, M. P. & Chen, J. ( 2001; ). Insertion mutagenesis of wca reduces acid and heat tolerance of enterohemorrhagic Escherichia coli O157 : H7. J Bacteriol 183, 3811–3815.[CrossRef]
    [Google Scholar]
  55. Matora, L. Y., Solovova, G. K., Serebrennikova, O. B., Selivanov, N. Y. & Shchyogolev, S. Y. ( 1995; ). Immunological properties of Azospirillum cell surface: the structure of carbohydrate antigens and evaluation of their involvement in bacteria–plant contact interactions. In Azospirillum VI and Related Microorganisms, pp. 377–382. Edited by I. Fendrik, M. del Gallo, M. de Zamaroczy & J. Vanderleyden. Berlin: Springer.
  56. McKay, G. A., Woods, D. E., MacDonald, K. L. & Poole, K. ( 2003; ). Role of phosphoglucomutase of Stenotrophomonas maltophilia in lipopolysaccharide biosynthesis, virulence, and antibiotic resistance. Infect Immun 71, 3068–3075.[CrossRef]
    [Google Scholar]
  57. Michel, G., Ball, G., Goldberg, J. B. & Lazdunski, A. ( 2000; ). Alteration of the lipopolysaccharide structure affects the functioning of the Xcp secretory system in Pseudomonas aeruginosa. J Bacteriol 182, 696–703.[CrossRef]
    [Google Scholar]
  58. Michiels, K. W., Croes, C. L. & Vanderleyden, J. ( 1991; ). Two different modes of attachment of Azospirillum brasilense Sp7 to wheat roots. J Gen Microbiol 137, 2241–2246.[CrossRef]
    [Google Scholar]
  59. Moens, S. & Vanderleyden, J. ( 1996; ). Functions of bacterial flagella. Crit Rev Microbiol 22, 67–100.[CrossRef]
    [Google Scholar]
  60. Moniot-Ville, N., Guibert, J., Acar, J. F., Collatz, E. & Gutmann, L. ( 1991; ). Mechanisms of quinolone resistance in a clinical isolate of Escherichia coli highly resistant to fluoroquinolones but susceptible to nalidixic acid. Antimicrob Agents Chemother 35, 519–523.[CrossRef]
    [Google Scholar]
  61. Nikaido, H. & Vaara, M. ( 1985; ). Molecular basis of bacterial outer membrane permeability. Microbiol Rev 49, 1–32.
    [Google Scholar]
  62. Nurminen, M., Hirvas, L. & Vaara, M. ( 1997; ). The outer membrane of lipid A-deficient Escherichia coli mutant LH530 has reduced levels of OmpF and leaks periplasmic enzymes. Microbiology 143, 1533–1537.[CrossRef]
    [Google Scholar]
  63. Ophir, T. & Gutnick, D. L. ( 1994; ). A role for exopolysaccharides in the protection of microorganisms from desiccation. Appl Environ Microbiol 60, 740–745.
    [Google Scholar]
  64. Pattanaik, B., Schumann, R. & Karsten, U. ( 2007; ). Effects of ultraviolet radiation on cyanobacteria and their protective mechanisms. In Algae and Cyanobacteria in Extreme Environments, pp. 31–48. Edited by J. Seckbach. Dordrecht, The Netherlands: Springer.
  65. Petrova, L. P., Matora, L. Y., Burygin, G. L., Borisov, I. V. & Fatsy, E. I. ( 2005; ). Analysis of DNA, lipopolysaccharide structure, and some cultural and morphological properties in closely related strains of Azospirillum brasilense. Mikrobiologiia 74, 224–230 (in Russian).
    [Google Scholar]
  66. Puente, M. E., Holguin, G., Glick, B. R. & Bashan, Y. ( 1999; ). Root-surface colonization of black mangrove seedlings by Azospirillum halopraeferens and Azospirillum brasilense in seawater. FEMS Microbiol Ecol 29, 283–292.[CrossRef]
    [Google Scholar]
