Elsevier

Biochimie

Volume 88, Issue 11, November 2006, Pages 1721-1731
Biochimie

Bioavailability of trace metals to aquatic microorganisms: importance of chemical, biological and physical processes on biouptake

https://doi.org/10.1016/j.biochi.2006.09.008Get rights and content

Abstract

An important challenge in environmental biogeochemistry is the determination of the bioavailability of toxic and essential trace compounds in natural media. For trace metals, it is now clear that chemical speciation must be taken into account when predicting bioavailability. Over the past 20 years, equilibrium models (free ion activity model (FIAM), biotic ligand model (BLM)) have been increasingly developed to describe metal bioavailability in environmental systems, despite the fact that environmental systems are always dynamic and rarely at equilibrium. In these simple (relatively successful) models, any reduction in the available, reactive species of the metal due to competition, complexation or other reactions will reduce metal bioaccumulation and thus biological effects. Recently, it has become clear that biological, physical and chemical reactions occurring in the immediate proximity of the biological surface also play an important role in controlling trace metal bioavailability through shifts in the limiting biouptake fluxes. Indeed, for microorganisms, examples of biological (transport across membrane), chemical (dissociation kinetics of metal complexes) and physical (diffusion) limitation can be demonstrated. Furthermore, the organism can employ a number of biological internalization strategies to get around limitations that are imposed on it by the physicochemistry of the medium. The use of a single transport site by several metals or the use of several transport sites by a single metal further complicates the prediction of uptake or effects using the simple chemical models. Finally, once inside the microorganism the cell is able to employ a large number of strategies including complexation, compartmentalization, efflux or the production of extracellular ligands to minimize or optimize the reactivity of the metal. The prediction of trace metal bioavailability will thus require multidisciplinary advances in our understanding of the reactions occurring at and near the biological interface. By taking into account medium constraints and biological adaptability, future bioavailability modeling will certainly become more robust.

Introduction

In natural waters, the bioavailability of trace metals, including their toxicity, is thought to be related to their ability to cross biological barriers (e.g. plasma membrane) and it is most often predicted by the concentration [1] or flux [2] of internalized metal. The biouptake process depends not only on the internalization pathways and their specificity but also on the physicochemistry of the medium and the size and nature of the organism [3]. Equilibrium models that have been developed to predict the role of chemical speciation on metal bioavailability are often (qualitatively) successful in predicting a reduction in trace metal effects due to complexation (inorganic and organic ligands, [4]) or competition (e.g. H+, Ca2+, etc., [5]); both processes result in a decreased interaction of the metal with uptake sites on the surface of the organism. Nonetheless, a fundamental understanding of the biouptake process is currently lacking, especially for the conditions that are the most relevant to the natural environment (i.e. presence of multiple stressors, ligand heterogeneity and polydispersity, non-equilibrium conditions, etc.). Such a quantitative understanding requires insights into:

  • the behavior of metal species during their transport from the bulk solution (i.e. >few microns from the biological surface) to the biological interface;

  • the transfer of the chemical across the biological membrane and;

  • the role of the organism in modifying the chemistry and biology of the uptake process (Fig. 1; [2], [6], [7], [8], [9], [10]).

This mini-review examines the influence of these processes on biouptake and is concluded with two examples where the importance of chemical, biological and physical processes is demonstrated.

Section snippets

Role of the physicochemistry of the bulk solution

A consensus exists in the literature with respect to the key fluxes that define the interaction of trace metals with aquatic organisms (Fig. 1). Trace metals, and their complexes, must first diffuse from the external medium to the surface of the organism (mass transport). Metal complexes are often dynamic, able to dissociate and reassociate (complexation/dissociation) in the time that it takes to diffuse to the biological surface. To have an effect, the metal must react with a sensitive site on

Metal internalization

Internalization is the key step in the overall biouptake process. As opposed to the processes in the bulk solution, the plasma membrane is biologically active and often able to control the magnitude of the internalization fluxes according to the requirements of the organism. Due to the overall hydrophobic nature of the biological membrane, only neutral or non-polar molecules cross into the cytosol by passive diffusion (based upon the concentration gradient between external and internal

