Inactivation of the lpcc gene alters surface-related properties and symbiotic capability of bradyrhizobium japonicum

Letters in Applied Microbiology

Volumn 59, Issue 1, 2014, Pages 9-16

  Lee, H I ^a   In, Y H ^a,b   Jeong, S Y ^a,b   Jeon, J M ^a   Noh, J G ^b   So, J S ^b   Chang, W S ^a  

^a UNIVERSITY OF TEXAS AT ARLINGTON   (United States)

^b Inha University   (South Korea)

Author keywords

Biofilm; Bradyrhizobium japonicum; Lipopolysaccharide; lpcC; Motility; Surface hydrophobicity; Symbiotic nitrogen fixation

Indexed keywords

AMINO ACIDS; ANTIGENS; BIOCHEMISTRY; BIOFILMS; CELL MEMBRANES; CYTOLOGY; GENE ENCODING; HYDROPHOBICITY; NITROGEN FIXATION; SURFACE PROPERTIES;

BRADYRHIZOBIUM JAPONICUM; CELL SURFACE HYDROPHOBICITY; LIPOPOLYSACCHARIDES; LPCC; MOTILITY; O-ANTIGEN; SURFACE HYDROPHOBICITY; SURFACE-RELATED PROPERTIES; SYMBIOTIC NITROGEN FIXATION; SYMBIOTICS;

BIOSYNTHESIS;

LIPOPOLYSACCHARIDE;

ANTIGEN; BACTERIUM; BIOFILM; ENZYME ACTIVITY; GROWTH RATE; HYDROPHOBICITY; MOTILITY; NITROGEN FIXATION; POLYSACCHARIDE; SOYBEAN; SYMBIONT;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIUM CULTURE; BACTERIUM MUTANT; BIOFILM; BIOSYNTHESIS; BRADYRHIZOBIUM JAPONICUM; CELL AGGREGATION; CELL SURFACE; CONTROLLED STUDY; GENE INACTIVATION; GROWTH RATE; HYDROPHOBICITY; LPCC GENE; NODULATION; NONHUMAN; SOYBEAN; SURFACE PROPERTY; SYMBIOSIS;

BRADYRHIZOBIUM JAPONICUM; GLYCINE MAX;

BIOFILM; BRADYRHIZOBIUM JAPONICUM; LIPOPOLYSACCHARIDE; LPCC; MOTILITY; SURFACE HYDROPHOBICITY; SYMBIOTIC NITROGEN FIXATION;

BACTERIAL ADHESION; BIOFILMS; BRADYRHIZOBIUM; GENE KNOCKOUT TECHNIQUES; GENES, BACTERIAL; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; O ANTIGENS; ROOT NODULES, PLANT; SOYBEANS; SURFACE PROPERTIES; SYMBIOSIS;

EID: 84902315179     PISSN: 02668254     EISSN: 1472765X     Source Type: Journal    
DOI: 10.1111/lam.12232     Document Type: Article

References (39)

