Abstract
This study characterized the extruded polymeric substances (EPS) secreted from Synechococcus mundulus cultures under the effect of 2-KGy gamma irradiation dose. The EPS demonstrated seven monosaccharides, two uronic acids and several chemical functional groups: O–H, N–H, =C–H, C=C, C=O, COO–, O–SO3, C–O–C and a newly formed peak at 1593 cm−1 (secondary imide). The roughness of EPS was 96.71 nm and only 28.4% total loss in weight was observed at 800 °C with a high degree of crystallinity quantified as CIDSC (0.722) and CIXRD (0.718). Preliminary comparative analyses of EPS exhibited high protein content in the radiologically modified (R-EPS) than control (C-EPS). Modified EPS were characterized with a high biosorption efficiency, which could be attributed to its high content of uronic acids, protein and sulphates as well as various saccharide monomers. Data revealed that 0.0213 mg L−1 h−1 is the maximum biosorption rate (SBRmax) of Cr(VI) for R-EPS, whereas 0.0204 mg L−1 h−1 SBRmax for the C-EPS respectively.








Similar content being viewed by others
References
Abbas T, Rizwan M, Ali S, Adrees M, Mahmood A, Rehman MZ, Ibrahim M, Arshad M, Qayyum MF (2018) Biochar application increased the growth and yield and reduced cadmium in drought stressed wheat grown in an aged contaminated soil. Ecotoxicol Environ Saf 148:825–833
Ali S, Rizwan M, Noureen S, Anwar S, Ali B, Naveed M, Abd_Allah E, Alqarawi AA, Ahmad P (2019) Combined use of biochar and zinc oxide nanoparticle foliar spray improved the plant growth and decreased the cadmium accumulation in rice (Oryza sativa L.) plant. Environ Sci Pollut Res 26:11288–11299
Andersen RA (2005) Algal culturing techniques. Elsevier, Amsterdam p589
Association APH, Association AWW (1989) Standard methods for the examination of water and wastewater. American Public Health Association, Washington, D.C.
Bhunia B, Uday USP, Oinam G, Mondal A, Bandyopadhyay TK, Tiwari ON (2018) Characterization, genetic regulation and production of cyanobacterial exopolysaccharides and its applicability for heavy metal removal. Carbohydr Polym 179:228–243
Billi D, Friedmann EI, Hofer KG, Caiola MG, Ocampo-Friedmann R (2000) Ionizing-radiation resistance in the desiccation-tolerant cyanobacterium Chroococcidiopsis. Appl Environ Microbiol 66:1489–1492
Bryan R, Zaragoza O, Zhang T, Ortiz G, Casadevall A, Dadachova E (2005) Radiological studies reveal radial differences in the architecture of the polysaccharide capsule of Cryptococcus neoformans. Eukaryot Cell 4:465–475
Chen JP, Lin YS (2007) Decolorization of azo dye by immobilized Pseudomonas luteola entrapped in alginate–silicate sol–gel beads. Process Biochem 42:934–942
Chen M, Wu WW, Nanz D, Sticher O, Leonticins DH (1997) Five triterpene saponins from Leontice kiangnanensis. Phytochem 44:497–504
Chowdhury S, Manna S, Saha P, Basak R, Sen R, Roy D, Adhikari B (2011) Composition analysis and material characterization of an emulsifying extracellular polysaccharide (EPS) produced by Bacillus megaterium RB-05: a hydrodynamic sediment-attached isolate of freshwater origin. J Appl Microbiol 111:1381–1393
De Philippis R, Vincenzini M (1998) Exocellular polysaccharides from cyanobacteria and their possible applications. FEMS Microbiol Rev 22:151–175
Dean JA (1995) Analytical chemistry handbook. McGraw-Hill Companies, New York City