  67. Rahaman, S. O., Mukherjee, J., Chakrabarti, A. & Pal, S. ( 1998; ). Decreased membrane permeability in a polymyxin B-resistant Escherichia coli mutant exhibiting multiple resistance to β-lactams as well as aminoglycosides. FEMS Microbiol Lett 161, 249–254.
    [Google Scholar]
  68. Rajyaguru, J. M. & Muszynski, M. J. ( 1997; ). Association of resistance to trimethoprim/sulphamethoxazole, chloramphenicol and quinolones with changes in major outer membrane proteins and lipopolysaccharide in Burkholderia cepacia. J Antimicrob Chemother 40, 803–809.[CrossRef]
    [Google Scholar]
  69. Reizer, J., Reizer, A. & Saier, M. H., Jr ( 1992; ). A new subfamily of bacterial ABC-type transport systems catalyzing export of drugs and carbohydrates. Protein Sci 1, 1326–1332.[CrossRef]
    [Google Scholar]
  70. Reuhs, B. L., Geller, D. P., Kim, J. S., Fox, J. E., Kolli, V. S. K. & Pueppke, S. G. ( 1998; ). Sinorhizobium fredii and Sinorhizobium meliloti produce structurally conserved lipopolysaccharides and strain-specific K antigens. Appl Environ Microbiol 64, 4930–4938.
    [Google Scholar]
  71. Riou, N., Poggi, M. C. & Le Rudukier, D. ( 1991; ). Characterization of an osmoregulated periplasmic glycine betaine-binding protein in Azospirillum brasilense Sp7. Biochimie 73, 1187–1193.[CrossRef]
    [Google Scholar]
  72. Roberson, E. B. & Firestone, M. K. ( 1992; ). Relationship between desiccation and exopolysaccharide production in a soil Pseudomonas sp. Appl Environ Microbiol 58, 1284–1291.
    [Google Scholar]
  73. Rodríguez Cáceres, E. A. ( 1982; ). Improved medium for isolation of Azospirillum spp. Appl Environ Microbiol 44, 990–991.
    [Google Scholar]
  74. Saigí, F., Climent, N., Piqué, N., Sanchez, C., Merino, S., Rubirés, X., Aguilar, A., Tomás, J. M. & Regué, M. ( 1999; ). Genetic analysis of the Serratia marcescens N28b O4 antigen gene cluster. J Bacteriol 181, 1883–1891.
    [Google Scholar]
  75. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  76. Schneider, E. & Hunke, S. ( 1998; ). ATP-binding-cassette (ABC) transport systems: functional and structural aspects of the ATP-hydrolyzing subunits/domains. FEMS Microbiol Rev 22, 1–20.[CrossRef]
    [Google Scholar]
  77. Silver, R. P., Prior, K., Nsahlai, C. & Wright, L. F. ( 2001; ). ABC transporters and the export of capsular polysaccharides from Gram-negative bacteria. Res Microbiol 152, 357–364.[CrossRef]
    [Google Scholar]
  78. Simon, R., Priefer, U. & Puhler, A. ( 1983; ). A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Biotechnology 1, 784–791.[CrossRef]
    [Google Scholar]
  79. Steenhoudt, O. & Vanderleyden, J. ( 2000; ). Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol Rev 24, 487–506.[CrossRef]
    [Google Scholar]
  80. Sukupolvi, S. & Vaara, M. ( 1989; ). Salmonella typhimurium and Escherichia coli mutants with increased outer membrane permeability to hydrophobic compounds. Biochim Biophys Acta 988, 377–387.[CrossRef]
    [Google Scholar]
  81. Tao, H., Brewin, N. J. & Noel, K. D. ( 1992; ). Rhizobium leguminosarum CFN42 lipopolysaccharide antigenic changes induced by environmental conditions. J Bacteriol 174, 2222–2229.
    [Google Scholar]
