Composition and molar mass characterisation of bacterial extracellular polymeric substances by using chemical, spectroscopic and fractionation techniques
Enrica Alasonati A C and Vera I. Slaveykova A B D
+ Author Affiliations
- Author Affiliations
A Environmental Biophysical Chemistry, IIE-ENAC, Ecole Polytechnique Fédérale de Lausanne (EPFL), Station 2, CH-1015 Lausanne, Switzerland.
B Aquatic Biogeochemistry and Ecotoxicology, Institute F.-A. Forel, Faculty of Sciences, University of Geneva, 10, route de Suisse, CH-1290 Versoix, Switzerland.
C Present address: Laboratoire National de Métrologies et d’Essais, DMSI, Département Biomédical et Chimie Inorganique, 1 rue Gaston Boissier, F-75724 Paris, France.
D Corresponding author. Email: vera.slaveykova@unige.ch
Environmental Chemistry 8(2) 155-162 https://doi.org/10.1071/EN10119
Submitted: 28 October 2010 Accepted: 17 January 2011 Published: 2 May 2011
Environmental context. Extracellular polymeric substances (EPS) released by microorganisms are an important component of organic matter in the environment. EPS play an essential role in cell adhesion to surfaces, biofilm and floc formation, soil aggregation and stability and in the activated sludge of waste water treatment plants. EPS are complex mixtures containing components of different chemical nature and molecular size, which make their characterisation difficult. The present work explores the link between chemical composition and molar-mass distribution of the EPS released by the bacterium Sinorhizobium meliloti by using a combination of chemical, spectroscopic and fractionation techniques.
Abstract. The chemical composition and molar-mass distribution of extracellular polymeric substances (EPS) produced by the bacterium Sinorhizobium meliloti have been characterised by combining asymmetrical flow field-flow fractionation (AFlFFF), chemical and spectroscopic techniques. The relationship between the EPS composition and molar-mass distribution has been studied by comparing the characteristics of EPS excreted by the wild type S. meliloti and by a mutant deficient in the production of high-molar-mass EPS, as well as by the analysis of total protein content in the collected AFlFFF fractions. Total organic carbon, protein and polysaccharide contents of the EPS were also determined. Obtained results demonstrate the existence of two major populations with weight-average molar masses of 1.40 × 105 and 4.57 × 105 g mol–1 respectively. The lower molar-mass population contained predominantly protein-like substances, detectable by UV-VIS spectroscopy, whereas the higher molar-mass population was rich in exopolysaccharides and exoproteins. These findings are in general agreement with the size distributions and chemical heterogeneity observed by nanoparticle tracking analysis, and the characterisation of the composition of all the EPS by different analytical techniques.
Additional keywords: asymmetrical flow field-flow fractionation, bacterium, extracellular polymeric substances, laser light scattering, size and molar mass distributions.
References
[1] J. Wingender, T. R. Neu, H. C. Flemming, Microbial Extracellular Polymeric Substances 1999 (Springer: Berlin).[2] H.-C. Flemming, J. Wingender, The biofilm matrix. Nat. Rev. Microbiol. 2010, 8, 623.
| The biofilm matrix.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsFWlur4%3D&md5=fba2997afdf8963dde771e00742dcbcdCAS | 20676145PubMed |
[3] M. Starkey, K. A. Gray, S. I. Chang, M. R. Parsel, A sticky business: the extracellular polymetic substance matrix of bacterial biofilms, in Microbial Biofilms (Eds M. Ghannoum, G. A. O’Toole) 2004, pp. 174–191 (ASM Press: Washington, DC).
[4] E. B. Roberson, S. Sarig, C. Shennan, M. K. Firestone, Nutritional management of microbial polysaccharide production and aggregation in an agricultural soil. Soil Sci. Soc. Am. J. 1995, 59, 1587.
| Nutritional management of microbial polysaccharide production and aggregation in an agricultural soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpvVSru7g%3D&md5=1508c8855b777d7990366e4665e3a2c9CAS |
[5] K. M. Jones, H. Kobayashi, B. W. Davies, M. E. Taga, G. C. Walker, How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model. Nat. Rev. Microbiol. 2007, 5, 619.
| How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXns12htbc%3D&md5=968244034e7088983208fc4893dff7caCAS | 17632573PubMed |
[6] K. J. Wilkinson, J. R. Lead, Environmental Colloids and Particles 2007, IUPAC Series on Analytical and Physical Chemistry of Environmental Systems, Vol. 10 (Wiley: Chichester).
