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Applied Microbiology and Biotechnology

, Volume 100, Issue 17, pp 7765–7775 | Cite as

Released polysaccharides (RPS) from Cyanothece sp. CCY 0110 as biosorbent for heavy metals bioremediation: interactions between metals and RPS binding sites

  • Rita Mota
  • Federico Rossi
  • Luisa Andrenelli
  • Sara Bernardes Pereira
  • Roberto De Philippis
  • Paula Tamagnini
Environmental biotechnology

Abstract

Bioremediation of heavy metals using microorganisms can be advantageous compared to conventional physicochemical methods due to the use of renewable resources and efficiencies of removal particularly cations at low concentrations. In this context, cyanobacteria/cyanobacterial extracellular polymeric substances (EPS) emerge as a valid alternative due to the anionic nature and particular composition of these polymers. In this work, various culture fractions of the unicellular cyanobacterium Cyanothece sp. CCY 0110 were employed in bioremoval assays using three of the most common heavy metal pollutants in water bodies—copper, cadmium, and lead—separately or in combined systems. Our study showed that the released polysaccharides (RPS) were the most efficient fraction, removing the metal(s) by biosorption. Therefore, this polymer was subsequently used to evaluate the interactions between the metals/RPS binding sites using SEM-EDX, ICP-OES, and FTIR. Acid and basic pretreatments applied to the polymer further improve the process efficiency, and the exposure to an alkaline solution seems to alter the RPS conformation. The differences observed in the specific metal bioremoval seem to be mainly due to the RPS organic functional groups available, mainly carboxyl and hydroxyl, than to an ion exchange mechanism. Considering that Cyanothece is a highly efficient RPS-producer and that RPS can be easily separated from the culture, immobilized or confined, this polymer can be advantageous for the establishment/improvement of heavy metal removal systems.

Keywords

Bioremediation Cyanobacteria Cyanothece Extracellular polymeric substances (EPS) Heavy metals Released polysaccharides (RPS) 

