Pb uptake by the freshwater alga Chlorella kesslerii in the presence of dissolved organic matter of variable composition
Cristina Lamelas A and Vera I. Slaveykova A BA Environmental Biophysical Chemistry, Environmental Science and Technology Institute, School of Architecture, Civil and Environmental Engineering (GR-SLV-ISTE-ENAC), Ecole Polytechnique Fédérale de Lausanne (EPFL), Station 2, CH-1015 Lausanne, Switzerland.
B Corresponding author. Email: vera.slaveykova@epfl.ch
Environmental Chemistry 5(5) 366-372 https://doi.org/10.1071/EN08043
Submitted: 20 July 2008 Accepted: 13 October 2008 Published: 31 October 2008
Environmental context. Dissolved organic matter (DOM) is of utmost importance for a toxic metal’s fate and ecotoxicity in the aquatic system, but the complex nature and variable composition of DOM makes the quantitative understanding of DOM’s role in the environment very difficult. We have demonstrated that the assumption that the properties of a DOM mixture are the sum of the properties of its individual fractions can capture the main trends characterising the role of DOM in lead speciation and adsorption by freshwater microalgae. This was done by mixing the isolated, well-characterised fractions of DOM and measuring levels of free lead ion and Pb adsorbed and internalised by algae.
Abstract. Dissolved organic matter (DOM) is a complex mixture of ill-defined components, which makes the quantitative understanding of DOM functions in aquatic systems a challenging task. The traditional approach for studying such complex mixtures involves their separation into groups of different components, while assuming minimal or no alteration of their properties. By mixing the pre-isolated and well-characterised individual fractions of the DOM, including humic, fulvic and alginic acids, we have demonstrated that the free Pb ion concentrations and the adsorbed Pb plus Pb internalised by the alga Chlorella kesslerii in the presence of DOM samples of different compositions can be predicted on the basis of the experiments performed in the presence of the individual DOM fractions. An additivity model assuming that the properties of the mixture can be considered as the sum of the properties of the individual components captured the Pb speciation and adsorption behaviour in the presence of DOM of variable compositions. Similarly to the results with the individual DOM fractions, internalised Pb concentrations in the presence of the reconstituted DOM were greater than that predicted by the corresponding free lead ion concentration. An improved fit between experimental observations and the model predictions of adsorbed plus internalised Pb in the presence of DOM of different compositions was observed by assuming that each individual component adsorbed by the algae gave access to additional binding sites for Pb. Furthermore, the contribution of the Pb–DOM complex to total cellular Pb was dominated by the humic and fulvic acids, whereas the contribution of alginate was minimal.
Additional keywords: additivity model, green alga.
Acknowledgements
Warm thanks are extended to the Swiss National Science Foundation PP002–102640 for providing funding directly related to the present work. Technical assistance of Michel Martin in ICP-MS measurements is highly appreciated.
[1]
G. Batley ,
S. Apte ,
J. Stauber ,
Speciation and bioavailability of trace metals in water: progress since 1982.
Aust. J. Chem. 2004
, 57, 903.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[2]
[3]
[4]
J.-P. Croué ,
Isolation of humic and non-humic NOM fractions: structural characterization.
Environ. Monit. Assess. 2004
, 92, 193.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
[5]
[6]
[7]
H. Kola ,
K. J. Wilkinson ,
Cadmium uptake by a green alga can be predicted by equilibrium modelling.
Environ. Sci. Technol. 2005
, 39, 3040.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[8]
B. Vigneault ,
A. Percot ,
M. Lafleur ,
P. G. C. 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 |
[9]
B. Vigneault ,
P. G. C. Campbell ,
Uptake of cadmium by freshwater green algae: effects of pH and aquatic humic substances.
J. Phycol. 2005
, 41, 55.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[10]
S. Bayen ,
I. Worms ,
N. Parthasarathy ,
K. Wilkinson ,
J. Buffle ,
Cadmium bioavailability and speciation using the permeation liquid membrane.
Anal. Chim. Acta 2006
, 575, 267.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[11]
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 |
[12]
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 |
[13]
A. Kungolos ,
P. Samaras ,
V. Tsiridis ,
M. Petala ,
G. Sakellaropoulos ,
Bioavailability and toxicity of heavy metals in the presence of natural organic matter.
J. Environ. Sci. Heal. A 2006
, 41, 1509.
|
CAS |
[14]
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 |
[15]
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 |
[16]
V. I. Slaveykova ,
K. J. Wilkinson ,
A. Ceresa ,
E. Pretsch ,
Role of fulvic acid on lead bioaccumulation by Chlorella kesslerii.
Environ. Sci. Technol. 2003
, 37, 1114.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[17]
K. J. Wilkinson ,
A. Joz-Roland ,
J. Buffle ,
Different roles of pedogenic fulvic acids and aquagenic biopolymers on colloid aggregation and stability in freshwaters.
