Preferences help
enabled [disable] Abstract
Number of results
2016 | 63 | 3 | 517-525
Article title

Rhizobium strains differ considerably in outer membrane permeability and polymyxin B resistance

Title variants
Languages of publication
Six rhizobium (Rhizobium leguminosarum bv. Trifolii TA1, Sinorhizobium meliloti 1021, Mesorhizobium huakuii IFO 15243T, Ochrobactrum lupini LUP 21T, Bradyrhizobium japonicum USDA110 and B. elkanii USDA 76) and two Escherichia coli strains (E. coli ATCC 25922 and E. coli HB 101) were compared in respect to polymyxin B and EDTA resistance, as well as bacterial outer membrane (OM) permeability to a fluorescent hydrophobic agent (N-phenyl-1-naphthylamine - NPN). TEM (Transmission Electron Microscopy) and a microbial test demonstrated that all the rhizobia were much more resistant to polymyxin B in comparison with E. coli strains. EDTA and polymyxin B enhance permeability of B. japonicum and O. lupini OM. Other rhizobia incorporated NPN independently of the presence of membrane-deteriorating agents; however, the level of fluorescence (measured as NPN absorption) was strain dependent.
Physical description
  • Department of Genetics and Microbiology, Maria Curie-Sklodowska University, Lublin, Poland
  • Department of Genetics and Microbiology, Maria Curie-Sklodowska University, Lublin, Poland
  • Department of Genetics and Microbiology, Maria Curie-Sklodowska University, Lublin, Poland
  • Department of Biochemistry, Maria Curie-Sklodowska University, Lublin, Poland
  • Department of Comparative Anatomy and Anthropology, Maria Curie-Sklodowska University, Lublin, Poland
  • Department of Genetics and Microbiology, Maria Curie-Sklodowska University, Lublin, Poland
  • Department of Genetics and Microbiology, Maria Curie-Sklodowska University, Lublin, Poland
  • Bhat UR, Carlson RW, Busch M, Mayer H (1991a) Distribution and phylogenetic significance of 27-hydroxy-octacosanoic acid in lipopolysaccharides from bacteria belonging to the alpha-2 subgroup of Proteobacteria. Int J Syst Bacteriol 41: 213-217.
  • Bhat UR, Forsberg LS, Carlson RW (1994) Structure of lipid A component of Rhizobium leguminosarum bv. phaseoli lipopolysaccharide. J Biol Chem 269: 14402-14410.
  • Bhat UR, Mayer H, Yokota A, Hollingsworth RI, Carlson RW (1991b) Occurrence of lipid A variants with 27-hydroxyoctacosanoic acid in lipopolysaccharides from members of the family Rhizobiaceae. J Bacteriol 173: 2155-2159.
  • Carlson RW, Forsberg LS, Kannenberg EL (2010) Lipopolysaccharides in Rhizobium-legume symbioses. Subcell Biochem 53: 339-386. doi: 10.1007/978-90-481-9078-2_16.
  • Carlson RW (1984) Heterogeneity of Rhizobium lipopolysaccharides. J Bacteriol 158: 1012-1017.
  • Chen WX, Li GS, Qi YL, Wang ET, Li JL (1991) Rhizobium huakuii sp. nov. isolated from the root nodules of Astragalus sinicus. Int J Syst Bacteriol 41: 275-280.
  • Choma A, Komaniecka I, Turska-Szewczuk A, Danikiewicz W, Spolnik G (2012) Structure of lipid A from a stem-nodulating bacterium Azorhizobium caulinodans. Carbohydr Res 352: 126-136. doi: 10.1016/j.carres.2012.03.003.
  • Choma A, Komaniecka I (2011) Straight and branched (ω-1)-hydroxylated very long chain fatty acids are components of Bradyrhizobium lipid A. Acta Biochim Pol 58: 51-57.
  • Choma A, Sowinski P, Mayer H (2000) Structure of the O-specific polysaccharide of Mesorhizobium huakuii IFO15243T. Carbohydr Res 329: 459-464.
  • Choma A, Sowiński P (2004) Characterization of Mesorhizobium huakuii lipid A containing both d-galacturonic acid and phosphate residues. Eur J Biochem 271: 1310-1322. doi: 10.1111/j.1432-1033.2004.04038.x.
  • De Castro C, Molinaro A, Lanzetta R, Silipo A, Parrilli M (2008) Lipopolysaccharide structures from Agrobacterium and Rhizobiaceae species. Carbohydr Res 343: 1924-1933. doi: 10.1016/j.carres.2008.01.036.
  • Delamuta JR, Ribeiro RA, Ormeño-Orrillo E, Melo IS, Martínez-Romero E, Hungria M (2013) Polyphasic evidence supporting the reclassification of Bradyrhizobium japonicum group Ia strains as Bradyrhizobium diazoefficiens sp. nov. Int J Syst Evol Microbiol 63: 3342-3351. doi: 10.1099/ijs.0.049130-0.