[7] S. E. Cabaniss, Q. H. Zhou, P. A. Maurice, Y. P. Chin, G. R. Aiken, A log-normal distribution model for the molecular weight of aquatic fulvic acids. Environ. Sci. Technol. 2000, 34, 1103.
| A log-normal distribution model for the molecular weight of aquatic fulvic acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhtVCkt74%3D&md5=bed5d7744c691eb53877c11d36b64c8eCAS |
[8] S. K. Ratanathanawongs Wiliams, D. Lee, Field-flow fractionation of proteins, polysaccharides, synthetic polymers, and supramolecular assemblies. J. Sep. Sci. 2006, 29, 1720.
| Field-flow fractionation of proteins, polysaccharides, synthetic polymers, and supramolecular assemblies.Crossref | GoogleScholarGoogle Scholar | 16977714PubMed |
[9] B. Roda, A. Zattoni, P. Reschiglian, M. H. Moon, M. Mirasoli, E. Michelini, A. Roda, Field-flow fractionation in bioanalysis: a review of recent trends. Anal. Chim. Acta 2009, 635, 132.
| Field-flow fractionation in bioanalysis: a review of recent trends.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1aitro%3D&md5=ff2e4ee2e3c6af9684eae63fb99f24d2CAS | 19216870PubMed |
[10] M. A. Benincasa, C. D. Fratte, Influence of ionic strength, sample size, and flow conditions on the retention behavior of pullulan in flow field-flow fractionation. J. Chromatogr. A 2004, 1046, 175.
| Influence of ionic strength, sample size, and flow conditions on the retention behavior of pullulan in flow field-flow fractionation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmt1Wiur4%3D&md5=8a9d4635987155c1bac5d6adbc244358CAS | 15387187PubMed |
[11] M. H. Moon, D. Y. Shin, N. Lee, E. Hwang, I. H. Cho, Flow field-flow fractionation/multiangle light scattering of sodium hyaluronate from various degradation processes. J. Chromatogr. B 2008, 864, 15.
| Flow field-flow fractionation/multiangle light scattering of sodium hyaluronate from various degradation processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtlCis7o%3D&md5=a6089ac826353bf3e4555d552ff1d7a6CAS |
[12] E. Alasonati, B. Stolpe, M. A. Benincasa, M. Hassellov, V. I. Slaveykova, Asymmetrical flow field flow fractionation – multidetection system as a tool for studying metal-alginate interactions. Environ. Chem. 2006, 3, 192.
| Asymmetrical flow field flow fractionation – multidetection system as a tool for studying metal-alginate interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xms1ersLw%3D&md5=6312e09bacf2c86d63c6ba85b7ddda0eCAS |
[13] B. Wittgren, J. Borgstrom, L. Piculell, K. G. Wahlund, Conformational change and aggregation of kappa-carrageenan studied by flow field-flow fractionation and multiangle light scattering. Biopolymers 1998, 45, 85.
| Conformational change and aggregation of kappa-carrageenan studied by flow field-flow fractionation and multiangle light scattering.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitVenug%3D%3D&md5=c2d1b0adc0b07fe9f01eac9734411d2fCAS |
[14] C. Viebke, P. A. Williams, Determination of molecular mass distribution of kappa-carrageenan and xanthan using asymmetrical flow field-flow fractionation. Food Hydrocoll. 2000, 14, 265.
| Determination of molecular mass distribution of kappa-carrageenan and xanthan using asymmetrical flow field-flow fractionation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXksVOhsrk%3D&md5=3222845bb9c529c56bf3ca364df780b3CAS |
[15] B. Wittgren, K. G. Wahlund, M. Andersson, C. Arfvidsson, Polysaccharide characterization by flow field-flow fractionation-multiangle light scattering: initial studies of modified starches. Int. J. Polym. Anal. Chem. 2002, 7, 19.
| Polysaccharide characterization by flow field-flow fractionation-multiangle light scattering: initial studies of modified starches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivFGnsL8%3D&md5=7bbe4fd993ce6a1d172559ce38ba0114CAS |
[16] A. M. Lambo-Fodje, M. Leeman, K. G. Wahlund, M. Nyman, R. Oste, H. Larsson, Molar mass and rheological characterisation of an exopolysaccharide from Pediococcus damnosus. Carbohydr. Polym. 2007, 68, 577.
