Exopolysaccharide Produced from Rhizobium spp. - An Interesting Product for Industry and Environment

Author(s): Tereza Cristina Luque Castellane*, Bruna Fernanda Silva de Sousa, Eliana Gertrudes de Macedo Lemos

Journal Name: Current Applied Polymer Science

Volume 3 , Issue 3 , 2019

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Graphical Abstract:


Abstract:

Most legume species, such as soybeans, beans, and clover, have the ability to establish a symbiotic relationship with nitrogen-fixing bacteria in the soil, which promotes plant growth and productivity. Exopolysaccharide macromolecules are particularly necessary for binding the bacteria to root hairs and initiating the deformation of root hairs, thus trapping the bacteria to initiate root invasion through a tube-like infection thread. Very few studies have focused on the isolation and characterization of new rhizobial exopolysaccharides, despite their unique and specific biological and physicochemical properties. However, rhizobial exopolysaccharides may be studied in detail in the near future, for the development of suitable substitutes for xanthan gum. This review discusses some analytical strategies for characterization of rhizobial exopolysaccharide, the relation between their structure and properties, and a novel application of rhizobial exopolysaccharides. The potential application of exopolysaccharides and living cells as biosorbents has also been reviewed.

Keywords: Biodegradability, Biological applications, Ensifer, Extracellular carbohydrate polymers, Heavy metals, Rhizobium.

[1]
Jayaraman D, Gilroy S, Ané JM. Staying in touch: Mechanical signals in plant-microbe interactions. Curr Opin Plant Biol 2014; 20: 104-9.
[http://dx.doi.org/10.1016/j.pbi.2014.05.003] [PMID: 24875767]
[2]
Poole P, Ramachandran V, Terpolilli J. Rhizobia: From saprophytes to endosymbionts. Nat Rev Microbiol 2018; 16(5): 291-303.
[http://dx.doi.org/10.1038/nrmicro.2017.171] [PMID: 29379215]
[3]
Carareto LM, Marcondes JA, Varani AM, Lemos EGM. Rhizobiaceae family The prokaryotes 4th. Berlin/Heidelberg/New York: Springer-Verlag 2014; pp. 419-37.
[http://dx.doi.org/10.1007/978-3-642-30197-1_297]
[4]
Marcondes JA, Carareto LM, Varani AM, Lemos EGM. Bradyrhizobiaceae family The prokaryotes 4th. Berlin/Heidelberg/New York: Springer-Verlag 2014; pp. 135-54.
[http://dx.doi.org/10.1007/978-3-642-30197-1_253]
[5]
Downie JA. The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol Rev 2010; 34(2): 150-70.
[http://dx.doi.org/10.1111/j.1574-6976.2009.00205.x] [PMID: 20070373]
[6]
Castellane TCL, Otoboni AMMB, Lemos EG de M. Characterization of exopolysaccharides produced by rhizobia species. Rev Bras Ciênc Solo 2015; 39(6): 1566-75.
[http://dx.doi.org/10.1590/01000683rbcs20150084]
[7]
Castellane TCL, Lemos MVF, Lemos EGDM. Evaluation of the biotechnological potential of Rhizobium tropici strains for exopolysaccharide production. Carbohydr Polym 2014; 1(111): 191-7.
[http://dx.doi.org/10.1016/j.carbpol.2014.04.066]
[8]
Cieśla J, Kopycińska M, Łukowska M, Bieganowski A, Janczarek M. Surface properties of wild type Rhizobium leguminosarum bv. trifolii strain 24.2 and its derivatives with different extracellular polysaccharide content. PLoS One 2016; 11(10) e0165080
[http://dx.doi.org/10.1371/journal.pone.0165080] [PMID: 27760230]
[9]
Castellane TCL, Campanharo JC, Colnago LA, et al. Characterization of new exopolysaccharide production by Rhizobium tropici during growth on hydrocarbon substrate. Int J Biol Macromol 2011; 96: 369-1.