Dobrowolski R, Szcześ A, Czemierska M, Jarosz-Wikołazka A (2017) Studies of cadmium (II), lead (II), nickel (II), cobalt (II) and chromium (VI) sorption on extracellular polymeric substances produced by Rhodococcus opacus and Rhodococcus rhodochrous. Bioresour Technol 225:113–120
Dubois M, Gilles KA, Hamilton JK, Rebers PT, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Freitas F, Alves VD, Pais J, Costa N, Oliveira C, Mafra L, Hilliou L, Oliveira R, Reis MA (2009) Characterization of an extracellular polysaccharide produced by a Pseudomonas strain grown on glycerol. Bioresour Technol 100:859–865
Gómez-Ordóñez E, Rupérez P (2011) FTIR-ATR spectroscopy as a tool for polysaccharide identification in edible brown and red seaweeds. Food Hydrocoll 25:1514–1520
Gupta P, Diwan B (2017) Bacterial exopolysaccharide mediated heavy metal removal: a review on biosynthesis mechanism and remediation strategies. Biotechnol Rep 13:58–71
Han P, Guo RJ, Shen SG, Yan R, Wu YK, Yao SY, Wang HY, Jia SR (2018) Proteomic profiling of Nostoc flagelliforme reveals the common mechanism in promoting polysaccharide production by different light qualities. Biochem Eng J 132:68–78
Hussain A, Ali S, Rizwan M, Rehman MZ, Javed MR, Imran M, Chatha SA, Nazir R (2018) Zinc oxide nanoparticles alter the wheat physiological response and reduce the cadmium uptake by plants. Environ Pollut 242:1518–1526
Hussein M, Abou-ElWafa GS, Shaaban-Dessuuki SA, Hassan NI (2015) Characterization and antioxidant activity of exopolysaccharide secreted by Nostoc carneum. Int J Pharm 11:432–439
Insulkar P, Kerkar S, Lele S (2018) Purification and structural-functional characterization of an exopolysaccharide from Bacillus licheniformis PASS26 with in-vitro antitumor and wound healing activities. Int J Biol Macromol 120:1441–1450
Jodłowska S, Śliwińska S (2014) Effects of light intensity and temperature on the photosynthetic irradiance response curves and chlorophyll fluorescence in three picocyanobacterial strains of Synechococcus. Photosynthetica 52:223–232
Kavita K, Mishra A, Jha B (2011) Isolation and physico-chemical characterisation of extracellular polymeric substances produced by the marine bacterium Vibrio parahaemolyticus. Biofouling 27:309–317
Khalil U, Shakoor MB, Ali S, Rizwan M (2018) Tea waste as a potential biowaste for removal of hexavalent chromium from wastewater: equilibrium and kinetic studies. Arab J Geosci 11:1–11
Khanna Y, Kuhn W (1997) Measurement of crystalline index in nylons by DSC: complexities and recommendations. J Polym Sci B Polym Phys 35:2219–2231
Korotaeva N, Ivanova M, Suvorova G, Borovskii G (2018) The impact of the environmental factors on the photosynthetic activity of common pine (Pinus sylvestris) in spring and in autumn in the region of Eastern Siberia. J For Res 29:1465–1473
Kumar CG, Joo HS, Choi JW, Koo YM, Chang CS (2004) Purification and characterization of an extracellular polysaccharide from haloalkalophilic Bacillus sp. I-450. Enzym Microb Technol 34:673–681
Lan G, Hong X, Fan Q, Luo B, Shi P, Chen X (2014) Removal of hexavalent chromium in wastewater by polyacrylamide modified iron oxide nanoparticle. J Appl Polym Sci 131:40945–40955
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
Magdoub MIN, EL-Fouly M, Meleigy SA, Aita OA, Hendawy WS (2010) Enhancement productivity of lactic acid bacteria (LAB) to produced ex polysaccharide. 2nd International conference on radiation sciences and applications 28:3