| Molar mass and rheological characterisation of an exopolysaccharide from Pediococcus damnosus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXislWgs7c%3D&md5=3e61c5e34ec46e763fa4acb691581326CAS |
[17] P. Reschiglian, A. Zattoni, B. Roda, L. Cinque, D. Parisi, A. Roda, F. Dal Piaz, M. H. Moon, B. R. Min, On-line hollow-fiber flow field-flow fractionation-electrospray ionization/time-of-flight mass spectrometry of intact proteins. Anal. Chem. 2005, 77, 47.
| On-line hollow-fiber flow field-flow fractionation-electrospray ionization/time-of-flight mass spectrometry of intact proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpvFWjt7o%3D&md5=7accf513eba4207cb3ab024971002bc7CAS | 15623277PubMed |
[18] H. J. Hwang, S. W. Kim, C. P. Xu, J. W. Choi, J. W. Yun, Production and molecular characteristics of four groups of exopolysaccharides from submerged culture of Phellinus gilvus. J. Appl. Microbiol. 2003, 94, 708.
| Production and molecular characteristics of four groups of exopolysaccharides from submerged culture of Phellinus gilvus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtlOhtrs%3D&md5=c62cdae0e9c09eee782b0b29b89af19bCAS | 12631207PubMed |
[19] H. J. Hwang, S. W. Kim, J. W. Choi, J. W. Yun, Production and characterization of exopolysaccharides from submerged culture of Phellinus linteus KCTC 6190. Enzyme Microb. Technol. 2003, 33, 309.
| Production and characterization of exopolysaccharides from submerged culture of Phellinus linteus KCTC 6190.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvVWisLY%3D&md5=047c4247c6169f4d087744995a91f655CAS |
[20] S. W. Kim, C. P. Xu, H. J. Hwang, J. W. Choi, C. W. Kim, J. W. Yun, Production and characterization of exopolysaccharides from an enthomopathogenic fungus Cordyceps militaris NG3. Biotechnol. Prog. 2003, 19, 428.
| Production and characterization of exopolysaccharides from an enthomopathogenic fungus Cordyceps militaris NG3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xos1Kjsb0%3D&md5=554d7a12cab975100c3c99b230874e3cCAS | 12675583PubMed |
[21] A. Ricciardi, E. Parente, M. A. Crudele, F. Zanetti, G. Scolari, I. Mannazzu, Exopolysaccharide production by Streptococcus thermophilus SY: production and preliminary characterization of the polymer. J. Appl. Microbiol. 2002, 92, 297.
| Exopolysaccharide production by Streptococcus thermophilus SY: production and preliminary characterization of the polymer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhsVGktb4%3D&md5=94c9ad816106c41839cc3b308a528afaCAS | 11849358PubMed |
[22] P. Ruas-Madiedo, C. G. De Los Reyes-Gavilan, Invited review: Methods for the screening, isolation, and characterization of exopolysaccharides produced by lactic acid bacteria. J. Dairy Sci. 2005, 88, 843.
| Invited review: Methods for the screening, isolation, and characterization of exopolysaccharides produced by lactic acid bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitFygtrg%3D&md5=a11319fafa9772b4db4ffa8266f2dc2dCAS | 15738217PubMed |
[23] C. P. Xu, J. W. Yun, Influence of aeration on the production and the quality of the exopolysaccharides from Paecilomyces tenuipes C240 in a stirred-tank fermenter. Enzyme Microb. Technol. 2004, 35, 33.
| Influence of aeration on the production and the quality of the exopolysaccharides from Paecilomyces tenuipes C240 in a stirred-tank fermenter.Crossref | GoogleScholarGoogle Scholar |
[24] C. Garnier, T. Gorner, B. S. Lartiges, S. Abdelouhab, P. De Donato, Characterization of activated sludge exopolymers from various origins: A combined size-exclusion chromatography and infrared microscopy study. Water Res. 2005, 39, 3044.
| Characterization of activated sludge exopolymers from various origins: A combined size-exclusion chromatography and infrared microscopy study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXms1Ols7k%3D&md5=212317766cd89604f992f50f8d828ec0CAS | 15996704PubMed |
[25] J. E. Gonzalez, G. M. York, G. C. Walker, Rhizobium meliloti exopolysaccharides: Synthesis and symbiotic function. Gene 1996, 179, 141.
