Skip to main content
SpringerLink
Log in
Book cover

Transgenic Microalgae as Green Cell Factories pp 99–109Cite as

Phycoremediation of Heavy Metals Using Transgenic Microalgae

  • Chapter

Part of the book series: Advances in Experimental Medicine and Biology ((volume 616))

Abstract

Microalgae account for most of the biologically sequestered trace metals in aquatic environments. Their ability to adsorb and metabolize trace metals is associated with their large surface:volume ratios, the presence of high-affinity, metal-binding groups on their cell surfaces, and efficient metal uptake and storage systems. Microalgae may bind up to 10% of their biomass as metals. In addition to essential trace metals required for metabolism, microalgae can efficiently sequester toxic heavy metals. Toxic heavy metals often compete with essential trace metals for binding to and uptake into cells. Recently, transgenic approaches have been developed to further enhance the heavy metal specificity and binding capacity of microalgae with the objective of using these microalgae for the treatment of heavy metal contaminated wastewaters and sediments. These transgenic strategies have included the over expression of enzymes whose metabolic products ameliorate the effects of heavy metal-induced stress, and the expression of high-affinity, heavy metal binding proteins on the surface and in the cytoplasm of transgenic cells. The most effective strategies have substantially reduced the toxicity of heavy metals allowing transgenic cells to grow at wild-type rates in the presence of lethal concentrations of heavy metals. In addition, the metal binding capacity of transgenic algae has been increased five-fold relative to wild-type cells. Recently, fluorescent heavy metal biosensors have been developed for expression in transgenic Chlamydomonas. These fluorescent biosensor strains can be used for the detection and quantification of bioavailable heavy metals in aquatic environments. The use of transgenic microalgae to monitor and remediate heavy metals in aquatic environments is not without risk, however. Strategies to prevent the release of live microalgae having enhanced metal binding properties are described.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Guerinot ML. The ZIP family of metal transporters. Biochim Biophys Acta 2000; 1465:190–198.

    Article  PubMed  CAS  Google Scholar 

  2. Williams LE, Pittman JK, Hall JL. Emerging mechanisms for heavy metal transport in plants. Biochim Biophys Acta 2000; 1465:104–126.

    Article  PubMed  CAS  Google Scholar 

  3. Cohen CK, Fox TC, Garvin DF et al. The role of iron-deficiency stress responses in stimulating heavy metal transport in plants. Plant Physiol 1998; 116:1063–1072.

    Article  PubMed  CAS  Google Scholar 

  4. Pence NS, Larsen PB, Ebbs SD et al. The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc Nat Acad Ssi 2000; 97:4956–4960.

    Article  CAS  Google Scholar 

  5. Logan TJ, Traina SJ. Trace metals in agriculture. In: Allen HE, Perdue EM, Brown DS, eds. Metals in Groundwater. Chelsea, MI: Lewis Pub, 1993:309–349.

    Google Scholar 

  6. Nriagu JO, Pacyna JM. Quantitative assessment of worldwide contamination of the air, water and soils by trace metals. Nature 1988; 333:134–139.

    Article  PubMed  CAS  Google Scholar 

  7. Harris PO, Ramelow GJ. Binding of metal ions by particulate biomass derived from Chlorella vulgaris and Scenedesmus quadracauda. Environ Sci Technol 1990; 24:220–228.

    Article  CAS  Google Scholar 

  8. Sandau E, Sandau P, Pulz O et al. Heavy metal sorption by marine algae and algal by-products. Acta Biotechnol 1996; 16:103–119.

    Article  CAS  Google Scholar 

  9. Xue HB, Stumm W, Sigg L The binding of heavy metals to algal surfaces. Wat Res 1988; 22:917–926.

    Article  CAS  Google Scholar 

  10. Luoma SN, van Geen A, Lee BG et al. Metal uptake by phytoplankton duringa bloom in South San Francisco Bay: Implications for metal cycling in estuaries. Limnol. Oceanogr 1998; 43:1007–1016.

    CAS  Google Scholar 

  11. Mehta SK, Gaur JP. Use of microalgae for removing heavy metal ions from wastewater: Progress and prospects. Crit Rev Biotechnol 2005; 25:113–152.

