Register      Login
Environmental Chemistry Environmental Chemistry Society
Environmental problems - Chemical approaches
RESEARCH ARTICLE

Cu and Pb accumulation by the marine diatom Thalassiosira weissflogii in the presence of humic acids

Paula Sánchez-Marín A B D , Vera I. Slaveykova C and Ricardo Beiras A B
+ Author Affiliations
- Author Affiliations

A Departamento de Ecoloxía e Bioloxía Animal, Facultade de Ciencias do Mar, Universidade de Vigo, Estrada Colexio Universitario s/n, E-36310 Vigo, Galicia, Spain.

B Estación de Ciencias Mariñas de Toralla (ECIMAT), Universidade de Vigo, Illa de Toralla, E-36331 Vigo, Galicia, Spain.

C Environmental Biophysical Chemistry, GR-SLV-IIE-ENAC, Ecole Polytechnique Fédérale de Lausanne (EPFL), Station 2, CH-1015 Lausanne, Switzerland.

D Corresponding author. Email: paulasanchez@uvigo.es

Environmental Chemistry 7(3) 309-317 https://doi.org/10.1071/EN10015
Submitted: 19 February 2010  Accepted: 15 April 2010   Published: 22 June 2010

Environmental context. Dissolved organic matter protects aquatic microorganisms from toxic metals by complexing and decreasing the concentration of the biologically reactive species such as free metal ions. However, there are some cases of enhancement of toxic effects when humic acids are present, which is thought to be due to effects of adsorbed humic acids on cell membranes. For a marine diatom, humic acids adsorbed to cell surfaces enhanced metal adsorption, whereas intracellular metal contents decreased as a result of metal binding by humic acids. These findings suggest that the diatom wall, the frustule, presents a barrier against direct effects of adsorbed humic acids on the plasma membrane.

Abstract. Metal complexation by dissolved organic matter, as humic acids, is considered to decrease metal bioavailability by lowering the free metal ion concentration. However, dissolved organic matter adsorption on cell surfaces can modify cell membrane properties, which can also influence metal uptake. Copper and lead accumulation and internalisation by the marine diatom Thalassiosira weissflogii were studied in the absence and presence of humic acids, and adsorption of humic acids to cell surfaces was evaluated. Both Pb and Cu intracellular concentrations decreased in the presence of humic acids according to labile metal concentrations measured by anodic stripping voltammetry, whereas total (intracellular plus adsorbed) metal content was enhanced in the presence of humic acids, probably owing to enhanced metal plus humics adsorption to cell surfaces. The results of the present work stress the importance of differentiating between intracellular and total cellular metal in bioavailability studies, and suggest that the silica frustule of diatoms represents a barrier against humic acids effects on cell membranes.

Additional keywords: anodic stripping voltammetry, DOM, metal bioavailability.


Acknowledgements

This work was partially funded by research projects CTM2006–13880-C03–01/MAR and CTM2009–10908 (Spanish Government). ICP-MS measurements were performed in the Centro de Apoio Científico Tecnolóxico á Investigación (CACTI) of the University of Vigo. We thank Damián Costas for the culture of the algae in the marine facilities of ECIMAT (University of Vigo). P. Sánchez-Marín was supported by the Spanish Ministry of Education and Science, Spanish Government. V. Slaveykova acknowledges the financial support of the Swiss National Science Foundation PP022 118989.


References


[1]   McKnight D. M., Aiken G. R., Sources and age of aquatic humus, in Aquatic Humic Substances: Ecology and Biogeochemistry (Eds D. O. Hessen, L. J. Tranvik) 1998, pp. 9–40 (Springer-Verlag: Berlin).

[2]   Benner R., Chemical composition and reactivity, in Biogeochemistry of Marine Dissolved Organic Matter (Eds D. A. Hansell, C. A. Carlson) 2002, pp. 59–90 (Elsevier: San Diego, CA, USA).

[3]   Campbell P. G. C., Interactions between trace metals and aquatic organisms: a critique of the free-ion activity model, in Metal Speciation and Bioavailability in Aquatic Systems (Eds A. Tessier, D. R. Turner) 1995, pp. 45–102 (Wiley: New York).

