Abstract
Cyanobacteria have been proven to be cheaper and more effective for the removal of metallic elements in aqueous solutions. In this study, the living cyanobacteria Synechocystis sp. PCC6803 was used to adsorb Cd(II) and its extracellular polymeric substances (EPS) were investigated in the adsorption process. The initial stage of adsorption of Cd(II) was a rapid process, and then increase slowly accompanied with the increases of biomass. The final adsorption percentage could achieve 86% when the Cd(II) concentration was 0.5 mg/L. It proved that Synechocystis sp. PCC6803 has a good adsorption capacity for heavy metal ions. EPS was extracted to investigate the secretion of which was dynamic and the maximum extracellular polysaccharides and proteins were 134.2 and 100.9 mg/g, respectively. Furthermore, the real-time PCR (RT-PCR) results of genes (slr0977 and exoD) involved in EPS synthesis and secretion indicated that the EPS production was firstly increased and then decreased slightly. Transmission electron microscope (TEM) observation revealed that heavy metal ions were absorbed into EPS layer. Fourier transform infrared spectrum (FT-IR) analysis showed that EPS was rich in functional groups which could combine with heavy metal ions, such as –OH and –NH groups. All the results obtained show that the secretion of EPS by cyanobacteria was one of the ways to resist heavy metal stress. And it shows a trend of rising first and then decreasing, the change regulation of which was consistent with adsorptive behavior.
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References
Bakatula EN, Cukrowska EM, Weiersbye IM, Mihaly-Cozmuta L, Peter A, Tutu H (2014) Biosorption of trace elements from aqueous systems in gold mining sites by the filamentous green algae (Oedogonium sp.). J Geochem Explor 144:492–503. https://doi.org/10.1016/j.gexplo
Blasi B, Peca L, Vass I, Kós PB (2012) Characterization of stress responses of heavy metal and metalloid inducible promoters in Synechocystis PCC6803. J Microbiol Biotechnol 22:166–169. https://doi.org/10.4014/jmb.1106.06050
Cammarota MC, Jr GLS (1998) Metabolic blocking of exopolysaccharides synthesis: effects on microbial adhesion and biofilm accumulation. Biotechnol Lett 20:1–4. https://doi.org/10.1023/A:1005394325549
Castielli O, Cerda BDL, Navarro JA, Hervás M, Rosa MADL (2009) Proteomic analyses of the response of cyanobacteria to different stress conditions. FEBS Lett 583:1753–1758. https://doi.org/10.1016/j.febslet.2009.03.069
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Fisher ML, Allen R, Luo Y, Roy Curtiss I (2013) Export of extracellular polysaccharides modulates adherence of the Cyanobacterium Synechocystis. PLoS One 8:e74514. https://doi.org/10.1371/journal.pone.0074514
Gavrilescu M, Chisti Y (2005) Biotechnology—a sustainable alternative for chemical industry. Biotechnol Adv 23:471–499. https://doi.org/10.1016/j.biotechadv.2005.03.004
General C (2006) Test no. 201: freshwater alga and cyanobacteria, growth inhibition test. Oecd Guidel Test Chem 1:1–1. https://doi.org/10.1787/9789264069923-en
Higgins CF (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67–113. https://doi.org/10.1146/annurev.cb.08.110192.000435
Hou J, Yang Y, Wang P, Wang C, Miao L, Wang X, Lv B, You G, Liu Z (2016) Effects of CeO2, CuO, and ZnO nanoparticles on physiological features of Microcystis aeruginosa and the production and composition of extracellular polymeric substances. Environ Sci Poll Res Int 24:1–10. https://doi.org/10.1007/s11356-016-7387-5
Ikeuchi M, Tabata S (2001) Synechocystis sp. PCC 6803—a useful tool in the study of the genetics of cyanobacteria. Photosynth Res 70:73–83. https://doi.org/10.1023/A:1013887908680
Islam ST, Lam JS (2014) Synthesis of bacterial polysaccharides via the Wzx/Wzy-dependent pathway. Can J Microbiol 60:697–716. https://doi.org/10.1139/cjm-2014-0595