    Article  PubMed  CAS  Google Scholar 

  12. Khoshmanesh A, Lawson F, Prince IG. Cell surface area as a major parameter in the uptake of cadmium by unicellular green microalgae. Chem Engineer J 1997; 65:13–19.

    Article  CAS  Google Scholar 

  13. Tuzun I, Bayramoglu G, Yalcin E et al. Equilibrium and kinetic studies on Biosorption of Hg(II), Cd(II) and Pb(II) ions onto microalgae, Chlamydomonas reinhardtii. J Environ Manag 2005; 77:85–92.

    Article  CAS  Google Scholar 

  14. Adhiya J, Cai XH, Sayre RT et al. Binding of aqueous cadmium by the lyophilized biomass of Chlamydomonas reinhardtii. Colloids and Surfaces A: Physicochemical and Engineering Aspects 2002; 210:1–11.

    Article  CAS  Google Scholar 

  15. Cai XH, Logan T, Gustafson T et al. Applications of eukaryotic algae for the removal of heavy metals from water. Molecular Marine Biology and Biotechnology 1995; 4:338–344.

    CAS  Google Scholar 

  16. Cai XH, Brown C, Adihya J et al. Heavy metal binding properties of wild type and transgenic algae (Chlamydomonas sp.). In: Le Gal Y, Halvorson H, eds. New Developments in Marine Biotechnology. Plenum Press, 1998:199–202.

    Google Scholar 

  17. Cai XH, Brown C, Adihya C et al. Growth and heavy metal binding properties of transgenic algae (Chlamydomonas reinhardtii) expressing a foreign metallothionein gene. Int J Phytoremediation 1999; 1:53–65.

    Article  CAS  Google Scholar 

  18. Roberts K, Gay MR, Hills GJ. Cell wall glycoproteins from Chlamydomonas reinhardtii are sulphated. Physiol Plant 1980; 49:421–424.

    Article  CAS  Google Scholar 

  19. Siripornadulsil S, Traina S, Verma DP et al. Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 2002; 14:2837–2847.

    Article  PubMed  CAS  Google Scholar 

  20. Hanikenne M, Kramer U, Demoulin V et al. A comparative inventory of metal transporters in the green alga Chlamydomonas reinhardtii and the red alga Cyanidioschizon merolae. Pl Physiol 2005; 137:428–446.

    Article  CAS  Google Scholar 

  21. Rosakis A, Koster W. Divalent metal transport in the green microalga, Chlamydomonas reinhardtii is mediated by a protein similar to prokaryotic Nramp homolgues. BioMetals 2005; 18:107–120.

    Article  PubMed  CAS  Google Scholar 

  22. Rubinelli P, Siripornadulsil S, Gao-Rubinelli F et al. Cadmium and iron-stress inducible gene expression in the green alga Chlamydomonas reinhardtii: Evidence for H43 protein function in iron assimilation. Planta 2002; 215:1–13.

    Article  PubMed  CAS  Google Scholar 

  23. Siripornadulsil S, Traina S, Sayre RT. Heavy metal binding properties of Chlamydomonas cells expressing plasmamembrane anchored metallothionein fusion proteins. 2006, (in preparation).

    Google Scholar 

  24. Sayre RT, Wagner RE. Method of making microalgal-based animal foodstuff supplements, microalgal-supplemented foodstuffs and method of animal nutrition. US Patent 2005, (Number 6,932,980).

    Google Scholar 

  25. Kagi JHR, Schaffer A. Biochemistry of metallothionein. Biochem 1988; 27:8509–8515.

    Article  CAS  Google Scholar 

  26. Stillman, Martin J. Metallothioneins. Coord Chem Rev 1995; 144:461–511.

    Article  CAS  Google Scholar 

  27. He Z, Weavers LK, Siripornadulsil S et al. Removal of mercury from sediment by ultrasound combined with Chlamydomonas reinhardtii. Am Chem Soc 2006, (Atlanta, GA).

    Google Scholar 

  28. Pinto E, Sigaud-Kutner TCS, Leitao MAS et al. Heavy metal-induced oxidative stress in algae. J Phycol 2003; 39:1008–1018.