  • Ding L, Yang L, Weiss TM, Waring AJ, Lehrer RI, Huang HW (2003) Interaction of antimicrobial peptides with lipopolysaccharides. Biochemistry 42: 12251-12259. doi: 10.1021/bi035130.
  • Gil-Serrano AM, Gonzalez-Jimenez I, Tejero-Mateo P, Megias M, Romero-Vazquez MJ (1994) Analysis of the lipid moiety of lipopolysaccharide from Rhizobium tropici CIAT899: Identification of 29-hydroxytriacontanoic acid. J Bacteriol 176: 2454-2457.
  • Gudlavalleti SK, Forsberg LS (2003) Structural characterization of the lipid A component of Sinorhizobium sp. NGR234 rough and smooth form lipopolysaccharide. J Biol Chem 278: 3957-3968. doi: 10.1074/jbc.M210491200.
  • Hartmann M, Berditsch M, Hawecker J, Ardakani MF, Gerthsen D, Ulrich AS (2010) Damage of the bacterial cell envelope by antimicrobial peptides gramicidin S and PGLa as revealed by transmission and scanning electron microscopy. Antimicrob Agents Chemother 54: 3132-3142. doi: 10.1128/AAC.00124-10.
  • Hitchcock PJ, Brown TM (1983) Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J Bacteriol 154: 269-277.
  • Jordan DC (1982) Transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen. nov., a genus of slow-growing root nodule bacteria from leguminous plants. Int J Syst Bacteriol 32: 136-139.
  • Kannenberg EL, Carlson RW (2001) Lipid A and O-chain modifications cause Rhizobium lipopolysaccharides to become hydrophobic during bacteroid development. Mol Microbiol 39: 379-391. doi: 10.1046/j.1365-2958.2001.02225.
  • Komaniecka I, Choma A, Lindner B, Holst O (2010) The structure of a novel neutral lipid A from the lipopolysaccharide of Bradyrhizobium elkanii containing three mannoses units in the backbone. Chem Eur J 16: 2922-2929. doi: 10.1002/chem.200902390.
  • Komaniecka I, Choma A, Mazur A, Duda KA, Lindner B, Schwudke D, Holst O (2014) Occurrence of an unusual hopanoid-containing lipid A among lipopolysaccharides from Bradyrhizobium species. J Biol Chem 289: 35644-35655. doi: 10.1074/jbc.M114.614529.
  • Kuykendall LD, Saxena B, Devine TE, Udell SE (1992) Genetic diversity in Bradyrhizobium japonicum Jordan 1982 and a proposal for Bradyrhizobium elkanii sp. nov. Can J Microbiol 38: 501-505. doi: 10.1139/m92-082.
  • Lesse AJ, Campagnari AA, Bittner WE, Apicella MA (1990) Increased resolution of lipopolysaccharides and lipooligosaccharides utilizing tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis. J Immunol Methods 126: 109-117. doi: 10.1016/0022-1759(90)90018-Q.
  • Loh B, Grant C, Hancock RE (1984) Use of the fluorescent probe 1-N-phenylnaphthylamine to study the interactions of aminoglycoside antibiotics with the outer membrane of Pseudomonas aeruginosa. Antimicrob Agents Chemother 26: 546-551.
  • Manterola L, Moriyón I, Moreno E, Sola-Landa A, Weiss DS, Koch MH, Howe J, Brandenburg K, López-Goñi I (2005) The lipopolysaccharide of Brucella abortus BvrS/BvrR mutants contains lipid A modifications and has higher affinity for bactericidal cationic peptides. J Bacteriol 187: 5631-5639. doi: 10.1128/JB.187.16.5631-5639.2005.
  • Mares J, Kumaran S, Gobbo M, Zerbe O (2009) Interactions of lipopolysaccharide and polymyxin studied by NMR spectroscopy. J Biol Chem 284: 11498-11506. doi: 10.1074/jbc.M806587200.
  • Martínez de Tejada G, Pizarro-Cerdá J, Moreno E, Moriyón I (1995) The outer membranes of Brucella spp. are resistant to bactericidal cationic peptides. Infect Immun 63: 3054-3061.
  • Meade HM, Long SR, Ruvkun GB, Brown SE, Ausubel FM (1982) Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis. J Bacteriol 149: 114-122.
  • Muszynski A, Laus M, Kijne JW, Carlson RW (2011) Structures of the lipopolysaccharides from Rhizobium leguminosarum RBL5523 and its UDP-glucose dehydrogenase mutant (exo5). Glycobiology 21: 55-68. doi: 10.1093/glycob/cwq131.
  • Nikaido H (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67: 593-656. doi: 10.1128/MMBR.67.4.593-656.2003.
  • Orwa JA, Govaerts C, Busson R, Roets E, Van Schepdael A, Hoogmartens J (2001) Isolation and structural characterization of polymyxin B components. J Chromatogr A 912: 369-373. doi: 10.1016/S0021-9673(01)00585-4.