| Rhizobium meliloti exopolysaccharides: Synthesis and symbiotic function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xnt1WisbY%3D&md5=2171125cf5eac29333ccf41e008d1f42CAS | 8955640PubMed |
[26] B. B. Reinhold, S. Y. Chan, T. L. Reuber, A. Marra, G. C. Walker, V. N. Reinhold, Detailed structural characterization of succinoglycan, the major exopolysaccharide of Rhizobium meliloti Rm1021. J. Bacteriol. 1994, 176, 1997.
| 1:CAS:528:DyaK2cXis1Gnt7k%3D&md5=48f27a94ebdceee1a75b037b462f8526CAS | 8144468PubMed |
[27] E. Alasonati, S. Dubascoux, G. Lespes, V. I. Slaveykova, Assessment of metal-extracellular polymeric substances interactions by asymmetrical flow field-flow fractionation coupled to inductively coupled plasma mass spectrometry. Environ. Chem. 2010, 7, 215.
| Assessment of metal-extracellular polymeric substances interactions by asymmetrical flow field-flow fractionation coupled to inductively coupled plasma mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsFelur4%3D&md5=18431672ce2b5ed843e3dcc074ce7842CAS |
[28] C. Lamelas, M. Benedetti, K. J. Wilkinson, V. I. Slaveykova, Characterization of H+ and Cd2+ binding properties of the bacterial exopolysaccharides. Chemosphere 2006, 65, 1362.
| Characterization of H+ and Cd2+ binding properties of the bacterial exopolysaccharides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVagsb3O&md5=a5c8e57807f75c6abebe365334b6d1edCAS | 16753198PubMed |
[29] V. I. Slaveykova, N. Parthasarathy, K. Dedieu, D. Toescher, Role of extracellular compounds in Cd-sequestration relative to Cd uptake by bacterium Sinorhizobium meliloti. Environ. Pollut. 2010, 158, 2561.
| Role of extracellular compounds in Cd-sequestration relative to Cd uptake by bacterium Sinorhizobium meliloti.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXos1yktrk%3D&md5=7979521d953db1b0e2a2eae39092a23bCAS | 20541857PubMed |
[30] K. Dedieu, T. Iuranova, V. I. Slaveykova, Do exudates affect cadmium speciation and bioavailability to the rhizobacterium Sinorhizobium meliloti? Environ. Chem. 2006, 3, 424.
| Do exudates affect cadmium speciation and bioavailability to the rhizobacterium Sinorhizobium meliloti?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlWnur7K&md5=6ca4be0663c05fca0633221267af9a61CAS |
[31] M. M. Bradford, A rapid and sensitive method for the estimation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248.
| A rapid and sensitive method for the estimation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=2e50d781c5da7c7a5f626b36d3cd5a68CAS | 942051PubMed |
[32] S. M. Myklestad, E. Skanoy, S. Hestmann, A sensitive and rapid method for analysis of dissolved mono- and polysaccharides in seawater. Mar. Chem. 1997, 56, 279.
| A sensitive and rapid method for analysis of dissolved mono- and polysaccharides in seawater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhsFClsr8%3D&md5=78f8e848a3dc296e829edddb486d5737CAS |
[33] Refractive index detector 2008 (Viscotekcorporation). Available at http://www.malvern.com/LabEng/technology/gel_permeation_chromatography_theory/refractive_index_detector_gpc_theory.htm [Verified 4 April 2011].
[34] M. Schimpf, K. Caldwell, J. C. Giddings, Field-Flow Fractionation Handbook 2000 (Wiley: Chichester).
[35] A. Litzen, K. G. Wahlund, Zone broadening and dilution in rectangular and trapezoidal asymmetrical flow field-flow fractionation channels. Anal. Chem. 1991, 63, 1001.
| Zone broadening and dilution in rectangular and trapezoidal asymmetrical flow field-flow fractionation channels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhvVKms7Y%3D&md5=c14ae5eadf6ac8327f237d7b338f8e7dCAS |
[36] S. Elliott, J. R. Lead, A. Baker, Characterisation of the fluorescence from freshwater, planktonic bacteria. Water Res. 2006, 40, 2075.