[4]   P. G. C. Campbell , O. Errécalde , C. Fortin , V. P. Hiriart-Baer , B. Vigneault , Metal bioavailability to phytoplankton – applicability to the biotic ligand model. Comp. Biochem. Phys. C 2002 , 133,  189.
         open url image1

[5]   Morel F. M. M., Principles of Aquatic Chemistry 1983 (Wiley: New York).

[6]   R. L. Wershaw , Model for humus in soils and sediments. Environ. Sci. Technol. 1993 , 27,  814.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[7]   E. Tipping , The adsorption of aquatic humic substances by iron oxides. Geochim. Cosmochim. Acta 1981 , 45,  191.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[8]   P. G. C. Campbell , M. R. Twiss , K. J. Wilkinson , Accumulation of natural organic matter on the surfaces of living cells: implications for the interaction of toxic solutes with aquatic biota. Can. J. Fish. Aquat. Sci. 1997 , 54,  2543.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[9]   V. B. Myers , R. L. Iverson , R. C. Harris , The effect of salinity and dissolved organic matter on surface charge characteristics of some euryhaline phytoplankton. J. Exp. Mar. Biol. Ecol. 1975 , 17,  59.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[10]   K. Knauer , J. Buffle , Adsorption of fulvic acid on algal surfaces and its effect on carbon uptake. J. Phycol. 2001 , 37,  47.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[11]   V. I. Slaveykova , K. J. Wilkinson , A. Ceresa , E. Pretsch , Role of fulvic acids on lead bioaccumulation by Chlorella kesslerii. Environ. Sci. Technol. 2003 , 37,  1114.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[12]   C. Lamelas , K. J. Wilkinson , V. I. Slaveykova , Influence of the composition of natural organic matter on Pb bioavailability to microalgae. Environ. Sci. Technol. 2005 , 39,  6109.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[13]   F. Galvez , A. Donini , D. S. Smith , M. J. O’Donnell , C. M. Wood , A matter of potential concern: natural organic matter alters the electrical properties of fish gills. Environ. Sci. Technol. 2008 , 42,  9385.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[14]   L. Parent , M. R. Twiss , P. G. C. Campbell , Influences of natural dissolved organic matter on the interaction of aluminum with microalga Chlorella: a test of the free-ion model of trace metal toxicity. Environ. Sci. Technol. 1996 , 30,  1713.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[15]   B. Vigneault , A. Percot , M. Lafleur , P. G. C. Campbell , Permeability changes in model and phytoplankton membranes in the presence of aquatic humic substances. Environ. Sci. Technol. 2000 , 34,  3907.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[16]   C. N. Glover , C. M. Wood , The disruption of Daphnia magna sodium metabolism by humic substances: mechanism of action and effect of humic substance source. Physiol. Biochem. Zool. 2005 , 78,  1005.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[17]   P. Sánchez-Marín , J. I. Lorenzo , R. Blust , R. Beiras , Humic acids increase dissolved lead bioavailability for marine invertebrates. Environ. Sci. Technol. 2007 , 41,  5679.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[18]   C. Lamelas , V. I. Slaveykova , Pb uptake by the freshwater alga Chlorella kesslerii in the presence of dissolved organic matter of variable composition. Environ. Chem. 2008 , 5,  366.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[19]   C. Lamelas , J. P. Pinheiro , V. I. Slaveykova , Effect of humic acid on Cd(II), Cu(II), and Pb(II) uptake by freshwater algae: kinetic and cell wall speciation considerations. Environ. Sci. Technol. 2009 , 43,  730.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[20]   C. Lamelas , V. I. Slaveykova , Comparison of Cd(II), Cu(II) and Pb(II) biouptake by green algae in the presence of humic acid. Environ. Sci. Technol. 2007 , 41,  4172.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[21]   J. I. Lorenzo , O. Nieto , R. Beiras , Effect of humic acids on speciation and toxicity of copper to Paracentrotus lividus larvae in seawater. Aquat. Toxicol. 2002 , 58,  27.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[22]   J. I. Lorenzo , R. Beiras , V. K. Mubiana , R. Blust , Copper uptake by Mytilus edulis in the presence of humic acids. Environ. Toxicol. Chem. 2005 , 24,  973.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[23]   J. I. Lorenzo , O. Nieto , R. Beiras , Anodic stripping voltammetry measures copper bioavailability for sea urchin larvae in the presence of fulvic acids. Environ. Toxicol. Chem. 2006 , 25,  36.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[24]   R. L. Malcolm , P. MacCarthy , Limitations in the use of commercial humic acids in water and soil research. Environ. Sci. Technol. 1986 , 20,  904.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[25]   Graham L. E., Wilcox L. W., Algae 2000 (Prentice Hall: Upper Saddle River, NJ).