  • Pac M, Komaniecka I, Zamlynska K, Turska-Szewczuk A, Choma A (2015) Structure of the O-specific polysaccharide from the legume endosymbiotic bacterium Ochrobactrum cytisi strain ESC1T. Carbohydr Res 413: 37-40. doi: 10.1016/j.carres.2015.05.002.
  • Palusińska-Szysz M, Zdybicka-Barabas A, Pawlikowska-Pawlęga B, Mak P, Cytryńska M (2012) Anti-Legionella dumoffii activity of Galleria mellonella defensin and apolipophorin III. Int J Mol Sci 13: 17048-17064. doi: 10.3390/ijms131217048.
  • Que NL, Lin S, Cotter RJ, Raetz CR (2000) Purification and mass spectrometry of six lipid A species from the bacterial endosymbiont Rhizobium etli. J Biol Chem 275: 28006-28016. doi: 10.1074/jbc.M004008200.
  • Raetz CR, Whitfield C (2002) Lipopolysaccharide endotoxins. Annu Rev Biochem 71: 635-700. doi: 10.1146/annurev.biochem.71.110601.135414.
  • Riley LK, Robertson DC (1984) Brucellacidal activity of human and bovine polymorphonuclear leukocyte granule extracts against smooth and rough strains of Brucella abortus. Infect Immun 46: 231-236.
  • Russa R, Urbanik-Sypniewska T, Lindström K, Mayer H (1995) Chemical characterization of two lipopolysaccharide species isolated from Rhizobium loti NZP2213. Arch Microbiol 163: 345-351.
  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
  • Sawyer JG, Martin NL, Hancock RE (1988) Interaction of macrophage cationic proteins with the outer membrane of Pseudomonas aeruginosa. Infect Immun 56: 693-698.
  • Schindler PR, Teuber M (1975) Action of polymyxin B on bacterial membranes: morphological changes in the cytoplasm and in the outer membrane of Salmonella typhimurium and Escherichia coli B. Antimicrob Agents Chemother 8: 95-104.
  • Silipo A, Vitiello G, Gully D, Sturiale L, Chaintreuil C, Fardoux J, Gargani D, Lee HI, Kulkarni G, Busset N, Marchetti R, Palmigiano A, Moll H, Engel R, Lanzetta R, Paduano L, Parrilli M, Chang WS, Holst O, Newman DK, Garozzo D, D'Errico G, Giraud E, Molinaro A (2014) Covalently linked hopanoid-lipid A improves outer-membrane resistance of a Bradyrhizobium symbiont of legumes. Nat Commun 5: 5106. doi: 10.1038/ncomms6106.
  • Triplett EW (1988) Isolation of genes involved in nodulation competitiveness from Rhizobium leguminosarum bv. trifolii T24. Proc Natl Acad Sci USA 85: 3810-3814.
  • Trujillo ME, Willems A, Abril A, Planchuelo AM, Rivas R, Ludena D, Mateos PF, Martinez-Molina E, Velazquez E (2005) Nodulation of Lupinus albus by strains of Ochrobactrum lupini sp. nov. Appl Environ Microbiol 71: 1318-1327. [Erratum: Appl Environ Microbiol (2006) 72(6): 4500]. doi: 10.1128/AEM.71.3.1318-1327.2005.
  • Tsai CM, Frasch CE (1982) A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem 119: 115-119. doi: 10.1016/0003-2697(82)90673-X.
  • Vaara M (1992) Agents that increase the permeability of the outer membrane. Microbiol Rev 56: 395-411.
  • Velasco J, Bengoechea JA, Brandenburg K, Lindner B, Seydel U, González D, Zähringer U, Moreno E, Moriyón I (2000) Brucella abortus and its closest phylogenetic relative, Ochrobactrum spp., differ in outer membrane permeability and cationic peptide resistance. Infect Immun 68: 3210-3218.
  • Vincent JM (1970) A manual for the practical study of root-nodule bacteria. International biological program handbook no. 15. Blackwell Scientific Publications Ltd, Oxford.
  • Wu M, Maier E, Benz R, Hancock RE (1999) Mechanism of interaction of different classes of cationic antimicrobial peptides with planar bilayers and with the cytoplasmic membrane of Escherichia coli. Biochemistry 38: 7235-7242. doi: 10.1021/bi9826299.
  • Zähringer U, Lindner B, Rietschel Eth (1999) Chemical structure of lipid A: recent advances in structural analysis of biologically active molecules. In Endotoxin in Health and Disease Brade H, Opal SM, Vogel SN, Morrison DC eds, pp 93-114. Marcel Dekker, New York.
  • Zavascki AP, Goldani LZ, Li J, Nation RL (2007) Polymyxin B for the treatment of multidrug-resistant pathogens: a critical review. J Antimicrob Chemother 60: 1206-1215. doi: 10.1093/jac/dkm357.
Document Type
Publication order reference
YADDA identifier
JavaScript is turned off in your web browser. Turn it on to take full advantage of this site, then refresh the page.