[10]
Carlson RW, Forsberg LS, Kannenberg EL. Lipopolysaccharides in rhizobium-legume symbiosesEndotoxins: Structure, function and recognition. Dordrecht: Springer 2010; pp. 386-9.
[http://dx.doi.org/10.1007/978-90-481-9078-2_16]
[11]
Kumar MS. SwarnaLakshmi K, Annapurna K Exopolysaccharide from Rhizobia: Production and role in symbiosis Rhizobium biology and biotechnology soil biology. Cham: Springer 2017; Vol. 50: pp. 257-92.
[http://dx.doi.org/10.1007/978-3-319-64982-5_13]
[12]
Marczak M, Mazur A, Koper P, Żebracki K, Skorupska A. Synthesis of rhizobial exopolysaccharides and their importance for symbiosis with legume plants. Genes (Basel) 2017; 8(12): 1-24.
[http://dx.doi.org/10.3390/genes8120360] [PMID: 29194398]
[13]
Gage DJ. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 2004; 68(2): 280-300.
[http://dx.doi.org/10.1128/MMBR.68.2.280-300.2004] [PMID: 15187185]
[14]
Guentas L, Pheulpin P, Michaud P, et al. Structure of a polysaccharide from a Rhizobium species containing 2-deoxy-β-D-arabino-hexuronic acid. Carbohydr Res 2001; 332(2): 167-73.
[http://dx.doi.org/10.1016/S0008-6215(01)00080-5] [PMID: 11434374]
[15]
Yang M, Zhu Y, Li Y, et al. Production and optimization of curdlan produced by Pseudomonas sp. QL212. Int J Biol Macromol 2016; 89: 25-34.
[http://dx.doi.org/10.1016/j.ijbiomac.2016.04.027] [PMID: 27086290]
[16]
Castellane TCL, Persona MR, Campanharo JC, de Macedo Lemos EG. Production of exopolysaccharide from rhizobia with potential biotechnological and bioremediation applications. Int J Biol Macromol 2015; 74: 515-22.
[http://dx.doi.org/10.1016/j.ijbiomac.2015.01.007] [PMID: 25592842]
[17]
Andhare P, Delattre C, Pierre G, Michaud P, Pathak H. Characterization and rheological behaviour analysis of the succinoglycan produced by Rhizobium radiobacter strain CAS from curd sample. Food Hydro 2017; 64: 1-8.
[http://dx.doi.org/10.1016/j.foodhyd.2016.10.008]
[18]
Priyanka P, Arun AB, Ashwini P, Rekha PD. Versatile properties of an exopolysaccharide R-PS18 produced by Rhizobium sp. PRIM-18. Carbohydr Polym 2015; 126: 215-21.
[http://dx.doi.org/10.1016/j.carbpol.2015.03.017] [PMID: 25933542]
[19]
Urai M, Aizawa T, Imamura K, Hamamoto H, Sekimizu K. Characterization of the chemical structure and innate immune-stimulating activity of an extracellular polysaccharide from Rhizobium sp. strain M2 screened using a silkworm muscle contraction assay. Drug Discov Ther 2017; 11(5): 238-45.
[http://dx.doi.org/10.5582/ddt.2017.01045] [PMID: 29021503]
[20]
Sethi D, Mohanty S, Pattanayak SK. Effect of different carbon, nitrogen and vitamine sources on exopolysaccharide production of Rhizobium species isolated from root nodule of redgram. Indian J Biochem Biophys 2019; 56: 86-93.
[21]
Breedveld MW, Cremers HC, Batley M, et al. Polysaccharide synthesis in relation to nodulation behavior of Rhizobium leguminosarum. J Bacteriol 1993; 175(3): 750-7.
[http://dx.doi.org/10.1128/jb.175.3.750-757.1993] [PMID: 8423148]
[22]
Ghosh AC, Ghosh S, Basu PS. Production of extracellular polysaccharide by a Rhizobium species from root nodules of leguminous tree Dalbergia lanceolaria L.f. Eng Life Sci 2005; 5: 378.
