Bioavailability of trace metals to aquatic microorganisms: importance of chemical, biological and physical processes on biouptake
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)
- et al.
Trace metal transport by marine microorganisms: implications of metal coordination kinetics
Deep-sea Res. I
(1993) Which aqueous species control the rates of trace metal uptake by aquatic biota? Observations and predictions of non-equilibrium effects
Sci. Total Environ.
(1998)- et al.
Metal bioavailability to phytoplankton-applicability of the biotic ligand model
Comp. Biochem. Physiol. C Toxicol. Pharmacol.
(2002) Modelling metal interactions at fish gills
Sci. Total Environ.
(1998)- et al.
Cobalt binding to gills of rainbow trout (Oncorhynchus mykiss): an equilibrium model
Comp. Biochem. Physiol. Part Toxicol. Pharmacol.
(1998) - et al.
The Saccharomyces cerevisiae high affinity phosphate transporter encoded by PHO84 also functions in manganese homeostasis
J. Biol. Chem.
(2003) - et al.
Determination of organic complexation of cobalt in seawater by cathodic stripping voltammetry
Mar. Chem.
(2001) - et al.
Molecular and ionic mimicry and the transport of toxic metals
Toxicol. Appl. Pharmacol.
(2005) - et al.
Metal toxicity in Chlamydomonas reinhardtii. Effect on sulfate and nitrate assimilation
Biomol. Eng.
(2003) - et al.
Biotic ligand model development predicting Zn toxicity to the alga Pseudokirchneriella subcapitata: possibilities and limitations
Comp. Biochem. Physiol. C Toxicol. Pharmacol.
(2002)
The yeast plasma membrane protein Alr1 controls Mg2+ homeostasis and is subject to Mg2+-dependent control of its synthesis and degradation
J. Biol. Chem.
Overexpression of the Saccharomyces cerevisiae magnesium transport system confers resistance to aluminum ion
J. Biol. Chem.
Escherichia coli soft metal ion-translocating ATPases
J. Biol. Chem.
Bacterial resistances to toxic metal ions—a review
Gene
Microbial resistance to metals in the environment
Ecotoxicol. Environ. Saf.
The ZIP family of metal transporters
Biochimica Biophysica Acta, Biomembranes
The ZRT2 gene encodes the low affinity zinc transporter in Saccharomyces cerevisiae
J. Biol. Chem.
Processes regulating cellular accumulation and physiological effects: phytoplankton as model systems
Sci. Total Environ.
Zinc-induced inactivation of the yeast ZRT1 zinc transporter occurs through endocytosis and vacuolar degradation
J. Biol. Chem.
Purification and characterization of Ag, Zn-superoxide dismutase from Saccharomyces cerevisiae exposed to silver
J. Biol. Chem.
Subcellular distribution of cadmium in the unicellular alga Chlamydomonas reinhardtii
J. Plant Physiol.
Ultrastructural changes in Clamydomonas acidophila (Chlorophyta) induced by heavy metals and polyphosphate metabolism
FEMS Microbiol. Ecol.
Transport of metal binding-peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein
J. Biol. Chem.
Phytochelatin concentrations in the equatorial Pacific
Deep-sea Res. I
Increase of free cysteine and citric acid in plant cells exposed to cobalt ions
Phytochemistry
Characterization of phytochelatin synthase-like protein encoded by alr0975 from a prokaryote, Nostoc sp. PCC 7120
Biochem. Biophys. Res. Commun.
Heavy metal detoxification in higher plants—a review
Gene
Effect of initial cell density on the bioavailability and toxicity of copper in microalgal bioassays
Environ. Toxicol. Chem.
Metal speciation dynamics and bioavailability. 2. Radial diffusion effects in the microorganism range
Environ. Sci. Technol.
Role of fulvic acid on lead bioaccumulation by Chlorella kesslerii
Environ. Sci. Technol.
Effect of pH on Pb biouptake by the freshwater alga Chlorella kesslerii
Environmental Chemistry Letters
Principles and Applications of Aquatic Chemistry
Metal speciation dynamics and bioavailability: inert and labile complexes
Environ. Sci. Technol.
Predicting the bioavailability of metals and metal complexes: critical review of the biotic ligand model
Environ. Chem.
The relationship between cupric ion activity and the toxicity of copper to phytoplankton
J. Mar. Res.
Silver uptake by the green alga Chlamydomonas reinhardtii in relation to chemical speciation: influence of chloride
Environ. Toxicol. Chem.
Failure of the biotic ligand and free-ion activity models to explain zinc bioaccumulation by Chlorella kesslerii
Environ. Toxicol. Chem.
Speciation of Cu and Zn in drainage water from agricultural soils
Environ. Sci. Technol.
Uptake of 64Cu-oxine by marine phytoplankton
Environ. Sci. Technol.
Uptake of lipophilic organic Cu, Cd, and Pb complexes in the coastal diatom Thalassiosira weissflogii
Environ. Sci. Technol.
Effects of dithiocarbamate and 8-hydroxyquinoline additions on algal uptake of ambient copper and nickel in South San Francisco Bay water
Estuaries
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.
Secondary transporters for citrate and the Mg(2+)-citrate complex in Bacillus subtilis are homologous proteins
J. Bacteriol.
Impact of the Mg(2+)-citrate transporter CitM on heavy metal toxicity in Bacillus subtilis
Arch. Microbiol.
Cadmium and zinc bioavailability to Selenastrum capricornutum (Chlorophyceae): accidental metal uptake and toxicity in the presence of citrate
J. Phycol.
Thiosulfate enhances silver uptake by a green alga: role of anion transporters in metal uptake
Environ. Sci. Technol.
Cited by (211)
Muddying the unexplored post-industrial waters: Biodiversity and conservation potential of freshwater habitats in fly ash sedimentation lagoons
2023, Science of the Total EnvironmentOpportunities and challenges of micronutrients supplementation and its bioavailability in anaerobic digestion: A critical review
2023, Renewable and Sustainable Energy ReviewsUntangling the role of biotic and abiotic ageing of various environmental plastics toward the sorption of metals
2023, Science of the Total EnvironmentTrace metals as key controlling switches regulating the efficiencies of aerobic and anaerobic bioprocesses
2023, Biochemical Engineering JournalAdvances in bacterial whole-cell biosensors for the detection of bioavailable mercury: A review
2023, Science of the Total Environment
- 1
Present address: CSIRO Atmospheric and Marine Research, Castray Esplanade, Hobart 7000, TAS, Australia