    Article  CAS  Google Scholar 

  29. Hu S, Lau KWK, Wu M. Cadmium sequestration in Chlamydomonas reinhardtii. Pl Sci 2001; 161:987–996.

    Article  CAS  Google Scholar 

  30. Gekeler W, Grill E, Winnacker EL et al. Algae sequester heavy metals via synthesis of phytochelatin complexes. Archiv Microbiol 1988; 150:197–202.

    Article  CAS  Google Scholar 

  31. Howe G, Merchant S. Heavy metal-activated synthesis of peptides in Chlamydomonas reinhardtii. Plant Physiol 1992; 98:127–136.

    Article  PubMed  CAS  Google Scholar 

  32. Clemens S, Kim EJ, Neumann D et al. Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J 1999; 18:3325–3333.

    Article  PubMed  CAS  Google Scholar 

  33. Suk-Bong H, Smith AP, Howden R et al. Phytochelatin synthase genes from Arabidopsis and the yeast Schizosacchromyces pombe. Plant Cell 1999; 11:1153–1163.

    Google Scholar 

  34. Vatamaniuk OK, Mari S, Lu YP et al. Mechanism of heavy metal ion activation of phytochelatin (PC) synthase-blocked thiols are sufficient for PC synthase-catalyzed transpeptidation of glu-tathione and related thiol peptides. J Biol Chem 2000; 275:31451–31459.

    Article  PubMed  CAS  Google Scholar 

  35. Lee JG, Ahner BA, Morel FMM. Export of Cadmium and phytochelatin by the marine diatom Thalassiosira weissflogii. Environ Sci Technol 1996; 30:1814–1821.

    Article  CAS  Google Scholar 

  36. Hu CA, Delauney AJ, Verma DPS. A bifunctional enzyme (Δ1-pyrroline-5-carboxylate syntetase) catalyzes the first two steps in proline biosynthesis in plants. Proc Nat Acad Sci 1992; 89:9354–9358.

    Article  PubMed  CAS  Google Scholar 

  37. Peng Z, Verma DPS. A rice HAL2-like gene encodes a Ca2+-sensitive 3′(2′), 5′-diphosphonucleoside 3′(2′)-phosphohydrolase and complements yeast met22 and Escherichia coli cysQ mutations. J Biol Chem 1995; 270:29105–29110.

    Article  PubMed  CAS  Google Scholar 

  38. Peng Z, Lu Q, Verma DPS. Reciprocal regulation of Δ1-pyrroline-5-carboxylate synthetase and proline dehydrogenase genes controls proline levels during and after osmotic stress in plants. Mol Gen Genet 1996; 253:334–341.

    PubMed  CAS  Google Scholar 

  39. Siripornadulsil S. Molecular characterization of heavy metal metabolism in transgenic microalgae (Chlamydomonas reinhardtii). Ph D thesis 2002, (Ohio State University).

    Google Scholar 

  40. Chaudri AM, Knight BP, Barbosa-Jefferson VL et al. Determination of acute zinc toxicity in pore water from soils previously treated with sewage sludge using bioluminescence assays. Environ Sci Technol 1999; 33:1880–1885.

    Article  CAS  Google Scholar 

  41. Monciardini P, Podini D, Marmiroli N. Exotic gene expression in transgenic plants as a tool for monitoring environmental pollution. Chemosphere 1998; 37:2761–2772.

    Article  CAS  Google Scholar 

  42. Mutwakil MHAZ, Reader JP, Holdich DM et al. Use of stress-inducible transgenic nematodes as biomarkers of heavy metal pollution in water samples from an English river system. Archiv Environ Contain Toxicol 1997; 32:146–153.

    Article  CAS  Google Scholar 

  43. Tauriainen S, Karp M, Chang W et al. Luminescent bacterial sensor for cadmium and lead. Biosens Bioelectron 1998; 13:931–938.