[http://dx.doi.org/10.1002/elsc.200500087]
[23]
Ghosh PK, Maiti TK. Structure of extracellular polysaccharides (EPS) produced by Rhizobia and their functions in legume - bacteria symbiosis: A review. Achiev in the Life Scien 2016; 10(2): 136-43.
[http://dx.doi.org/10.1016/j.als.2016.11.003]
[24]
Bomfeti CA, Florentino AF, Guimarães AP, Cardoso PG, Guerreiro MC, Moreira FMS. Exopolysaccharides produced by the symbiotic nitrogen-fixing bacteria of leguminosae. Rev Bras Ciênc Solo 2011; 35: 657-71.
[http://dx.doi.org/10.1590/S0100-06832011000300001]
[25]
de Oliveira JM, Amaral SA, Burkert CAV, Burkert V. Rheological, textural and emulsifying properties of an exopolysaccharide produced by Mesorhizobium loti grown on a crude glycerol-based medium. Int J Biol Macromol 2018; 120(Pt B): 2180-7.
[http://dx.doi.org/10.1016/j.ijbiomac.2018.06.158] [PMID: 29964110]
[26]
Castellane TCL, Lemos MVF, Lemos EGM. Exploring and utilization of some bacterial exopolysaccharide. Biopo Resea 2018; 2(1): 1-7.
[27]
Couto MR, Gudiña EJ, Ferreira D, Teixeira JA, Rodrigues LR. The biopolymer produced by Rhizobium viscosum CECT 908 is a promising agent for application in microbial enhanced oil recovery. N Biotechnol 2019; 49: 144-50.
[http://dx.doi.org/10.1016/j.nbt.2018.11.002] [PMID: 30445186]
[28]
Kawaharada Y, Kelly S, Nielsen MW, et al. Receptor-mediated exopolysaccharide perception controls bacterial infection. Nature 2015; 523(7560): 308-12.
[http://dx.doi.org/10.1038/nature14611] [PMID: 26153863]
[29]
Wang L, Yang J, Chen Z, Liu X, Ma F. Biosorption of Pb(II) and Zn(II) by extracellular polymeric substance (EPS) of Rhizobium radiobacter: Equilibrium, kinetics and reuse studies. Arch Environ Prot 2013; 39(2): 129-40.
[http://dx.doi.org/10.2478/aep-2013-0020]
[30]
Shuhong Y, Meiping Z, Hong Y, et al. Biosorption of Cu(2+), Pb(2+) and Cr(6+) by a novel exopolysaccharide from Arthrobacter ps-5. Carbohydr Polym 2014; 101: 50-6.
[http://dx.doi.org/10.1016/j.carbpol.2013.09.021] [PMID: 24299748]
[31]
Muthu M, Wu H-F, Gopal J, Sivanesan I, Chun S. Exploiting microbial polysaccharides for biosorption of trace elements in aqueous environments-scope for expansion via nanomaterial intervention. Polymers (Basel) 2017; 9(12): 721.
[http://dx.doi.org/10.3390/polym9120721] [PMID: 30966021]
[32]
Gupta P, Diwan B. Bacterial Exopolysaccharide mediated heavy metal removal: A review on biosynthesis, mechanism and remediation strategies. Biotechnol Rep (Amst) 2016; 13: 58-71.
[http://dx.doi.org/10.1016/j.btre.2016.12.006] [PMID: 28352564]
[33]
Upadhyay KH, Vaishnav AM, Tipre DR, et al. Kinetics and mechanisms of mercury biosorption by an exopolysaccharide producing marine isolate Bacillus licheniformis. 3 Biotech 2017; 7: 313.
[34]
Okaiyeto K, Nwodo UU, Mabinya LV, Okoli AS, Okoh AI. Characterization of a Bioflocculant (MBF-UFH) produced by Bacillus sp. AEMREG7. Int J Mol Sci 2015; 16(6): 12986-3003.
[http://dx.doi.org/10.3390/ijms160612986] [PMID: 26062133]
[35]
Medhi K, Thakur IS. Bioremoval of nutrients from wastewater by a denitrifier Paracoccus denitrificans ISTOD1. Bioresource Technology Reports 2018; 1: 56-60.