1. Ames, P. and Bergman, K. (1981) Competitive advantage provided by bacterial motility in the formation of nodules by Rhizobium meliloti. J Bacteriol 148, 728-729.
2. Araujo, R.S., Robleto, E.A. and Handelsman, J. (1994) A hydrophobic mutant of Rhizobium etli altered in nodulation competitiveness and growth in the rhizosphere. Appl Environ Microbiol 60, 1430-1436.
3. Becker, A., Fraysse, N. and Sharypova, L. (2005) Recent advances in studies on structure and symbiosis-related function of rhizobial K-antigens and lipopolysaccharides. Mol Plant Microbe Interact 18, 899-905.
4. Bergersen, F.J. (1961) The growth of rhizobium in synthetic media. Aust J Biol Sci 14, 349-360.
5. Borucki, M.K., Peppin, J.D., White, D., Loge, F. and Call, D.R. (2003) Variation in biofilm formation among strains of Listeria monocytogenes. Appl Environ Microbiol 69, 7336-7342.
6. Brechenmacher, L., Lei, Z., Libault, M., Findley, S., Sugawara, M., Sadowsky, M.J., Sumner, L.W. and Stacey, G. (2010) Soybean metabolites regulated in root hairs in response to the symbiotic bacterium Bradyrhizobium japonicum. Plant Plysiol 153, 1808-1822.
7. Broughton, W.J. and Dilworth, M.J. (1971) Control of leghaemoglobin synthesis in snake beans. Biochem J 125, 1075-1080.
8. Caetano-Anolles, G., Wall, L.G., Demicheli, A.T., Macchi, E.M., Bauer, W.D. and Favelukes, G. (1988) Role of motility and chemotaxis in efficiency of nodulation by Rhizobium meliloti. Plant Physiol 86, 1228-1235.
9. Campbell, G.R., Reuhs, B.L. and Walker, G.C. (2002) Chronic intracellular infection of alfalfa nodules by Sinorhizobium meliloti requires correct lipopolysaccharide core. Proc Natl Acad Sci USA 99, 3938-3943.
10. Carlson, R.W., Kalembasa, S., Turowski, D., Pachori, P. and Noel, K.D. (1987) Characterization of the lipopolysaccharide from a Rhizobium phaseoli mutant that is defective in infection thread development. J Bacteriol 169, 4923-4928.
11. Carlson, R.W., Forsberg, L.S. and Kannenberg, E.L. (2010) Lipopolysaccharides in Rhizobium-legume symbioses. In Endotoxins: Structure, Function and Recognition eds Wang, X. and Quinn, P.J. pp. 339-386. New York: Springer.
12. Carrion, M., Bhat, U.R., Reuhs, B. and Carlson, R.W. (1990) Isolation and characterization of the lipopolysaccharides from Bradyrhizobium japonicum. J Bacteriol 172, 1725-1731.
13. Castro, C.D., Molinaro, A., Lanzetta, R., Silipo, A. and Parrilli, M. (2008) Lipopolysaccharide structures from Agrobacterium and Rhizobiaceae species. Carbohydr Res 343, 1924-1933.
14. Cava, J.R., Elias, P.M., Turowski, D.A. and 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.
15. Chang, W.S., Park, K.M., Koh, S.C. and So, J.S. (2008) Characterization of the Bradyrhizobium japonicum galE gene: its impact on lipopolysaccharide profile and nodulation of soybean. FEMS Microbiol Lett 280, 242-249.
16. Datsenko, K.A. and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97, 6640-6645.
17. Dazzo, F.B., Truchet, G.L., Hollingsworth, R.I., Hrabak, E.M., Pankratz, H.S., Philip-Hollingsworth, S., Salzwedel, J.L., Chapman, K. et al. (1991) Rhizobium lipopolysaccharide modulates infection thread development in white clover root hairs. J Bacteriol 173, 5371-5384.
18. Fraysse, N., Couderc, F. and Poinsot, V. (2003) Surface polysaccharide involvement in establishing the rhizobium-legume symbiosis. Eur J Biochem 270, 1365-1380.
19. Fujishige, N.A., Kapadial, N.N., De Hoff, P.L. and Hirsch, A.M. (2006) Investigations of Rhizobium biofilm formation. FEMS Microbiol Ecol 56, 195-206.
20. Kanipes, M.I., Ribeiro, A.A., Lin, S.H., Cotter, R.J. and Raetz, C.R.H. (2003) A mannosyl transferase required for lipopolysaccharide inner core assembly in Rhizobium leguminosarum - Purification, substrate specificity, and expression in Salmonella waaC mutants. J Biol Chem 278, 16356-16364.
21. Lee, Y.W., Jeong, S.Y., In, Y.H., Kim, K.Y., So, J.S. and Chang, W.S. (2010) Lack of O-polysaccharide enhances biofilm formation by Bradyrhizobium japonicum. Lett Appl Microbiol 50, 452-456.
