Cadmium thiosulfate complexes can be assimilated by a green alga via a sulfate transporter but do not increase Cd toxicity
Frédéric Boily A B , Claude Fortin A and Peter G. C. Campbell A *A Institut national de la recherche scientifique, Centre Eau Terre Environnement, Québec, QC, Canada.
B Present address: Ministère des Transports du Québec, Direction des matériaux d’infrastructures, Québec, QC, Canada.
Environmental Chemistry 19(4) 167-176 https://doi.org/10.1071/EN22038
Submitted: 23 April 2022 Accepted: 5 July 2022 Published: 30 August 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing.
Environmental context. Thiosulfate is present in natural waters, especially those influenced by sulfide oxidation, and it has a marked affinity for metals such as cadmium. Normally the binding of cadmium by thiosulfate would be expected to reduce the metal’s bioavailability. However, here we demonstrate that algal uptake of cadmium is enhanced in the presence of thiosulfate, indicating that Cd can enter the alga via a novel route as an intact Cd-thiosulfate complex.
Rationale. For a given free metal ion activity in the exposure solution, the Biotic Ligand Model assumes that metal uptake will be independent of the various ligands present in solution that are buffering [Mz+]. In this context, we have evaluated cadmium bioavailability in the absence or presence of thiosulfate, using Chlamydomonas reinhardtii as the test alga.
Methodology. Short-term exposures (≤41 min) were run with a fixed concentration of the free Cd2+ ion (3.0 ± 0.1 nM), buffered with either nitrilotriacetate or thiosulfate, to determine Cd uptake. Subsequent long-term exposures (72 h) over a range of free Cd2+ concentrations were used to determine the effects of Cd on algal growth.
Results. Contrary to Biotic Ligand Model predictions, Cd uptake was enhanced when Cd2+ was buffered with thiosulfate. Removal of sulfate from this exposure medium increased Cd uptake; conversely, if [SO42−] was increased, Cd uptake decreased. In the absence of thiosulfate, Cd uptake was unaffected by changes in [SO42−]. In the long-term exposures, the cellular Cd quota needed to reduce algal growth by 50% was significantly higher in the presence of thiosulfate than in its absence.
Discussion. In the presence of thiosulfate, Cd can enter the algal cell not only by cation transport but also by transport of the intact Cd-thiosulfate complex via the anion transporter responsible for sulfate uptake. We speculate that some of the Cd taken up by anion transport remains in complexed form and is less bioavailable than the Cd that enters the cell via cation transport.
Keywords: anionic uptake, cationic uptake, Cd, cell quota, growth inhibition, intracellular metal speciation, phytoplankton, sulfate, thiosulfate, trace metals, unicellular alga.
References
Batley GE, Apte SC, Stauber JL (2004). Speciation and bioavailability of trace metals in water: progress since 1982. Australian Journal of Chemistry 57, 903–919.| Speciation and bioavailability of trace metals in water: progress since 1982.Crossref | GoogleScholarGoogle Scholar |
Biedlingmaier S, Schmidt A (1989). Sulfate transport in normal and S-deprived Chlorella fusca. Zeitschrift Fur Naturforschung C 44, 495–503.
| Sulfate transport in normal and S-deprived Chlorella fusca.Crossref | GoogleScholarGoogle Scholar |
Blaby-Haas CE, Merchant SS (2012). The ins and outs of algal metal transport. Biochimica et Biophysica Acta (BBA) – Molecular Cell Research 1823, 1531–1552.
| The ins and outs of algal metal transport.Crossref | GoogleScholarGoogle Scholar |
Boullemant A, Lavoie M, Fortin C, Campbell PGC (2009). Uptake of hydrophobic metal complexes by three freshwater algae: unexpected influence of pH. Environmental Science & Technology 43, 3308–3314.
| Uptake of hydrophobic metal complexes by three freshwater algae: unexpected influence of pH.Crossref | GoogleScholarGoogle Scholar |
Bridges CC, Zalups RK (2005). Molecular and ionic mimicry and the transport of toxic metals. Toxicology and Applied Pharmacology 204, 274–308.