[http://dx.doi.org/10.1016/j.biteb.2018.02.006]
[36]
Borah D, Nainamalai S, Gopalakrishnan S, et al. Biolubricant potential of exopolysaccharides from the cyanobacterium Cyanothece epiphytica. Appl Microbiol Biotechnol 2018; 102(8): 3635-47.
[http://dx.doi.org/10.1007/s00253-018-8892-x] [PMID: 29520599]
[37]
Badel S, Bernardi T, Michaud P. New perspectives for Lactobacilli exopolysaccharides. Biotechnol Adv 2011; 29(1): 54-66.
[http://dx.doi.org/10.1016/j.biotechadv.2010.08.011] [PMID: 20807563]
[38]
Becker A, Pühler A. Production of exopolysaccharides The rhizobiaceae: Molecular biology of model plant-associated bacteria. Kluwer Academic Publishers 1998; pp. 566-101.
[http://dx.doi.org/10.1007/978-94-011-5060-6_6]
[39]
Fraysse N, Couderc F, Poinsot V. Surface polysaccharide involvement in establishing the rhizobium-legume symbiosis. Eur J Biochem 2003; 270(7): 1365-80.
[http://dx.doi.org/10.1046/j.1432-1033.2003.03492.x] [PMID: 12653992]
[40]
Abinaya M, Vaseeharan B, Divya M, et al. Bacterial exopolysaccharide (EPS)-coated ZnO nanoparticles showed high antibiofilm activity and larvicidal toxicity against malaria and Zika virus vectors. J Trace Elem Med Biol 2018; 45(45): 93-103.
[http://dx.doi.org/10.1016/j.jtemb.2017.10.002] [PMID: 29173489]
[41]
de Sousa BFS, Castellane TCL, Campanharo JC, Lemos EGM. Rhizobium spp. exopolysaccharides production and xanthan lyase use on its structural modification. Int J Biol Macromol 2019; (136): 424-35.
[42]
Zhang J, Liu L, Ren Y, Chen F. Characterization of exopolysaccharides produced by microalgae with antitumor activity on human colon cancer cells. Int J Biol Macromol 2019; 128: 761-7.
[http://dx.doi.org/10.1016/j.ijbiomac.2019.02.009] [PMID: 30726750]
[43]
Bourassa DV, Kannenberg EL, Sherrier DJ, Buhr RJ, Carlson RW. The lipopolysaccharide lipid-A long chain fatty acid is important for Rhizobium leguminosarum growth and stress adaptation in free-living and nodule environments. Mol Plant Microbe Interact 2017; 30(2): 161-75.
[http://dx.doi.org/10.1094/MPMI-11-16-0230-R] [PMID: 28054497]
[44]
Donot F, Fontana A, Baccou JC, Schorr-Galindo S. Microbial exopolysaccharides: Main examples of synthesis, excretion, genetics and extraction. Carb Poly 2012; 87(2): 951-62.
[http://dx.doi.org/10.1016/j.carbpol.2011.08.083]
[45]
Skorupska A, Janczarek M, Marczak M, Mazur A, Król J. Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microb Cell Fact 2006; 5: 7.
[http://dx.doi.org/10.1186/1475-2859-5-7] [PMID: 16483356]
[46]
Marczak M, Żebracki K, Koper P, et al. Mgl2 is a hypothetical methyltransferase involved in exopolysaccharide production, biofilm formation, and motility in Rhizobium leguminosarum bv trifolii. Mol Plant-Microbe Inter 2019.
[http://dx.doi.org/10.1094/MPMI-01-19-0026-R]
[47]
Marczak M, Matysiak P, Kutkowska J, Skorupska A. PssP2 is a polysaccharide co-polymerase involved in exopolysaccharide chain-length determination in Rhizobium leguminosarum. PLoS One 2014; 9(9) e109106
[http://dx.doi.org/10.1371/journal.pone.0109106] [PMID: 25268738]
[48]
Wang D, Couderc F, Tian CF, Gu W, Liu LX, Poinsot V. Conserved composition of nod factors and exopolysaccharides produced by different phylogenetic lineage Sinorhizobium strains nodulating soybean. Front Microbiol 2018; 9: 2852.