22. Lee, H.I., Lee, J.H., Park, K.H., Sangurdekar, D. and Chang, W.S. (2012) Effect of soybean coumestrol on nodulation ability, biofilm formation, and the transcriptional profile of Bradyrhizobium japonicum. Appl Environ Microbiol 78, 2896-2903.
23. Liu, Y.Q., Gao, W.M., Wang, Y., Wu, L.Y., Liu, X.D., Yan, T.F., Alm, E., Arkin, A. et al. (2005) Transcriptome analysis of Shewanella oneidensis MR-1 in response to elevated salt conditions. J Bacteriol 187, 2501-2507.
24. Noh, J., Kim, D.H., Oh, E.T. and So, J.S. (2002) Characterization of the rfaD gene region of Bradyrhizobium japonicum 61A101C. J Microbiol Biotechnol 12, 826-828.
25. Park, K.M. and So, J.S. (2000) Altered cell surface hydrophobicity of lipopolysaccharide-deficient mutant of Bradyrhizobium japonicum. J Microbiol Methods 41, 219-226.
26. Perez-Gimenez, J., Mongiardini, E.J., Althabegoiti, M.J., Covelli, J., Quelas, J.I., Lopez-Garcia, S.L. and Lodeiro, A.R. (2009) Soybean lectin enhances biofilm formation by Bradyrhizobium japonicum in the absence of plants. Int J Microbiol 2009, 719367.
27. Perotto, S., Brewin, N.J. and Kannenberg, E.L. (1994) Cytological evidence for a host-defense response that reduces cell and tissue invasion in pea nodules by lipopolysaccharide-defective mutants of Rhizobium leguminosarum strain 3841. Mol Plant Microbe Interact 7, 99-112.
28. Priefer, U.B. (1989) Genes involved in lipopolysaccharide production and symbiosis are clustered on the chromosome of Rhizobium leguminosarum biovar viciae Vf39. J Bacteriol 171, 6161-6168.
29. Quandt, J. and Hynes, M.F. (1993) Versatile suicide vectors which allow direct selection for gene replacement in Gram-negative bacteria. Gene 127, 15-21.
30. Rodriguez-Navarro, D.N., Dardanelli, M.S. and Ruiz-Sainz, J.E. (2007) Attachment of bacteria to the roots of higher plants. FEMS Microbiol Lett 272, 127-136.
31. Rosenberg, M., Gutnick, D. and Rosenberg, E. (1980) Adherence of bacteria to hydrocarbons - a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol Lett 9, 29-33.
32. Sadowsky, M.J., Tully, R.E., Cregan, P.B. and Keyser, H.H. (1987) Genetic diversity in Bradyrhizobium japonicum serogroup-123 and its relation to genotype-specific nodulation of soybean. Appl Environ Microbiol 53, 2624-2630.
33. Simon, R., Priefer, U. and Puhler, A. (1983) A broad host range mobilization system for in vivo genetic engineering - Transposon mutagenesis in Gram-negative bacteria. Nat Biotechnol 1, 784-791.
34. So, J.S. (1991) Molecular cloning of a gene region from Bradyrhizobium japonicum essential for lipopolysaccharide synthesis. FEMS Microbiol Lett 83, 299-304.
35. So, J.S., Kim, W.S. and Stacey, G. (2000) Molecular characterization of a gene region involved in lipopolysaccharide biosynthesis in Bradyrhizobium japonicum: cloning, sequencing and expression of rfaF gene. FEMS Microbiol Lett 190, 109-114.
36. Stacey, G., So, J.S., Roth, L.E., Bhagya, L.S.K. and Carlson, R.W. (1991) A lipopolysaccharide mutant of Bradyrhizobium japonicum that uncouples plant from bacterial differentiation. Mol Plant Microbe Interact 4, 332-340.
37. Staskawicz, B., Dahlbeck, D., Keen, N. and Napoli, C. (1987) Molecular characterization of cloned avirulence genes from Race-0 and Race-1 of Pseudomonas syringae pv. Glycinea. J Bacteriol 169, 5789-5794.
38. Vanderlinde, E.M., Muszynski, A., Harrison, J.J., Koval, S.F., Foreman, D.L., Ceri, H., Kannenberg, E.L., Carlson, R.W. et al. (2009) Rhizobium leguminosarum biovar viciae 3841, deficient in 27-hydroxyoctacosanoate-modified lipopolysaccharide, is impaired in desiccation tolerance, biofilm formation and motility. Microbiology 155, 3055-3069.
39. Vedam, V., Haynes, J.G., Kannenberg, E.L., Carlson, R.W. and Sherrier, D.J. (2004) A Rhizobium leguminosarum lipopolysaccharide lipid-A mutant induces nitrogen-fixing nodules with delayed and defective bacteroid formation. Mol Plant Microbe Interact 17, 283-291.