| Characterisation of the fluorescence from freshwater, planktonic bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksFyju70%3D&md5=f76df4a167e6e4f1e8ce82bc9b482971CAS | 16697027PubMed |
[37] G. P. Sheng, H. Q. Yu, Z. Yu, Extraction of extracellular polymeric substances from the photosynthetic bacterium Rhodopseudomonas acidophila. Appl. Microbiol. Biotechnol. 2005, 67, 125.
| Extraction of extracellular polymeric substances from the photosynthetic bacterium Rhodopseudomonas acidophila.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksFagt74%3D&md5=253a11d9eac53222090882e13d0577f0CAS | 15309338PubMed |
[38] B.-J. Ni, F. Fang, W. M. Xie, M. Sun, G.-P. Sheng, W.-H. Li, H.-Q. Yu, Characterization of extracellular polymeric substances produced by mixed microorganisms in activated sludge with gel-permeating chromatography, excitation-emission matrix fluorescence spectroscopy measurement and kinetic modelling. Water Res. 2009, 43, 1350.
| Characterization of extracellular polymeric substances produced by mixed microorganisms in activated sludge with gel-permeating chromatography, excitation-emission matrix fluorescence spectroscopy measurement and kinetic modelling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXislKlsro%3D&md5=55e3e5546b9a3bcf613954da7805de48CAS | 19215955PubMed |
[39] L. C. Ong, Y. H. Lin, Metabolite profiles and growth characteristics of Rhizobium meliloti cultivated at different specific growth rates. Biotechnol. Prog. 2003, 19, 714.
| Metabolite profiles and growth characteristics of Rhizobium meliloti cultivated at different specific growth rates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhslSlurs%3D&md5=80eb9a72851fa70a86a5da0966b41d44CAS | 12790629PubMed |
[40] R. Russa, M. Bruneteau, A. S. Shashkov, T. Urbaniksypniewska, H. Mayer, Characterization of the lipopolysaccharides from Rhizobium meliloti strain 102F51 and its nonnodulating mutant WL113. Arch. Microbiol. 1996, 165, 26.
| Characterization of the lipopolysaccharides from Rhizobium meliloti strain 102F51 and its nonnodulating mutant WL113.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XisVersb8%3D&md5=91ba08da5ed9f7b7ccb0c5246a7c6a93CAS | 8639022PubMed |
[41] A. M. Cosme, A. Becker, M. R. Santos, L. A. Sharypova, P. M. Santos, L. M. Moreira, The outer membrane protein TolC from Sinorhizobium meliloti affects protein secretion, polysaccharide biosynthesis, antimicrobial resistance, and symbiosis. Mol. Plant Microbe Interact. 2008, 21, 947.
| The outer membrane protein TolC from Sinorhizobium meliloti affects protein secretion, polysaccharide biosynthesis, antimicrobial resistance, and symbiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsVOqsr8%3D&md5=af5a88ff2096a6dca2471320de857c1eCAS | 18533835PubMed |
[42] M. Fauvart, J. Michiels, Rhizobial secreted proteins as determinants of host specificity in the rhizobium-legume symbiosis. FEMS Microbiol. Lett. 2008, 285, 1.
| Rhizobial secreted proteins as determinants of host specificity in the rhizobium-legume symbiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpt12htbc%3D&md5=d81e1bd7e3a08d13ae8809c59ca66ccdCAS | 18616593PubMed |
[43] A. F. Haag, S. Wehmeier, S. Beck, V. L. Marlow, V. Fletcher, E. K. James, G. P. Ferguson, The Sinorhizobium meliloti LpxXL and AcpXL proteins play important roles in bacteroid development within alfalfa. J. Bacteriol. 2009, 191, 4681.
| The Sinorhizobium meliloti LpxXL and AcpXL proteins play important roles in bacteroid development within alfalfa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosl2ltrk%3D&md5=10cfab6be94cb38dbf27cfaeb4fc2062CAS | 19429615PubMed |
[44] A. Becker, K. Niehaus, A. Puhler, Low-molecular-weight succinoglycan is predominantly produced by Rhizobium meliloti strains carrying a mutated Exop protein characterized by a periplasmic N-terminal domain and a missing C-terminal domain. Mol. Microbiol. 1995, 16, 191.