Jittawuttipoka T, Planchon M, Spalla O, Benzerara K, Guyot F, Cassierchauvat C, Chauvat F (2013) Multidisciplinary evidences that Synechocystis PCC6803 exopolysaccharides operate in cell sedimentation and protection against salt and metal stresses. PLoS One 8:e55564. https://doi.org/10.1371/journal.pone.0055564
Kanmani P, Satish KR, Yuvaraj N, Paari KA, Pattukumar V, Arul V (2011) Production and purification of a novel exopolysaccharide from lactic acid bacterium Streptococcus phocae PI80 and its functional characteristics activity in vitro. Bioresour Technol 102:4827–4833. https://doi.org/10.1016/j.biortech.2010.12.118
Ke GZ, Peng SP, Xu T, Li H, Zhu L (2017) Research progress on remediation technology on soil heavy metal of cadmium in soil. Guangzhou Chem Ind 45:28–31 (in Chinese). https://doi.org/10.3969/j.issn.1001-9677.2017.14.011
Latifi A, Ruiz M, Zhang CC (2009) Oxidative stress in cyanobacteria. FEMS Microbiol Rev 33:258–278. https://doi.org/10.1111/j.1574-6976.2008.00134
Mezhoud N, Zili F, Bouzidi N, Helaoui F, Ammar J, Ouada HB (2014) The effects of temperature and light intensity on growth, reproduction and EPS synthesis of a thermophilic strain related to the genus Graesiella. Bioprocess Biosyst Eng 37:2271–2280. https://doi.org/10.1007/s00449-014-1204-7
More TT, Yadav JS, Yan S, Tyagi RD, Surampalli RY (2014) EPS of bacteria and their potential environmental applications. J Environ Manag 144:1–25. https://doi.org/10.1016/j.jenvman.2014.05.010
Morillo Pérez JA, Garcíaribera R, Quesada T, Aguilera M, Ramoscormenzana A, Monteolivasánchez M (2008) Biosorption of heavy metals by the exopolysaccharide produced by Paenibacillus jamilae. World J Microb Biot 24:2699–2704. https://doi.org/10.1007/s11274-008-9800-9
Mota R, Pereira SB, Meazzini M, Rui F, Santos A, Evans CA, Philippis RD, Wright PC, Tamagnini P (2015) Effects of heavy metals on Cyanothece sp. CCY 0110 growth, EPS (EPS) production, ultrastructure and protein profiles. J Proteome 120:75–94. https://doi.org/10.1016/j.jprot.2015.03.004
Ozturk S, Aslim B, Suludere Z (2010) Cadmium(II) sequestration characteristics by two isolates of Synechocystis sp. in terms of exopolysaccharide (EPS) production and monomer composition. Bioresour Technol 101:9742–9748. https://doi.org/10.1016/j.biortech.2010.07.105
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. https://doi.org/10.1016/j.carbpol.2013.09.040
Pereira S, Zille A, Micheletti E, Moradasferreira 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. https://doi.org/10.1111/j.1574-6976.2009.00183.x
Pereira SB, Mota R, Santos CL, Philippis RD, Tamagnini P (2013) Chapter seven-assembly and export of EPS (EPS) in cyanobacteria: a phylogenomic approach. Adv Bot Res 65:235–279. https://doi.org/10.1016/B978-0-12-394313-2.00007-X
Pereira SB, Mota R, Vieira CP, Vieira J, Tamagnini P (2015) Phylum-wide analysis of genes/proteins related to the last stEPS of assembly and export of EPS (EPS) in cyanobacteria. Sci Rep-UK 5:14835. https://doi.org/10.1038/srep14835
Pradhan S, Singh S, Rai LC (2007) Characterization of various functional groups present in the capsule of Microcystis and study of their role in biosorption of Fe, Ni and Cr. Bioresource Technol 98:595–601. https://doi.org/10.1016/j.biortech.2006.02.041
Sathishkumar M, Pavagadhi S, Vijayaraghavan K, Balasubramanian R, Ong SL (2010) Experimental studies on removal of microcystin-LR by peat. J Hazard Mater 184:417–424. https://doi.org/10.1016/j.jhazmat.2010.08.051
Sharma M, Somvir KA, Bala K, Kamra A (2008) Sequestration of chromium by exopolysaccharides of Nostoc and Gloeocapsa from dilute aqueous solutions. J Hazard Mater 157:315–318. https://doi.org/10.1016/j.jhazmat.2007.12.100