Notes

Acknowledgments

We thank Daniela Silva from Centro de Materiais da Universidade do Porto (CEMUP), Porto, Portugal, for technical assistance with SEM-EDX. We also thank Ricardo Silva from INEB—Instituto de Engenharia Biomédica, Universidade do Porto, Porto, Portugal, for technical assistance with FTIR. The financial support was by national funds through FCT—Fundação para a Ciência e a Tecnologia/MEC—Ministério da Educação e Ciência and when applicable co-funded by FEDER funds within the partnership agreement PT2020 related with the research unit number 4293, by the project FCOMP-01-0124-FEDER-028314 (PTDC/BIA-MIC/2889/2012) and by the scholarships SFRH/BD/84914/2012 and SFRH/BDP/72400/2010.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Anjana K, Kaushik K, Kiran B, Nisha R (2007) Biosorption of Cr(VI) by immobilized biomass of two indigenous strains of cyanobacteria isolated from metal contaminated soil. J Hazard Mater 148:383–386. doi: 10.1016/j.jhazmat.2007.02.051 CrossRefPubMedGoogle Scholar
  2. Azizi SN, Colagar AH, Hafeziyan SM (2012) Removal of Cd(II) from aquatic system using Oscillatoria sp. biosorbent. Sci World J 2012:1–7. doi: 10.1100/2012/347053 Google Scholar
  3. Cavet JS, Borrelly GP, Robinson NJ (2003) Zn, Cu and Co in cyanobacteria: selective control of metal availability. FEMS Microbiol Rev 27:165–181. doi: 10.1016/S0168-6445(03)00050-0 CrossRefPubMedGoogle Scholar
  4. Chojnacka K (2010) Biosorption and bioaccumulation—the prospects for practical applications. Environ Int 36:299–307. doi: 10.1016/j.envint.2009.12.001 CrossRefPubMedGoogle Scholar
  5. Chojnacka K, Chojnacki A, Gorecka H (2005) Biosorption of Cr3+, Cd2+ and Cu2+ ions by blue-green algae Spirulina sp.: kinetics, equilibrium and the mechanism of the process. Chemosphere 59:75–84. doi: 10.1016/j.chemosphere.2004.10.005 CrossRefPubMedGoogle Scholar
  6. Comte S, Guibaud G, Baudu M (2006) Relations between extraction protocols for activated sludge extracellular polymeric substances (EPS) and EPS complexation properties. Part I. Comparison of the efficiency of eight EPS extraction methods. Enzym Microb Technol 38:237–245. doi: 10.1016/j.enzmictec.2005.06.016 CrossRefGoogle Scholar
  7. De Philippis R, Colica G, Micheletti E (2011) Exopolysaccharide-producing cyanobacteria in heavy metal removal from water: molecular basis and practical applicability of the biosorption process. Appl Microbiol Biotechnol 92:697–708. doi: 10.1007/s00253-011-3601-z CrossRefPubMedGoogle Scholar
  8. De Philippis R, Micheletti E (2009) Heavy metal removal with exopolysaccharide-producing cyanobacteria. In: Wang LK, Chen JP, Hung YT, Shammas NK (eds) Heavy metals in the environment. CRC Press, Boca Raton, pp. 89–122Google Scholar
  9. De Philippis R, Paperi R, Sili C (2007) Heavy metal sorption by released polysaccharides and whole cultures of two exopolysaccharide-producing cyanobacteria. Biodegradation 18:181–187. doi: 10.1007/s10532-006-9053-y CrossRefPubMedGoogle Scholar
  10. Dmytryk A, Saeid A, Chojnacka K (2014) Biosorption of microelements by Spirulina: towards technology of mineral feed supplements. Sci World J 2014:1–15. doi: 10.1155/2014/356328 CrossRefGoogle Scholar
  11. 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. doi: 10.1021/ac60111a017 CrossRefGoogle Scholar
  12. Fourest E, Volesky B (1997) Alginate properties and heavy metal biosorption by marine algae. Appl Biochem Biotechnol 67:215–226CrossRefGoogle Scholar
  13. Guo J, Zheng XD, Chen QB, Zhang L, Xu XP (2012) Biosorption of Cd(II) from aqueous solution by Pseudomonas plecoglossicida: kinetics and mechanism. Curr Microbiol 65:350–355. doi: 10.1007/s00284-012-0164-x CrossRefPubMedGoogle Scholar
  14. Huang C, Chung Y, Liou M (1996) Adsorption of Cu(II) and Ni(II) by pelletized biopolymer. J Hazard Mater 45:265–277CrossRefGoogle Scholar
  15. Jarup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182. doi: 10.1093/bmb/ldg032 CrossRefPubMedGoogle Scholar
  16. Kapoor A, Viraraghavan T (1997) Heavy metal biosorption sites in Aspergillus niger. Bioresour Technol 61:221–227CrossRefGoogle Scholar
  17. Lesmana SO, Febriana N, Soetaredjo FE, Sunarso J, Ismadji S (2009) Studies on potential applications of biomass for the separation of heavy metals from water and wastewater. Biochem Eng J 44:19–41. doi: 10.1016/j.bej.2008.12.009 CrossRefGoogle Scholar
  18. Lopéz-Maury L, Giner-Lamia J, Florencio FJ (2012) Redox control of copper homeostasis in cyanobacteria. Plant Signal Behav 7:1712–1714. doi: 10.4161/psb.22323 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Michalak I, Chojnacka K, Marycz K (2011) Using ICP-OES and SEM-EDX in biosorption studies. Mikrochim Acta 172:65–74. doi: 10.1007/s00604-010-0468-0 CrossRefPubMedGoogle Scholar
  20. Micheletti E, Colica G, Viti C, Tamagnini P, De Philippis R (2008a) Selectivity in the heavy metal removal by exopolysaccharide-producing cyanobacteria. J Appl Microbiol 105:88–94. doi: 10.1111/j.1365-2672.2008.03728.x CrossRefPubMedGoogle Scholar
  21. Micheletti E, Pereira S, Mannelli F, Moradas-Ferreira P, Tamagnini P, De Philippis R (2008b) Sheathless mutant of cyanobacterium Gloeothece sp. strain PCC 6909 with increased capacity to remove copper ions from aqueous solutions. Appl Environ Microbiol 74:2797–2804. doi: 10.1128/AEM.02212-07 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Mota R, Guimaraes R, Buttel Z, Rossi F, Colica G, Silva CJ, Santos C, Gales L, Zille A, De Philippis R, Pereira SB, Tamagnini P (2013) Production and characterization of extracellular carbohydrate polymer from Cyanothece sp. CCY 0110. Carbohydr Polym 92:1408–1415. doi: 10.1016/j.carbpol.2012.10.070 CrossRefPubMedGoogle Scholar