Limnol. Oceanogr. 1997
, 42, 1714.
|
CAS |
[18]
K. Dedieu ,
T. Iuranova ,
V. I. Slaveykova ,
Do exudates mitigate Cd biouptake by rhizobacterium Sinorhizobium melilotii?
Environ. Chem. 2006
, 3, 424.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[19]
A. Smiejan ,
K. J. Wilkinson ,
C. Rossier ,
Cd bioaccumulation by a freshwater bacterium, Rhodospirillum rubrum.
Environ. Sci. Technol. 2003
, 37, 701.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[20]
B. Koukal ,
P. Rossé ,
A. Reinhardt ,
B. Ferrari ,
K. J. Wilkinson ,
J.-L. Loizeau ,
J. Dominik ,
Effect of Pseudokirchneriella subcapitata (Chlorophyceae) exudates on metal toxicity and colloid aggregation.
Water Res. 2007
, 41, 63.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[21]
[22]
C. Lamelas ,
F. Avaltroni ,
M. Benedetti ,
K. J. Wilkinson ,
V. I. Slaveykova ,
Quantifying Pb and Cd complexation by alginates and the role of metal binding on macromolecular aggregation.
Biomacromolecules 2005
, 6, 2756.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[23]
H. M. V. M. Soares ,
P. C. F. L. Conde ,
A. A. N. Almeida ,
M. T. S. D. Vasconcelos ,
Evaluation of n-substituted aminosulfonic acid pH buffers with a morpholinic ring for cadmium and lead speciation studies by electroanalytical techniques.
Anal. Chim. Acta 1999
, 394, 325.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[24]
H. E. Mash ,
Y.-P. Chin ,
L. Sigg ,
R. Hari ,
H. Xue ,
Complexation of copper by zwitterionic aminosulfonic (Good) buffers.
Anal. Chem. 2003
, 75, 671.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[25]
[26]
C. S. Hassler ,
V. I. Slaveykova ,
K. J. Wilkinson ,
Discriminating between intra- and extracellular bound metal using chemical extraction.
Limnol. Oceanogr. Methods 2004
, 2, 237.
[27]
V. I. Slaveykova ,
K. J. Wilkinson ,
Physicochemical aspects of lead bioaccumulation by Chlorella vulgaris.
Environ. Sci. Technol. 2002
, 36, 969.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[28]
J. Galceran ,
J. Monné ,
J. Puy ,
H. P. van Leewen ,
Transient biouptake flux and accumulation by microorganisms: the case of two types of sites with Langmuir adsorption.
Mar. Chem. 2006
, 99, 162.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[29]
J. M. Zachara ,
C. T. Resch ,
S. C. Smith ,
Influence of humic substances on Co2+ sorption by a subsurface mineral separate and its mineralogic components.
Geochim. Cosmochim. Acta 1994
, 58, 553.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[30]
M. F. Benedetti ,
Metal ion binding to colloids from database to field systems.
J. Geochem. Explor. 2006
, 88, 81.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[31]
D. Kinniburgh ,
W. van Riemsdijk ,
L. Koopal ,
M. Borkovec ,
M. Benedetti ,
M. Avena ,
Ion binding to natural organic matter: competition, heterogeneity, stoichiometry and thermodynamic consistency.
Colloid Surf. A 1999
, 151, 147.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[32]
D. Kinniburgh ,
C. J. Milne ,
M. Benedetti ,
J. Pinheiro ,
J. Filius ,
L. Koopal ,
W. Van Riemsdijk ,
Metal ion binding by humic acid: application of the NICA–Donnan model.
Environ. Sci. Technol. 1996
, 30, 1687.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[33]
E. R. Unsworth ,
K. W. Warnken ,
H. Zhang ,
W. Davison ,
F. Black ,
J. Buffle ,
J. Cao ,
R. Cleven ,
J. Galceran ,
P. Gunkel ,
E. Kalis ,
D. Kistler ,
H. P. van Leeuwen ,
M. Martin ,
S. Noel ,
Y. Nur ,
N. Odzak ,
J. Puy ,
W. van Riemsdijk ,
L. Sigg ,
E. Temminghoff ,
M.-L. Tercier-Waeber ,
S. Toepperwien ,
R. M. Town ,
L. Weng ,
H. Xue ,
Model predictions of metal speciation in freshwaters compared to measurements by in situ techniques.
Environ. Sci. Technol. 2006
, 40, 1942.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[34]
I. A. M. Worms ,
N. Parthasarathy ,
K. J. Wilkinson ,
Ni uptake by a green alga: 1. Validation of equilibrium models for complexation effects.
Environ. Sci. Technol. 2007
, 41, 4258.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[35]
E. Tipping ,
Humic ion-binding model VI: An improved description of the interactions of protons and metal ions with humic substances.
Aquat. Geochem. 1998
, 4, 3.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[36]