  82. Tarrand, J. J., Krieg, N. R. & Dobereiner, J. ( 1978; ). A taxonomic study of the Spirillum lipoferum group with the description of a new genus, Azospirillum gen. nov. and two species, Azospirillum lipoferum (Beijerinck) comb. nov. and Azospirillum brasilense sp. nov. Can J Microbiol 24, 967–980.[CrossRef]
    [Google Scholar]
  83. Thomsen, L. E., Chadfield, M. S., Bispham, J., Wallis, T. S., Olsen, J. E. & Ingmer, H. ( 2003; ). Reduced amounts of LPS affect both stress tolerance and virulence of Salmonella enterica serovar Dublin. FEMS Microbiol Lett 228, 225–231.[CrossRef]
    [Google Scholar]
  84. Touze, T., Goude, R., Georgeault, S., Blanco, C. & Bonnassie, S. ( 2004; ). Erwinia chrysanthemi O antigen is required for betaine osmoprotection in high-salt media. J Bacteriol 186, 5547–5550.[CrossRef]
    [Google Scholar]
  85. Tsai, C. M. & Frasch, C. E. ( 1982; ). A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem 119, 115–119.[CrossRef]
    [Google Scholar]
  86. Turcotte, M. L., Martin, D., Brodeur, B. R. & Peppler, M. S. ( 1997; ). Tn5-induced lipopolysaccharide mutations in Bordetella pertussis that affect outer membrane function. Microbiology 143, 2381–2394.[CrossRef]
    [Google Scholar]
  87. Vanbleu, E., Marchal, K., Lambrecht, M., Mathys, J. & Vanderleyden, J. ( 2004; ). Annotation of the pRhico plasmid of Azospirillum brasilense reveals its role in determining the outer surface composition. FEMS Microbiol Lett 232, 165–172.[CrossRef]
    [Google Scholar]
  88. Vanstockem, M., Michiels, K., Vanderleyden, J. & Van Gool, A. P. ( 1987; ). Transposon mutagenesis of Azospirillum brasilense and Azospirillum lipoferum: physical analysis of Tn5 and Tn5-mob insertion mutants. Appl Environ Microbiol 53, 410–415.
    [Google Scholar]
  89. Wai, S. N., Mizunoe, Y. & Yoshida, S. I. ( 1999; ). How Vibrio cholerae survive during starvation. FEMS Microbiol Lett 180, 123–131.[CrossRef]
    [Google Scholar]
  90. Wang, H., Jiang, X., Mu, H., Liang, X. & Guan, H. ( 2007; ). Structure and protective effect of exopolysaccharide from P. agglomerans strain KFS-9 against UV radiation. Microbiol Res 162, 124–129.[CrossRef]
    [Google Scholar]
  91. Whitfield, C., Keenleyside, W. J. & Clarke, B. R. ( 1994; ). Structure, function and synthesis of cell surface polysaccharides in Escherichia coli. In Escherichia coli in Domestic Animals and Man, pp. 437–494. Edited by C. L. Gyles. Wallingford, UK: CAB International.
  92. Wolf, J. K. & Goldberg, J. B. ( 2006; ). Bacterial cell walls. In Molecular Paradigms of Infectious Disease, pp. 176–206. Edited by C. A. Nickerson & M. J. Schurr. New York: Springer.
  93. Yokota, S. & Fujii, N. ( 2007; ). Contributions of the lipopolysaccharide outer core oligosaccharide region on the cell surface properties of Pseudomonas aeruginosa. Comp Immunol Microbiol Infect Dis 30, 97–109.[CrossRef]
    [Google Scholar]
  94. Zuleta, L. F. G., Italiani, V. C. S. & Marques, M. V. ( 2003; ). Isolation and characterization of NaCl-sensitive mutants of Caulobacter crescentus. Appl Environ Microbiol 69, 3029–3035.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.021824-0
Loading
/content/journal/micro/10.1099/mic.0.021824-0
Loading

Data & Media loading...

Supplements

vol. , part 3, pp. 791 - 804

Bacterial strains and plasmids used in this study [PDF file](67 KB)



PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error