  23. Mota R, Pereira SB, Meazzini M, Fernandes R, Santos A, Evans CA, De Philippis R, Wright PC, Tamagnini P (2015) Effects of heavy metals on Cyanothece sp. CCY 0110 growth, extracellular polymeric substances (EPS) production, ultrastructure and protein profiles. J Proteome 120:75–94. doi: 10.1016/j.jprot.2015.03.004 CrossRefGoogle Scholar
  24. Nagase H, Inthorn D, Oda A, Nishimura J, Kajiwara Y, Park MO, Hirata K, Miyamoto K (2005) Improvement of selective removal of heavy metals in cyanobacteria by NaOH treatment. J Biosci Bioeng 99:372–377. doi: 10.1263/jbb.99.372 CrossRefPubMedGoogle Scholar
  25. Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339. doi: 10.1016/S0168-6445(03)00048-2 CrossRefPubMedGoogle Scholar
  26. 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. doi: 10.1016/j.carbpol.2013.09.040 CrossRefPubMedGoogle Scholar
  27. Paperi R, Micheletti E, De Philippis R (2006) Optimization of copper sorbing-desorbing cycles with confined cultures of the exopolysaccharide-producing cyanobacterium Cyanospira capsulata. J Appl Microbiol 101:1351–1356. doi: 10.1111/j.1365-2672.2006.03021.x CrossRefPubMedGoogle Scholar
  28. Parker DL, Mihalick JE, Plude JL, Plude MJ, Clark TP, Egan L, Flom JJ, Rai LC, Kumar HD (2000) Sorption of metals by extracellular polymers from the cyanobacterium Microcystis aeruginosa f.flos-aquae strain C3-40. J Appl Phycol 12:219–224CrossRefGoogle Scholar
  29. Pereira S, Micheletti E, Zille A, Santos A, Moradas-Ferreira P, Tamagnini P, De Philippis R (2011) Using extracellular polymeric substances (EPS)-producing cyanobacteria for the bioremediation of heavy metals: do cations compete for the EPS functional groups and also accumulate inside the cell? Microbiology 157:451–458. doi: 10.1099/mic.0.041038-0 CrossRefPubMedGoogle Scholar
  30. 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. doi: 10.1111/j.1574-6976.2009.00183.x CrossRefPubMedGoogle Scholar
  31. Rao MM, Ramesh A, Rao GP, Seshaiah K (2006) Removal of copper and cadmium from the aqueous solutions by activated carbon derived from Ceiba pentandra hulls. J Hazard Mater 129:123–129. doi: 10.1016/j.jhazmat.2005.08.018 CrossRefPubMedGoogle Scholar
  32. Rao MM, Rao GP, Seshaiah K, Choudary NV, Wang MC (2008) Activated carbon from Ceiba pentandra hulls, an agricultural waste, as an adsorbent in the removal of lead and zinc from aqueous solutions. Waste Manag 28:849–858. doi: 10.1016/j.wasman.2007.01.017 CrossRefPubMedGoogle Scholar
  33. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61. doi: 10.1099/00221287-111-1-1 Google Scholar
  34. Sampedro MA, Blanco A, Llama MJ, Serra JL (1995) Sorption of heavy metals to Phormidium laminosum biomass. Biotechnol Appl Biochem 22:355–366Google Scholar
  35. Schiewer S (1999) Modelling complexation and electrostatic attraction in heavy metal biosorption by Sargassum biomass. J Appl Phycol 11:79–87CrossRefGoogle Scholar
  36. Schiewer S, Volesky B (1995) Modeling of the proton-metal ion exchange in biosorption. Environ Sci Technol 29:3049–3058. doi: 10.1021/es00012a024 CrossRefPubMedGoogle Scholar
  37. Schiewer S, Volesky B (1997) Ionic strength and electrostatic effects in biosorption of divalent metal ions and protons. Environ Sci Technol 31:2478–2485CrossRefGoogle Scholar
  38. Stuart B (2004) Infrared spectroscopy: fundamentals and applications. Analytical techniques in the sciences. John Wiley & Sons, Ltd, Chichester, U.K.CrossRefGoogle Scholar
  39. Sulaymon AH, Mohammed AA, Al-Musawi TJ (2013) Competitive biosorption of lead, cadmium, copper, and arsenic ions using algae. Environ Sci Pollut Res Int 20:3011–3023. doi: 10.1007/s11356-012-1208-2 CrossRefPubMedGoogle Scholar
  40. Tien CJ (2002) Biosorption of metal ions by freshwater algae with different surface characteristics. Process Biochem 38:605–613CrossRefGoogle Scholar
  41. Volesky B (2001) Detoxification of metal-bearing effluents: biosorption for the next century. Hydrometallurgy 59:203–216. doi: 10.1016/S0304-386x(00)00160-2 CrossRefGoogle Scholar
  42. Volesky B, Holan ZR (1995) Biosorption of heavy-metals. Biotechnol Prog 11:235–250. doi: 10.1021/Bp00033a001 CrossRefPubMedGoogle Scholar
  43. Volesky B, May-Phillips HA (1995) Biosorption of heavy metals by Saccharomyces cerevisiae. Appl Microbiol Biotechnol 42:797–806CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Rita Mota
    • 1
    • 2
    • 3
  • Federico Rossi
    • 4
  • Luisa Andrenelli
    • 4
  • Sara Bernardes Pereira
    • 1
  • Roberto De Philippis
    • 4
    • 5
  • Paula Tamagnini
    • 1
    • 2
    • 3
  1. 1.i3S—Instituto de Investigação e Inovação em SaúdeUniversidade do PortoPortoPortugal
  2. 2.IBMC—Instituto de Biologia Molecular e CelularUniversidade do PortoPortoPortugal
  3. 3.Faculdade de Ciências, Departamento de BiologiaUniversidade do PortoPortoPortugal
  4. 4.Department of Agrifood Production and Environmental SciencesUniversity of FlorenceFlorenceItaly
  5. 5.Institute of Ecosystem Study (ISE)National Research Council (CNR)Sesto FiorentinoItaly

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