Impact of cellular regulation on metal bioavailability

Organisms have a number of transport systems that are sensitive to their external surroundings [66]. For example, in yeast, the Zrt1 (ZIP family) transporter may be induced at low Zn concentrations and rapidly degraded via the ubiquitin pathway if the Zn concentration increases. Transporter degradation is likely stimulated, but with less efficiency, in the presence of Cd or Co [67]. Such feedback has also been demonstrated in marine phytoplankton for Mn, Cd and Zn [68]. Regulation of the

Examples of interactions among chemistry, biology and physics: metals at the biological interface

Zn and Fe are essential trace metals that are required for the development of microorganisms. Their complex chemical speciation, highly specialized biological uptake and intracellular homeostasis have been extensively studied to the point that they are good examples of the complexity of trace metal bioavailability (Fig. 3). Indeed, under some conditions, the bioavailability of either metal is likely limited by its diffusive flux or by ligand exchange kinetics [19], [121], [122], [123] such

Acknowledgements

The authors thank the Swiss National Science Foundation, the National Science and Engineering Research Council of Canada and the ECODIS project (European Commission's 6th framework program, subpriority 6.3 “Global Change and Ecosystems”, contract 518043) for funding contributing to this work.

References (160)

  • A. Graschopf et al.

    The yeast plasma membrane protein Alr1 controls Mg2+ homeostasis and is subject to Mg2+-dependent control of its synthesis and degradation

    J. Biol. Chem.

    (2001)
  • C.W. MacDiarmid et al.

    Overexpression of the Saccharomyces cerevisiae magnesium transport system confers resistance to aluminum ion

    J. Biol. Chem.

    (1998)
  • D. Gatti et al.

    Escherichia coli soft metal ion-translocating ATPases

    J. Biol. Chem.

    (2000)
  • S. Silver

    Bacterial resistances to toxic metal ions—a review

    Gene

    (1996)
  • M.R. Bruins et al.

    Microbial resistance to metals in the environment

    Ecotoxicol. Environ. Saf.

    (2000)
  • M.L. Guerinot

    The ZIP family of metal transporters

    Biochimica Biophysica Acta, Biomembranes

    (2000)
  • H. Zhao et al.

    The ZRT2 gene encodes the low affinity zinc transporter in Saccharomyces cerevisiae

    J. Biol. Chem.

    (1996)
  • W.G. Sunda et al.

    Processes regulating cellular accumulation and physiological effects: phytoplankton as model systems

    Sci. Total Environ.

    (1998)
  • R.S. Gitan et al.

    Zinc-induced inactivation of the yeast ZRT1 zinc transporter occurs through endocytosis and vacuolar degradation

    J. Biol. Chem.

    (1998)
  • M.R. Ciriolo et al.

    Purification and characterization of Ag, Zn-superoxide dismutase from Saccharomyces cerevisiae exposed to silver

    J. Biol. Chem.

    (1994)
  • K. Nagel et al.

    Subcellular distribution of cadmium in the unicellular alga Chlamydomonas reinhardtii

    J. Plant Physiol.

    (1996)
  • K. Nishikawa et al.

    Ultrastructural changes in Clamydomonas acidophila (Chlorophyta) induced by heavy metals and polyphosphate metabolism

    FEMS Microbiol. Ecol.

    (2003)
  • D. Ortiz et al.

    Transport of metal binding-peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein

    J. Biol. Chem.

    (1995)
  • B.A. Ahner et al.

    Phytochelatin concentrations in the equatorial Pacific

    Deep-sea Res. I

    (1998)
  • M. Oven et al.

    Increase of free cysteine and citric acid in plant cells exposed to cobalt ions

    Phytochemistry

    (2002)
  • N. Tsuji et al.

    Characterization of phytochelatin synthase-like protein encoded by alr0975 from a prokaryote, Nostoc sp. PCC 7120

    Biochem. Biophys. Res. Commun.