| Molecular and ionic mimicry and the transport of toxic metals.Crossref | GoogleScholarGoogle Scholar |
Buffle J, Wilkinson KJ, van Leeuwen HP (2009). Chemodynamics and bioavailability in natural waters. Environmental Science & Technology 43, 7170–7174.
| Chemodynamics and bioavailability in natural waters.Crossref | GoogleScholarGoogle Scholar |
Campbell PGC, Fortin C (2013) Biotic ligand model. In ‘Encyclopedia of Aquatic Ecotoxicology’. (Eds JF Férard, C Blaise) pp. 237–245. (Springer-Verlag: Heidelberg, Germany)
Campbell PGC, Errécalde O, Fortin C, Hiriart-Baer VP, Vigneault B (2002). Metal bioavailability to phytoplankton―applicability of the Biotic Ligand Model. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 133, 189–206.
| Metal bioavailability to phytoplankton―applicability of the Biotic Ligand Model.Crossref | GoogleScholarGoogle Scholar |
Chivers PT, Benanti EL, Heil-Chapdelaine V, Iwig JS, Rowe JL (2012). Identification of Ni-(l-His)2 as a substrate for NikABCDE-dependent nickel uptake in Escherichia coli. Metallomics 4, 1043–1050.
| Identification of Ni-(l-His)2 as a substrate for NikABCDE-dependent nickel uptake in Escherichia coli.Crossref | GoogleScholarGoogle Scholar |
Druschel GK, Schoonen MAA, Nordstrom DK, Ball JW, Xu Y, Cohn CA (2003). Sulfur geochemistry of hydrothermal waters in Yellowstone National Park, Wyoming, USA. III. An anion-exchange resin technique for sampling and preservation of sulfoxyanions in natural waters. Geochemical Transactions 4, 12–19.
| Sulfur geochemistry of hydrothermal waters in Yellowstone National Park, Wyoming, USA. III. An anion-exchange resin technique for sampling and preservation of sulfoxyanions in natural waters.Crossref | GoogleScholarGoogle Scholar |
Errécalde O, Campbell PGC (2000). Cadmium and zinc bioavailability to Selenastrum capricornutum (Chlorophyceae): accidental metal uptake and toxicity in the presence of citrate. Journal of Phycology 36, 473–483.
| Cadmium and zinc bioavailability to Selenastrum capricornutum (Chlorophyceae): accidental metal uptake and toxicity in the presence of citrate.Crossref | GoogleScholarGoogle Scholar |
Fortin C, Campbell PGC (1998). An ion-exchange technique for free-metal ion measurements (Cd2+, Zn2+): applications to complex aqueous media. International Journal of Environmental Analytical Chemistry 72, 173–194.
| An ion-exchange technique for free-metal ion measurements (Cd2+, Zn2+): applications to complex aqueous media.Crossref | GoogleScholarGoogle Scholar |
Fortin C, Campbell PGC (2000). Silver uptake by the green alga, Chlamydomonas reinhardtii, in relation to chemical speciation: influence of chloride. Environmental Toxicology and Chemistry 19, 2769–2778.
| Silver uptake by the green alga, Chlamydomonas reinhardtii, in relation to chemical speciation: influence of chloride.Crossref | GoogleScholarGoogle Scholar |
Fortin C, Campbell PGC (2001). Thiosulfate enhances silver uptake by a green alga: role of anion transporters in metal uptake. Environmental Science & Technology 35, 2214–2218.
| Thiosulfate enhances silver uptake by a green alga: role of anion transporters in metal uptake.Crossref | GoogleScholarGoogle Scholar |
Hassler CS, Slaveykova VI, Wilkinson KJ (2004). Discriminating between intra- and extracellular metals using chemical extractions. Limnology and Oceanography: Methods 2, 237–247.