Shen L, Xia J, He H, Nie Z, Qiu G (2007) Biosorption mechanism of Cr(VI) onto cells of Synechococcus sp. J Cent South Univ 14:157–162. https://doi.org/10.1007/s11771-007-0032-1
Singh S, Pradhan S, Rai LC (2000) Metal removal from single and multimetallic systems by different biosorbent materials as evaluated by differential pulse anodic stripping voltammetry. Process Biochem 36:175–182. https://doi.org/10.1016/S0032-9592(00)00211-9
Singh S, Mishra AK (2014) Regulation of calcium ion and its effect on growth and developmental behavior in wild type and ntcA mutant of Anabaena sp. PCC 7120 under varied levels of CaCl2. Microbiology 83:235–246. https://doi.org/10.1134/S002626171403014X
Singh S, Niveshika VE, Tiwari B, Mishra AK (2016) Exopolysaccharide production in Anabaena sp. PCC 7120 under different CaCl2 regimes. Physiol Mol Biol Plants 22:557–566. https://doi.org/10.1007/s12298-016-0380-0
Srivastava S, Vishwakarma RK, Arafat YA, Gupta SK, Khan BM (2015) Abiotic stress induces change in Cinnamoyl CoA Reductase (CCR) protein abundance and lignin deposition in developing seedlings of Leucaena leucocephala. Physiol Mol Biol Plants Int J Function Plant Biol 21:197. https://doi.org/10.1007/s12298-015-0289-z
Vanguilder HD, Vrana KE, Freeman WM (2008) Twenty-five years of quantitative PCR for gene expression analysis. BioTechniques 44:619–626. https://doi.org/10.2144/000112776
Whitney JC, Howell PL (2013) Synthase-dependent exopolysaccharide secretion in Gram-negative bacteria. Trends Microbiol 21:63–72. https://doi.org/10.1016/j.tim.2012.10.001
Willis LM, Whitfield C (2013) Structure, biosynthesis, and function of bacterial capsular polysaccharides synthesized by ABC transporter-dependent pathways. Carbohydr Res 378:35–44. https://doi.org/10.1016/j.carres.2013.05.007
Wingender J, Neu TR, Flemming HC (1999) Microbial EPS. Springer, Berlin Heidelberg, pp 45–53
Xu H, Cai H, Yu G, Jiang H (2013) Insights into EPS of cyanobacterium Microcystis aeruginosa using fractionation procedure and parallel factor analysis. Water Res 47:2005–2014. https://doi.org/10.1016/j.watres.2013.01.019
Yan C, Ding H (2008) Effect of cadmium on the growth of Synechocystis PCC 6803. J South-Central Univ Nat (Natural Science Edition) 27:34–36 (in Chinese). https://doi.org/10.3969/j.issn.1672-4321.2008.04.010
Yu R, Hou C, Liu A, Peng T, Xia M, Wu X, Shen L, Liu Y, Li J, Yang F (2018) Extracellular DNA enhances the adsorption of Sulfobacillus thermosulfidooxidans strain ST on chalcopyrite surface. Hydrometallurgy 176:97–103. https://doi.org/10.1016/j.hydromet.2018.01.018
Zhang HO, Zhou WZ, Ma YH, Zhao HX, Zhang YZ (2013) FTIR spectrum and detoxication of EPS secreted by microorganism. Guang pu xue yu guang pu fen xi = Guang pu 33:3041 (in Chinese). https://doi.org/10.3964/j.issn.1000-0593(2013)11-3041-03
Zheng L, Ding AZ, Wang JS, Tian Y, Sun DZ (2008) Adsorption characteristics of Cd2+ and Zn2+ by EPS with varied constituents from activated sludge. Environ Sci 29:2850 (in Chinese). https://doi.org/10.3321/j.issn:0250-3301.2008.10.029
Zhou K, Yi H, Zhang L, Yang K, Lin D (2016) The role of exopolymeric substances in the bioaccumulation and toxicity of Ag nanoparticles to algae. ScI Rep-UK 6:32998. https://doi.org/10.1038/srep32998
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This work was supported by the National Natural Science Foundation of China (No. 51604308, 31470230, 51320105006) and the Natural Science Foundation of Hunan Province (No. 2018JJ2486).
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Shen, L., Li, Z., Wang, J. et al. Characterization of extracellular polysaccharide/protein contents during the adsorption of Cd(II) by Synechocystis sp. PCC6803. Environ Sci Pollut Res 25, 20713–20722 (2018). https://doi.org/10.1007/s11356-018-2163-3
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DOI: https://doi.org/10.1007/s11356-018-2163-3