Maurice PA, Pullin MJ, Cabaniss SE, Zhou Q, Namjesnik-Dejanovic K, Aiken GR (2002) A comparison of surface water natural organic matter in raw filtered water samples, XAD, and reverse osmosis isolates. Water Res 36:2357–2371
Mishra A, Kavita K, Jha B (2011) Characterization of extracellular polymeric substances produced by microalgae Dunaliella salina. Carbohydr Polym 83:852–857
Mota R, Guimarães R, Büttel Z, Rossi F, Colica G, Silva CJ et al (2013a) Production and characterization of extracellular carbohydrate polymer from Cyanothece sp. CCY 0110. Carbohydr Polym 92(2):1408–1415
Netzahuatl-Muñoz AR, del Carmen Cristiani-Urbina M, Cristiani-Urbina E (2015) Chromium biosorption from Cr (VI) aqueous solutions by Cupressus lusitanica bark: kinetics, equilibrium and thermodynamic studies. PLoS One 10(9):e0137086
Ozturk S, Aslim B (2010) Modification of exopolysaccharide composition and production by three cyanobacterial isolates under salt stress. Environ Sci Pollut Res 17:595–602
Ozturk S, Aslim B, Suludere Z (2009) Evaluation of chromium (VI) removal behaviour by two isolates of Synechocystis sp. in terms of exopolysaccharide (EPS) production and monomer composition. Bioresour Technol 100:5588–5559
Ozturk S, Aslim B, Suludere Z, Tan S (2014) Metal removal of cyanobacterial exopolysaccharides by uronic acid content and monosaccharide composition. Carbohydr Polym 101:265–271
Padmavathi AR, Periyasamy M, Pandian SK (2015) Assessment of 2, 4-di-tert-butylphenol induced modifications in extracellular polymeric substances of Serratia marcescens. Bioresour Technol 188:185–189
Parikh A, Madamwar D (2006) Partial characterization of extracellular polysaccharides from cyanobacteria. Bioresour Technol 97(15):1822–1827
Pereira Duta F, Pessôa de França F, de Almeida Lopes LM (2006) Optimization of culture conditions for exopolysaccharides production in Rhizobium sp. using the response surface method. Electron J Biotechnol 9
Pereira L, Sousa A, Coelho H, Amado AM, Ribeiro-Claro PJ (2003) Use of FTIR, FT-Raman and 13C-NMR spectroscopy for identification of some seaweed phycocolloids. Biomol Eng 20:223–228
Pereira S, Zille A, Micheletti E, Moradas-Ferreira P, De Philippis R, Tamagnini P (2009) Complexity of cyanobacterial exopolysaccharides: composition, structures, inducing factors and putative genes involved in their biosynthesis and assembly. FEMS Microbiol Rev 33:917–941
Rani RP, Anandharaj M, Ravindran AD (2018) Characterization of a novel exopolysaccharide produced by Lactobacillus gasseri FR4 and demonstration of its in vitro biological properties. Int J Biol Macromol 109:772–783
Reddy K, Soper B, Tang J, Bradley R (1996) Phenotypic variation in exopolysaccharide production in the marine, aerobic nitrogen-fixing unicellular cyanobacterium Cyanothece sp. World J Microbiol Biotechnol 12:311–318
Ricou P, Pinel E, Juhasz N (2005) Temperature experiments for improved accuracy in the calculation of polyamide-11 crystallinity by X-ray diffraction, Advances in X-ray Analysis, vol 48. International Centre for Diffraction Data, Newtown Square, pp 170–175
Richert L, Golubic S, Le Guédès R, Ratiskol J, Payri C, Guezennec J (2005) Characterization of exopolysaccharides produced by cyanobacteria isolated from Polynesian microbial mats. Curr Microbiol 51:379–384