[26]   Guillard R. R. L., Culture of phytoplankton for feeding marine invertebrates, in Culture of Marine Invertebrate Animals (Eds W. L. Smith, M. H. Chanley) 1975 (Plenum Press: New York).

[27]   F. Berbel , J. M. Díaz-Cruz , C. Ariño , M. Esteban , F. Mas , J. Ll. Garcés , J. Puy , Voltammetric analysis of heterogeneity in metal ion binding by humics. Environ. Sci. Technol. 2001 , 35,  1097.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[28]   I. Christl , C. J. Milne , D. G. Kinniburgh , R. Kretzchmar , Relating ion binding by fulvic and humic acids to chemical composition and molecular size. 2. Metal binding. Environ. Sci. Technol. 2001 , 35,  2512.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[29]   C. J. Milne , D. G. Kinniburgh , W. H. Van Riemsdijk , E. Tipping , Generic NICA–Donnan model parameters for metal-ion binding by humic substances. Environ. Sci. Technol. 2003 , 37,  958.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[30]   Mota A. M., Correia dos Santos M. M., Trace metal speciation of labile chemical species in natural waters: electrochemical methods, in Metal Speciation and Bioavailability in Aquatic Systems (Eds A. Tessier, D. R. Turner) 1995, pp. 205–258 (Wiley: New York).

[31]   Buffle J., Complexation Reactions in Aquatic Systems: an Analytical Approach 1990 (Ellis Horwood: Chichester, UK).

[32]   R. M. Town , M. Filella , Determination of metal ion binding parameters for humic substances. Part 2: Utility of ASV pseudo-polarography. J. Electroanal. Chem. 2000 , 488,  1.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[33]   F. L. Greter , J. Buffle , W. Haerdi , Voltammetric study of humic and fulvic substances. Part I. Study of their complexing properties with lead. J. Electroanal. Chem. 1979 , 101,  211.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[34]   V. I. Slaveykova , Predicting Pb bioavailability to freshwater microalgae in the presence of fulvic acid: algal cell density as a variable. Chemosphere 2007 , 69,  1438.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[35]   M.-A. Benincasa , G. Cartoni , N. Imperia , Effects of ionic strength and electrolyte composition on the aggregation of fractionated humic substances studied by flow field-flow fractionation. J. Sep. Sci. 2002 , 25,  405.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[36]   N. A. Wall , G. R. Choppin , Humic acids coagulation: influence of divalent cations. Appl. Geochem. 2003 , 18,  1573.
        | Crossref | GoogleScholarGoogle Scholar | CAS |  open url image1

[37]   A. Siripinyanond , S. Worapanyanond , J. Shiowatana , Field-flow fractionation–inductively coupled plasma mass spectrometry: an alternative approach to investigate metal-humic substances interaction. Environ. Sci. Technol. 2005 , 39,  3295.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |  open url image1

[38]   Round F. E., Crawford R. M., Mann D. G., The Diatoms. Biology & Morphology of the Genera 1990 (Cambridge University Press: Bath, UK).

[39]   P. Sánchez-Marín , J. Santos-Echeandía , M. Nieto-Cid , X. A. Álvarez-Salgado , R. Beiras , Effect of dissolved organic matter (DOM) of contrasting origins on Cu and Pb speciation and toxicity to Paracentrotus lividus larvae. Aquat. Toxicol. 2010 , 96,  90.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[40]   M. S. Hale , J. G. Mitchell , Functional morphology of diatom frustule microstructures: hydrodynamic control of Brownian particle diffusion and advection. Aquat. Microb. Ecol. 2001 , 24,  287.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1