    (2004)
  • M. Zenk

    Heavy metal detoxification in higher plants—a review

    Gene

    (1996)
  • N.M. Franklin et al.

    Effect of initial cell density on the bioavailability and toxicity of copper in microalgal bioassays

    Environ. Toxicol. Chem.

    (2002)
  • K.J. Wilkinson et al.
  • J.P. Pinheiro et al.

    Metal speciation dynamics and bioavailability. 2. Radial diffusion effects in the microorganism range

    Environ. Sci. Technol.

    (2001)
  • V.I. Slaveykova et al.

    Role of fulvic acid on lead bioaccumulation by Chlorella kesslerii

    Environ. Sci. Technol.

    (2003)
  • V.I. Slaveykova et al.

    Effect of pH on Pb biouptake by the freshwater alga Chlorella kesslerii

    Environmental Chemistry Letters

    (2003)
  • F.M.M. Morel et al.

    Principles and Applications of Aquatic Chemistry

    (1993)
  • M. Whitfield et al.
  • A. Tessier et al.
  • H.P. van Leeuwen

    Metal speciation dynamics and bioavailability: inert and labile complexes

    Environ. Sci. Technol.

    (1999)
  • V.I. Slaveykova et al.

    Predicting the bioavailability of metals and metal complexes: critical review of the biotic ligand model

    Environ. Chem.

    (2005)
  • P.G.C. Campbell
  • W.G. Sunda et al.

    The relationship between cupric ion activity and the toxicity of copper to phytoplankton

    J. Mar. Res.

    (1976)
  • C. Fortin et al.

    Silver uptake by the green alga Chlamydomonas reinhardtii in relation to chemical speciation: influence of chloride

    Environ. Toxicol. Chem.

    (2000)
  • C.S. Hassler et al.

    Failure of the biotic ligand and free-ion activity models to explain zinc bioaccumulation by Chlorella kesslerii

    Environ. Toxicol. Chem.

    (2003)
  • A.P. Aldrich et al.

    Speciation of Cu and Zn in drainage water from agricultural soils

    Environ. Sci. Technol.

    (2002)
  • P.L. Croot et al.

    Uptake of 64Cu-oxine by marine phytoplankton

    Environ. Sci. Technol.

    (1999)
  • J.T. Phinney et al.

    Uptake of lipophilic organic Cu, Cd, and Pb complexes in the coastal diatom Thalassiosira weissflogii

    Environ. Sci. Technol.

    (1994)
  • J.T. Phinney et al.

    Effects of dithiocarbamate and 8-hydroxyquinoline additions on algal uptake of ambient copper and nickel in South San Francisco Bay water

    Estuaries

    (1997)
  • J.T. Phinney et al.

    Trace metal exchange in solution by the fungicides ziram and maneb (dithiocarbamates) and subsequent uptake of lipophilic organic zinc, copper and lead complexes into phytoplankton cells

    Environ. Toxicol. Chem.

    (1997)
  • A. Boorsma et al.

    Secondary transporters for citrate and the Mg(2+)-citrate complex in Bacillus subtilis are homologous proteins

    J. Bacteriol.

    (1996)
  • B.P. Krom et al.

    Impact of the Mg(2+)-citrate transporter CitM on heavy metal toxicity in Bacillus subtilis

    Arch. Microbiol.

    (2002)
  • O. Errecalde et al.

    Cadmium and zinc bioavailability to Selenastrum capricornutum (Chlorophyceae): accidental metal uptake and toxicity in the presence of citrate

    J. Phycol.

    (2000)
  • C. Fortin et al.

    Thiosulfate enhances silver uptake by a green alga: role of anion transporters in metal uptake

    Environ. Sci. Technol.

    (2001)
  • Cited by (211)

    View all citing articles on Scopus
    1

    Present address: CSIRO Atmospheric and Marine Research, Castray Esplanade, Hobart 7000, TAS, Australia

    View full text