| Low-molecular-weight succinoglycan is predominantly produced by Rhizobium meliloti strains carrying a mutated Exop protein characterized by a periplasmic N-terminal domain and a missing C-terminal domain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlvV2lurg%3D&md5=dcd5b4b07248c155a1dca8e7679a95ecCAS | 7565082PubMed |
[45] L. X. Wang, Y. Wang, B. Pellock, G. C. Walker, Structural characterization of the symbiotically important low-molecular-weight succinoglycan of Sinorhizobium meliloti. J. Bacteriol. 1999, 181, 6788..
| 10542182PubMed |
[46] J. A. Leigh, G. C. Walker, Exopolysaccharides of Rhizobium: Synthesis, regulation and symbiotic function. Trends Genet. 1994, 10, 63.
| Exopolysaccharides of Rhizobium: Synthesis, regulation and symbiotic function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXktVCmt7k%3D&md5=40a479b468f72bd1edab858ef6089ba4CAS | 8191588PubMed |
[47] A. Becker, M. J. Barnett, D. Capela, M. Dondrup, P. B. Kamp, E. Krol, B. Linke, S. Rueberg, K. Runte, B. K. Schroeder, S. Weidner, S. N. Yurgel, J. Batut, S. R. Long, A. Puehler, A. Goesmann, A portal for rhizobial genomes: RhizoGATE integrates a Sinorhizobium meliloti genome annotation update with postgenome data. J. Biotechnol. 2009, 140, 45.
| A portal for rhizobial genomes: RhizoGATE integrates a Sinorhizobium meliloti genome annotation update with postgenome data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjtFOjtLc%3D&md5=020e2532b73746bf6cba3b942b6ee67eCAS | 19103235PubMed |
[48] B. J. Pellock, M. Teplitski, R. P. Boinay, W. D. Bauer, G. C. Walker, A LuxR homolog controls production of symbiotically active extracellular polysaccharide II by Sinorhizobium meliloti. J. Bacteriol. 2002, 184, 5067.
| A LuxR homolog controls production of symbiotically active extracellular polysaccharide II by Sinorhizobium meliloti.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xmslyktbs%3D&md5=49bd0dce2e8c131514466dfc485552c3CAS | 12193623PubMed |
[49] N. Fraysse, B. Lindner, Z. Kaczynski, L. Sharypova, O. Holst, K. Niehaus, V. Poinsot, Sinorhizobium meliloti strain 1021 produces a low-molecular-mass capsular polysaccharide that is a homopolymer of 3-deoxy-D-manno-oct-2-ulosonic acid harboring a phospholipid anchor. Glycobiology 2005, 15, 101. [Published online ahead of print 8 September 2004]
[50] L. P. T. M. Zevenhuizen, Succinoglycan and galactoglucan. Carbohydr. Polym. 1997, 33, 139.
| Succinoglycan and galactoglucan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitVSktQ%3D%3D&md5=b1a5b01a1490e4c8009d961589579ce0CAS |
[51] H. J. Zhan, C. C. Lee, J. A. Leigh, Induction of the 2nd exopolysaccharide (Epsb) in Rhizobium meliloti Su47 by low phosphate concentrations. J. Bacteriol. 1991, 173, 7391..
| 1938929PubMed |
[52] P. Delepelaire, Type I secretion in gram-negative bacteria. Biochim. Biophys. Acta 2004, 1694, 149.
| Type I secretion in gram-negative bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpslOltb0%3D&md5=df58cbbaf86bb05864a0699b1a67b1b9CAS | 15546664PubMed |
[53] D. Keating, The Sinorhizobium meliloti ExoR protein is required for the downregulation of lpsS transcription and succinoglycan biosynthesis in response to divalent cations. FEMS Microbiol. Lett. 2007, 267, 23.
| The Sinorhizobium meliloti ExoR protein is required for the downregulation of lpsS transcription and succinoglycan biosynthesis in response to divalent cations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVWksbo%3D&md5=ecb16e0ca04d3fd180a1363840e7c164CAS | 17233674PubMed |
[54] J. F. L. Duval, V. I. Slaveykova, M. Hosse, J. Buffle, K. J. Wilkinson, Electrohydrodynamic properties of succinoglycan as probed by fluorescence correlation spectroscopy, potentiometric titration and capillary electrophoresis. Biomacromolecules 2006, 7, 2818.
| Electrohydrodynamic properties of succinoglycan as probed by fluorescence correlation spectroscopy, potentiometric titration and capillary electrophoresis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xptlelurw%3D&md5=27ed5e459dedb971aa43a059ced43135CAS | 17025358PubMed |