Rizwan M, Ali S, Hussain A, Ali Q, Shakoor MB, Rehman MZ, Farid M, Asma M (2017) Effect of zinc-lysine on growth, yield and cadmium uptake in wheat (Triticum aestivum L.) and health risk assessment. Chemosphere 187:35–42
Rizwan M, Ali S, Rehman MZ, Rinklebe J, Tsang DC, Bashir A, Maqbool A, Tack FM, Ok YS (2018) Cadmium phytoremediation potential of Brassica crop species: a review. Sci Total Environ 631:1175–1191
Ruber J, Bauer FR, Millard AD, Raeder U, Geist J, Zwirglmaier K (2016) Synechococcus diversity along a trophic gradient in the Osterseen Lake District, Bavaria. Microbiol 162:2053–2063
Ruffing A, Jensen TJ, Strickland LM (2016) Ionizing radiation resistance in cyanobacteria (No. SAND2016-4406C). Sandia National Lab.(SNLNM), Albuquerque, NM (United States)
Sahmoune MN, Louhab K, Boukhiar A (2011) Advanced biosorbents materials for removal of chromium from water and wastewaters. Environ Prog Sustain Energy 30:284–293
Saravanan C, Shetty PKH (2016) Isolation and characterization of exopolysaccharide from Leuconostoc lactis KC117496 isolated from idli batter. Int J Biol Macromol 90:100–106
Sardar UR, Bhargavi E, Devi I, Bhunia B, Tiwari ON (2018) Advances in exopolysaccharides based bioremediation of heavy metals in soil and water: a critical review. Carbohydr Polym 199:353–364
Sardari RR, Kulcinskaja E, Ron EY, Björnsdóttir S, Friðjónsson ÓH, Hreggviðsson GÓ, Karlsson EN (2017) Evaluation of the production of exopolysaccharides by two strains of the thermophilic bacterium Rhodothermus marinus. Carbohydr Polym 156:1–8
Sasaki H, Shirato S, Tahara T, Sato K, Takenaka H (2013) Accumulation of radioactive cesium released from Fukushima Daiichi Nuclear Power Plant in terrestrial cyanobacteria Nostoc commune. Microbes Environ 28:466–469
Sattar MS, Shakoor MB, Ali S, Rizwan M, Niazi NK, Jilani A (2019) Comparative efficiency of peanut shell and peanut shell biochar for removal of arsenic from water. Environ Sci Pollut Res 26:18624–18635. https://doi.org/10.1007/s11356-019-05185-z
Schopf JW (2000) The fossil record: tracing the roots of the cyanobacterial lineage. In: The ecology of cyanobacteria. Springer, Berlin, pp 13–35
Shen L, Li Z, Wang J, Liu A, Li Z, Yu R, Wu X, Liu Y, Li J, Zeng W (2018) Characterization of extracellular polysaccharide/protein contents during the adsorption of Cd (II) by Synechocystis sp. PCC6803. Environ Sci Pollut Res:1–10
Shevchenko T (1999) Accumulation of radionuclides by communities of Periphytic algae in the cooling pond of the Chernobyl NPP (8 years after the accident). Hydrobiol J 35(2):117–130
Shokier H, EI-Adly A, Hussein H, Shabon M, EI-Shanshoury I (2010) Effect of gamma rays on antibiotic resistance of Staphylococcus aureus and Pseudomonas aeruginosa isolated from human skin. J Radiat Res Appl Sci 3:1687–1507
Shuhong Y, Meiping Z, Hong Y, Han W, Shan X, Yan L, Jihui W (2014) Biosorption of Cu2+, Pb2+ and Cr6+ by a novel exopolysaccharide from Arthrobacter ps-5. Carbohydr Polym 101:50–56
Shuryak I (2019) Review of microbial resistance to chronic ionizing radiation exposure under environmental conditions. J Environ Radioact 196:50–63
Singh OV, Gabani P (2011) Extremophiles: radiation resistance microbial reserves and therapeutic implications. J Appl Microbiol 110:851–861
Singh H, Fernandes T, Apte SK (2010) Unusual radioresistance of nitrogen-fixing cultures of Anabaena strains. J Biosci 35:427–434