[http://dx.doi.org/10.3389/fmicb.2018.02852] [PMID: 30534119]
[49]
Acosta-Jurado S, Navarro-Gómez P, Murdoch Pdel S, et al. Exopolysaccharide production by Sinorhizobium fredii HH103 is repressed by genistein in a NodD1-dependent manner. PLoS One 2016; 11(8) e0160499
[http://dx.doi.org/10.1371/journal.pone.0160499] [PMID: 27486751]
[50]
Wang P, Zhong Z, Zhou J, Cai T, Zhu J. Exopolysaccharide biosynthesis is important for Mesorhizobium tianshanense: plant host interaction. Arch Microbiol 2008; 189(5): 525-30.
[http://dx.doi.org/10.1007/s00203-007-0345-3] [PMID: 18188540]
[51]
Liu W, Sun Y, Shen R, et al. A chemotaxis-like pathway of Azorhizobium caulinodans controls flagella-driven motility, which regulates biofilm formation, exopolysaccharide biosynthesis, and competitive nodulation. Mol Plant Microbe Interact 2018; 31(7): 737-49.
[http://dx.doi.org/10.1094/MPMI-12-17-0290-R] [PMID: 29424664]
[52]
Cuzzi B, Herasimenka Y, Silipo A, et al. Versatility of the Burkholderia cepacia complex for the biosynthesis of exopolysaccharides: A comparative structural investigation. PLoS One 2014; 9(4) e94372
[http://dx.doi.org/10.1371/journal.pone.0094372] [PMID: 24722641]
[53]
Jones KM. Increased production of the exopolysaccharide succinoglycan enhances Sinorhizobium meliloti 1021 symbiosis with the host plant Medicago truncatula. J Bacteriol 2012; 194(16): 4322-31.
[http://dx.doi.org/10.1128/JB.00751-12] [PMID: 22685282]
[54]
Petri DFS. Xanthan gum: A versatile biopolymer for biomedical and technological applications. J Appl Poly Sci 2015; 1(132): 1.
[http://dx.doi.org/10.1002/app.42035]
[55]
Varki A, Cummings RD, Aebi M, et al. symbol nomenclature for graphical representations of glycans. Glycobiology 2015; 25(12): 1323-4.
[http://dx.doi.org/10.1093/glycob/cwv091] [PMID: 26543186]
[56]
Kaci Y, Heyraud A, Barakat M, Heulin T. Isolation and identification of an EPS-producing Rhizobium strain from arid soil (Algeria): characterization of its EPS and the effect of inoculation on wheat rhizosphere soil structure. Res Microbiol 2005; 156(4): 522-31.
[http://dx.doi.org/10.1016/j.resmic.2005.01.012] [PMID: 15862451]
[57]
Muszyński A, Heiss C, Hjuler CT, et al. Structures Of exopolysaccharides involved in receptor-mediated perception of Mesorhizobium loti by Lotus japonicus. J Biol Chem 2016; 291(40): 20946-61.
[http://dx.doi.org/10.1074/jbc.M116.743856] [PMID: 27502279]
[58]
Castellane TCL, Lemos EGDM. Composição de exopolissacarídeos produzidos por estirpes de rizóbios cultivados em diferentes fontes de carbono. Pesqui Agropecu Bras 2007; 42(10): 1503-6.
[http://dx.doi.org/10.1590/S0100-204X2007001000019]
[59]
Moretto C, Castellane TCL, Lopes EM, Omori WP, Sacco LP, Lemos EG de M. Chemical and rheological properties of exopolysaccharides produced by four isolates of rhizobia. Int J Biol Macrom 2015; 1(81): 291-8.
[http://dx.doi.org/10.1016/j.ijbiomac.2015.07.056]
[60]
Zhou F, Wu Z, Chen C, Han J, Ai L, Guo B. Exopolysaccharides produced by Rhizobium radiobacter S10 in whey and their rheological properties. Food Hydro 2014; 581(36): 362-8.