| Discriminating between intra- and extracellular metals using chemical extractions.Crossref | GoogleScholarGoogle Scholar |
Hiriart-Baer VP, Fortin C, Lee DY, Campbell PGC (2006). Toxicity of silver to two freshwater algae, Chlamydomonas reinhardtii and Pseudokirchneriella subcapitata, grown under continuous culture conditions: influence of thiosulphate. Aquatic Toxicology 78, 136–148.
| Toxicity of silver to two freshwater algae, Chlamydomonas reinhardtii and Pseudokirchneriella subcapitata, grown under continuous culture conditions: influence of thiosulphate.Crossref | GoogleScholarGoogle Scholar |
Kondo R, Kasashima N, Matsuda H, Hata Y (2000). Determination of thiosulfate in a meromictic lake. Fisheries Science 66, 1076–1081.
| Determination of thiosulfate in a meromictic lake.Crossref | GoogleScholarGoogle Scholar |
Lu X, Wang H (2012). Microbial oxidation of sulfide tailings and the environmental consequences. Elements 8, 119–124.
| Microbial oxidation of sulfide tailings and the environmental consequences.Crossref | GoogleScholarGoogle Scholar |
Macfie SM, Tarmohamed Y, Welbourn PM (1994). Effects of cadmium, cobalt, copper, and nickel on growth of the green alga Chlamydomonas reinhardtii: the influences of the cell wall and pH. Archives of Environmental Contamination and Toxicology 27, 454–458.
| Effects of cadmium, cobalt, copper, and nickel on growth of the green alga Chlamydomonas reinhardtii: the influences of the cell wall and pH.Crossref | GoogleScholarGoogle Scholar |
Martell AE, Smith RM, Motekaitis RJ (2004) ‘NIST Critical Stability Constants of Metal Complexes Database, 8.0.’ (U.S. Department of Commerce: Gaithersburg, MD, USA)
Morel FMM (1983) ‘Principles and Applications of Aquatic Chemistry.’ (J. Wiley & Sons Ltd.: New York, NY, USA)
Paquet N, Lavoie M, Maloney F, Duval JFL, Campbell PGC, Fortin C (2015). Cadmium accumulation and toxicity in the unicellular alga Pseudokirchneriella subcapitata: influence of metal-binding exudates and exposure time. Environmental Toxicology and Chemistry 34, 1524–1532.
| Cadmium accumulation and toxicity in the unicellular alga Pseudokirchneriella subcapitata: influence of metal-binding exudates and exposure time.Crossref | GoogleScholarGoogle Scholar |
Pérez-Castiñeira JR, Prieto JL, González-Arroyo JG, Vega JM (1998). Kinetic properties of sulfate uptake in two types of eukaryotic green microalgae. Journal of Plant Physiology 153, 324–331.
| Kinetic properties of sulfate uptake in two types of eukaryotic green microalgae.Crossref | GoogleScholarGoogle Scholar |
Purcell TW, Peters JJ (1998). Sources of silver in the environment. Environmental Toxicology and Chemistry 17, 539–546.
| Sources of silver in the environment.Crossref | GoogleScholarGoogle Scholar |
Schecher WD, McAvoy D (2001) ‘MINEQL+: A Chemical Equilibrium Modeling System’, 4.62 edn. (Environmental Research Software: Hallowell, ME, USA)
Stein WD (1990) ‘Channels, Carriers and Pumps: an Introduction to Membrane Transport.’ (Academic Press Inc.: San Diego, CA, USA)
Twiss MR, Errécalde O, Fortin C, Campbell PGC, Jumarie C, Denizeau F, Berkelaar E, Hale B, van Rees K (2001). Coupling the use of computer chemical speciation models and culture techniques in laboratory investigations of trace metal toxicity. Chemical Speciation & Bioavailability 13, 9–24.
| Coupling the use of computer chemical speciation models and culture techniques in laboratory investigations of trace metal toxicity.Crossref | GoogleScholarGoogle Scholar |