Singh RP, Shukla MK, Mishra A, Kumari P, Reddy C, Jha B (2011) Isolation and characterization of exopolysaccharides from seaweed associated bacteria Bacillus licheniformis. Carbohydr Polym 84:1019–1026
Sinha RP, Häder DP (2006) UV-protectants in cyanobacteria. Plant Sci 174(2008):278–289
Skuja H (1964) Grundzüge der Algenflora und Algenvegetation der Fjeldgegenden um Abisko in Schwedish-Lappland. Nova Acta Regiae Societas Scientarum Upsaliensis 18:465
Stanier R, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev 35:171
Stuart BH (2004) Infrared spectroscopy: fundamentals and applications. Wiley, Hoboken
Su X, Wang Y, Xue B, Hashmi MZ, Lin H, Chen J, Wang Z, Mei R, Sun F (2019) Impact of resuscitation promoting factor (Rpf) in membrane bioreactor treating high-saline phenolic wastewater: performance robustness and Rpf-responsive bacterial populations. Chem Eng J 357:715–723
Tahir U, Yasmin A (2019) Role of bacterial extracellular polymeric substances (EPS) in uptake and accumulation of co-contaminants. Int J Environ Sci Technol:1–12
Trabelsi L, M’sakni NH, Ouada HB, Bacha H, Roudesli S (2009) Partial characterization of extracellular polysaccharides produced by cyanobacterium Arthrospira platensis. Biotechnol Bioprocess Eng 14:27–31
Wang K, Li W, Rui X, Chen X, Jiang M, Dong M (2014) Characterization of a novel exopolysaccharide with antitumor activity from Lactobacillus plantarum 70810. Int J Biol Macromol 63:133–139
Wei L, Li Y, Noguera DR, Zhao N, Song Y, Ding J, Zhao Q, Cui F (2017) Adsorption of Cu2+ and Zn2+ by extracellular polymeric substances (EPS) in different sludges: Effect of EPS fractional polarity on binding mechanism. J Hazard Mater 321:473–483
Whitton BA (2012) Ecology of cyanobacteria II: their diversity in space and time. Springer Science & Business Media, Berlin
Yun U, Park H (2003) Physical properties of an extracellular polysaccharide produced by Bacillus sp. CP912. Lett Appl Microbiol 36:282–287
Zeng J, Gao JM, Chen YP, Yan P, Dong Y, Shen Y et al (2016) Composition and aggregation of extracellular polymeric substances (EPS) in hyperhaline and municipal wastewater treatment plants. Sci Rep 6:1–14
Zhang H, Tang Y, Cai D, Liu X, Wang X, Huang Q, Yu Z (2010) Hexavalent chromium removal from aqueous solution by algal bloom residue derived activated carbon: equilibrium and kinetic studies. J Hazard Mater 181(1-3):801–808
Zhang J, Cao Y, Wang J, Guo X, Zheng Y, Zhao W, Mei X, Guo T, Yang Z (2016) Physicochemical characteristics and bioactivities of the exopolysaccharide and its sulphated polymer from Streptococcus thermophilus GST-6. Carbohydr Polym 146:368–375
Zhao M, Yang N, Yang B, Jiang Y, Zhang G (2007) Structural characterization of water-soluble polysaccharides from Opuntia monacantha cladodes in relation to their anti-glycated activities. Food Chem 105:1480–1486
Funding
This study was supported by the Genetic Engineering and Biotechnology Research Institute, University of Sadat City, Sadat City, Egypt
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Tito Roberto Cadaval Jr
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Hussein, M.H., Hamouda, R.A., Elhadary, A.M.A. et al. Characterization and chromium biosorption potential of extruded polymeric substances from Synechococcus mundulus induced by acute dose of gamma irradiation. Environ Sci Pollut Res 26, 31998–32012 (2019). https://doi.org/10.1007/s11356-019-06202-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-019-06202-x