[http://dx.doi.org/10.1016/j.foodhyd.2013.08.016]
[61]
Zhao L, Chen Y, Ren S, Han Y, Cheng H. Studies on the chemical structure and antitumor activity of an exopolysaccharide from Rhizobium sp. N613. Carbohydr Res 2010; 345(5): 637-43.
[http://dx.doi.org/10.1016/j.carres.2009.11.017] [PMID: 20100608]
[62]
Zykwinska A, Marchand L, Bonnetot S, Sinquin C, Colliec-Jouault S, Delbarre-Ladrat C. Deep-sea hydrothermal vent bacteria as a source of glycosaminoglycan-mimetic exopolysaccharides. Molecules 2019; 24(9): 1703.
[http://dx.doi.org/10.3390/molecules24091703] [PMID: 31052416]
[63]
Venugopal V. Polysaccharide from seaweed and microalgae Marine polysaccharides: Food applications; 1nd. Boca Raton, FL, USA, Taylor and Francis Group 2016; pp. 111-22.
[http://dx.doi.org/10.1201/b10516]
[64]
Fitriyanto NA, Nakamura M, Muto S, et al. Ce3+-induced exopolysaccharide production by Bradyrhizobium sp. MAFF211645. J Biosci Bioeng 2011; 111(2): 146-52.
[http://dx.doi.org/10.1016/j.jbiosc.2010.09.008] [PMID: 20947420]
[65]
Alvarez VM, Jurelevicius D, Serrato RV, Barreto-Bergter E, Seldin L. Chemical characterization and potential application of exopolysaccharides produced by Ensifer adhaerens JHT2 as a bioemulsifier of edible oils. Int J Biol Macromol 2018; 114: 18-25.
[http://dx.doi.org/10.1016/j.ijbiomac.2018.03.063] [PMID: 29550419]
[66]
Leonel TF, Moretto C, Castellane TLC, Inácio P, Lemos EGM. The influence of cooper and chromium ions on the production of exopolysaccharide and polyhydroxybutyrate by Rhizobium tropici LBMP-C01. Jour of Polym and the Envir 2019; 0(0): 0.
[67]
Duta FP, De França FP, Sérvulo EFC, De Almeida Lopes LM, Da Costa ACA, Barros A. Effect of process parameters on production of a biopolymer by Rhizobium sp. Appl Biochem Biotechnol 2004; 113-116: 639-52.
[http://dx.doi.org/10.1385/ABAB:114:1-3:639] [PMID: 15054283]
[68]
Redouan E, Emmanuel P, Philippe M, Bernard C, Josiane C, Cedric D. Synthesis of new glycosaminoglycans-like families by regioselective oxidation followed by sulphation of glucoglucuronan from Rhizobium sp. T1. Carbohydr Polym 2012; 89(4): 1261-7.
[http://dx.doi.org/10.1016/j.carbpol.2012.04.035] [PMID: 24750940]
[69]
Masson-Boivin C, Giraud E, Perret X, Batut J. Establishing nitrogen-fixing symbiosis with legumes: How many rhizobium recipes? Trends Microbiol 2009; 17(10): 458-66.
[http://dx.doi.org/10.1016/j.tim.2009.07.004] [PMID: 19766492]
[70]
Madsen LH, Tirichine L, Jurkiewicz A, et al. The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun 2010; 1(1): 10.
[http://dx.doi.org/10.1038/ncomms1009] [PMID: 20975672]
[71]
D’Haeze W, Holsters M. Surface polysaccharides enable bacteria to evade plant immunity. Trends Microbiol 2004; 12(12): 555-61.
[http://dx.doi.org/10.1016/j.tim.2004.10.009] [PMID: 15539115]
[72]
Kopycińska M, Lipa P, Cieśla J, Kozieł M, Janczarek M. Extracellular polysaccharide protects Rhizobium leguminosarum cells against zinc stress in vitro and during symbiosis with clover. Environ Microbiol Rep 2018; 10(3): 355-68.