    Article  PubMed  CAS  Google Scholar 

  44. Williams RE, Holt PJ, Bruce NC et al. Heavy metals. Biosensors for Environmental Monitoring. 2000:213–225.

    Google Scholar 

  45. Rajamani S, Ewalt J, Torres M et al. Transgenic microalgae as heavy metal biosensors. (in preparation)

    Google Scholar 

  46. Stryer L, Haugland RP. Energy transfer: A spectroscopic ruler. Proc Natl Acad Sci 1967; 58:719–726.

    Article  PubMed  CAS  Google Scholar 

  47. Selvin PR. Fluorescence resonance energy transfer. Methods Enzymol 1995; 246:300–334.

    Article  PubMed  CAS  Google Scholar 

  48. Weiss S. Measuring conformational dynamics of biomolecules by single molecule fluorescence spectroscopy. Nat Struct Biol 2000; 7:724–729.

    Article  PubMed  CAS  Google Scholar 

  49. Tsien RY. The green fluorescent protein. Annu Rev Biochem 1998; 67:509–544.

    Article  PubMed  CAS  Google Scholar 

  50. Cubitt AB, Woollenweber LA, Heim R. Understanding structure-function relationships in the Aequorea victoria green fluorescent protein. Methods Cell Biol 1999; 58:19–30.

    Article  PubMed  CAS  Google Scholar 

  51. Truong K, Ikura M. The use of FRET imaging microscopy to detect protein-protein interactions and protein conformational changes in vivo. Curr Opin Struct Biol 2001; 11:573–578.

    Article  PubMed  CAS  Google Scholar 

  52. Miyawaki A, Llopis J, Heim R et al. Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 1997; 388:882–887.

    Article  PubMed  CAS  Google Scholar 

  53. Zaccolo M. Use of chimeric fluorescent proteins and fluorescence resonance energy transfer to monitor cellular responses. Circ Res 2004; 94:866–873.

    Article  PubMed  CAS  Google Scholar 

  54. Pearce LL, Gandley RE, Han W et al. Role of metallothionein in nitric oxide signaling as revealed by a green fluorescent fusion protein. Proc Nat Acad Sci 2000; 97:477–482.

    Article  PubMed  CAS  Google Scholar 

  55. Nagai T, Ibata K, Park ES et al. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 2002; 20:87–90.

    Article  PubMed  CAS  Google Scholar 

  56. Zacharias DA, Violin JD, Newton AC et al. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 2002; 296:913–916.

    Article  PubMed  CAS  Google Scholar 

  57. Diener DR, Curry AM, Johnson KA et al. Rescue of a paralyzed-flagella mutant of Chlamydomonas by transformation. Proc Natl Acad Sci 1990; 87:5739–5743.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Plant Cellular and Molecular Biology, Ohio State University, Columbus, Ohio, 43210, USA

    Richard Sayre

  2. Biophysics Program, Ohio State University, Columbus, Ohio, USA

    Sathish Rajamani

  3. Department of Microbiology, Khon Kaen University, Khon Kaen, Thailand

    Surasak Siripornadulsil

  4. Department of Biochemistry, University of Sao Paulo, Sao Paulo, Brazil

    Vanessa Falcao, Moacir Torres & Pio Colepicolo

  5. Biophysics Program and Department of Plant Cellular and Molecular Biology, Ohio State University, Columbus, Ohio, USA

    Richard Sayre

Authors
  1. Sathish Rajamani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Surasak Siripornadulsil
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vanessa Falcao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Moacir Torres
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pio Colepicolo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Richard Sayre
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Departamento de Química y Ciencia de Materiales, Facultad de Ciencias Experimentales, Universidad de Huelva, Huelva, Spain

    Rosa León Ph.D.

  2. Departamento de Bioquímica y Biología Molecular, Campus de Rabanales, Universidad de Córdoba, Córdoba, Spain

    Aurora Galván Ph.D.  & Emilio Fernández Ph.D.  & 

Rights and permissions

Reprints and permissions

Copyright information

© 2007 Landes Bioscience and Springer Science+Business Media

About this chapter

Cite this chapter

Rajamani, S., Siripornadulsil, S., Falcao, V., Torres, M., Colepicolo, P., Sayre, R. (2007). Phycoremediation of Heavy Metals Using Transgenic Microalgae. In: León, R., Galván, A., Fernández, E. (eds) Transgenic Microalgae as Green Cell Factories. Advances in Experimental Medicine and Biology, vol 616. Springer, New York, NY. https://doi.org/10.1007/978-0-387-75532-8_9

Download citation

Publish with us

Policies and ethics

Search

Navigation