[http://dx.doi.org/10.1111/1758-2229.12646] [PMID: 29633524]
[73]
Stambulska UY, Bayliak MM, Lushchak VI. Chromium(VI) Toxicity in legume plants: Modulation effects of rhizobial symb. BioMed Res Int 2018. 8031213
[74]
Zahran HH. Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 1999; 63(4): 968-89.
[PMID: 10585971]
[75]
Cervantes C, Campos-García J, Devars S, et al. Interactions of chromium with microorganisms and plants. FEMS Microbiol Rev 2001; 25(3): 335-47.
[http://dx.doi.org/10.1111/j.1574-6976.2001.tb00581.x] [PMID: 11348688]
[76]
Arora NK, Khare E, Singh S, Maheshwari DK. Effect of Al and heavy metals on enzymes of nitrogen metabolism of fast and slow growing rhizobia under explanta conditions. World J Microbiol Biotechnol 2010; (26): 811-6.
[http://dx.doi.org/10.1007/s11274-009-0237-6]
[77]
Kalita D, Joshi SR. Study on bioremediation of Lead by exopolysaccharide producing metallophilic bacterium isolated from extreme habitat. Biotechnol Rep (Amst) 2017; 16(16): 48-57.
[http://dx.doi.org/10.1016/j.btre.2017.11.003] [PMID: 29167759]
[78]
Wei L, Li Y, et al. Adsorption of Cu2+ and Zn2+ by extracellular polymeric substances (EPS) in different sludges: Effect of EPS fractional polarity on binding mechanism. Journ of Haza Mater 2016; 1(321): 473-83.
[79]
Lau TC, Wu XA, Chua H, Qian P-Y, Wong P. Effect of exopolysaccharides on the adsorption of metal ions by Pseudomonas sp. CU-1. Water Sci Technol 2004; 52(7): 63-8.
[http://dx.doi.org/10.2166/wst.2005.0182]
[80]
Sheng GP, Xu J, Luo HW, et al. Thermodynamic analysis on the binding of heavy metals onto extracellular polymeric substances (EPS) of activated sludge. Water Res 2013; 47(2): 607-14.
[http://dx.doi.org/10.1016/j.watres.2012.10.037] [PMID: 23159005]
[81]
Guibaud G, Bordas F, Saaid A, D’Abzac P, Van Hullebusch E. Effect of pH on cadmium and lead binding by extracellular polymeric substances (EPS) extracted from environmental bacterial strains. Colloids Surf B Bioin 2008; 1(63): 48-54.
[82]
Hernandez-Lucas I, Segovia L, Martinez-Romero E, Pueppke SG. Phylogenetic relationships and host range of Rhizobium spp. that nodulate Phaseolus vulgaris L. Appl Environ Microbiol 1995; 61(7): 2775-9.
[PMID: 7618891]
[83]
González-Guerrero M, Escudero V, Saéz Á, Tejada-Jiménez M. Saéz Ángela, Tejada-Jiménez M. Transition metal transport in plants and associated endosymbionts: arbuscular mycorrhizal fungi and rhizobia. Front Plant Sci 2016; 7(7): 1088.
[PMID: 27524990]
[84]
Deepika KV, Raghuram M, Kariali E, Bramhachar PV. Biological responses of symbiotic Rhizobium radiobacter strain VBCK1062 to the arsenic contaminated rhizosphere soils of mung bean. Ecotoxi Environ Safe 2016; 1(134): 1-10.
[http://dx.doi.org/10.1016/j.ecoenv.2016.08.008]
[85]
Wani PA, Khan MS, Zaidi A. Chromium-reducing and plant growth-promoting Mesorhizobium improves chickpea growth in chromium-amended soil. Biotechnol Lett 2008; 30(1): 159-63.
[http://dx.doi.org/10.1007/s10529-007-9515-2] [PMID: 17849087]
[86]
Hao X, Taghavi S, Xie P, et al. Phytoremediation of heavy and transition metals aided by legume-rhizobia symbiosis. Int J Phytoremediation 2014; 16(2): 179-202.
[http://dx.doi.org/10.1080/15226514.2013.773273] [PMID: 24912209]
[87]
Mohammad O, Mohammad SK, Huda AQ. Ensifer adhaerens for heavy metal bioaccumulation, biosorption, and phosphate solubilization under metal stress condition. Jour Taiwan Inst Chem E 2017; 80: 540-52.
[http://dx.doi.org/10.1016/j.jtice.2017.08.026]
[88]
Sheng GP, Yu HQ, Li XY. Extracellular polymeric substances (EPS) of microbial aggregates in biological wastewater treatment systems: a review. Biotechnol Adv 2010; 28(6): 882-94.
[http://dx.doi.org/10.1016/j.biotechadv.2010.08.001] [PMID: 20705128]
[89]
Uzoigwe C, Burgess JG, Ennis CJ, Rahman PKSM. Bioemulsifiers are not biosurfactants and require different screening approaches. Front Microbiol 2015; 6: 245.
[http://dx.doi.org/10.3389/fmicb.2015.00245] [PMID: 25904897]
[90]
Staehelin C, Forsberg LS, D’Haeze W, et al. Exo-oligosaccharides of Rhizobium sp. strain NGR234 are required for symbiosis with various legumes. J Bacteriol 2006; 188(17): 6168-78.
[http://dx.doi.org/10.1128/JB.00365-06] [PMID: 16923883]
[91]
Lopes EM, Castellane TCL, Moretto C, Lemos EGM, Souza JAM. Emulsification properties of bioemulsifiers produced by wild-type and mutant Bradyrhizobium elkanii strains. Jour of Biore Biod 2014; 05(06): 1-6.
[92]
Cooper DG, Goldenberg BG. Surface-active agents from two bacillus species. Appl Environ Microbiol 1987; 53(2): 224-9.
[PMID: 16347271]
[93]
Sofia GB, Djamel A. A rheological study of xanthan polymer for enhanced oil recovery. J Macromol Sci Part B Phys 2016; 55(8): 793-809.
[http://dx.doi.org/10.1080/00222348.2016.1207544]
[94]
Larson SL, Nijak G Jr, Griggs C, Talley J. Rhizobium tropici produced biopolymer salt WO Patent 2012078515A3. 2012.
[95]
García RM, Andrés FG, Lasala JB, García DM. A complex mineral fertilizer comprising the Rhizobium leguminosarum microorganism, production process and uses thereof EP Patent 3085679B1. 2018.
[96]
Lintner K. Composition for cosmetic or dermopharmaceutical use containing a combination of algae extract and exopolysaccharides WO Patent 1999013855A1. 1999.
[97]
Kavitake D, Delattre C, Devi PB, et al. Physical and functional characterization of succinoglycan exopolysaccharide produced by Rhizobium radiobacter CAS from curd sample. Int J Biol Macrom 2019; 1(134): 1013-21.
[http://dx.doi.org/10.1016/j.ijbiomac.2019.05.050]
[98]
Vieira IRS, Sales JS, Cerqueira-Coutinho CS, et al. Development and in vivo evaluation of the moisturising potential of cosmetic formulations containing Babassu (Orbignya phalerata Martius) oily extract. Jour Biom and Biopha Resea 2017; 14(2): 204-19.
[99]
Kim JW, Lee J, Yoo AY, Choi JW, Park Y. Immune-stimulating activity of water-soluble extracellular polysaccharide isolated from Rhizobium massiliae. Proce Bioch 2017; 1(63): 236-43.
[100]
Patel DM, Patel DK, Patel BK, Patel CN. An overview on intelligent drug delivery systems. Int J Adv Pharm Rev 2011; 1(2): 57-63.
[101]
Moscovici M. Present and future medical applications of microbial exopolysaccharides. Front Microbiol 2015; 6(6): 1012.
[http://dx.doi.org/10.3389/fmicb.2015.01012] [PMID: 26483763]


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Article Details

VOLUME: 3
ISSUE: 3
Year: 2019
Page: [157 - 166]
Pages: 10
DOI: 10.2174/2452271603666191016143811

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