Algal bioaccumulation and toxicity of platinum are increased in the presence of humic acids
Océane Hourtané
A , Geneviève Rioux A , Peter G. C. Campbell A and Claude Fortin A *
+ Author Affiliations
- Author Affiliations
A EcotoQ, Institut national de la recherche scientifique, Centre Eau Terre Environnement, 490 de la Couronne, Québec, QC, G1K 9A9, Canada.
Environmental Chemistry 19(4) 144-155 https://doi.org/10.1071/EN22037
Submitted: 23 April 2022 Accepted: 5 July 2022 Published: 8 September 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing.
Environmental context. The growth in demand for platinum has led to an increase in the presence of this metal in the environment but little is known about its toxicity to aquatic organisms. The presence of organic matter should contribute to decreasing metal bioavailability but the opposite was found for platinum. How ubiquitous natural organic matter can alter the accumulation and effects of platinum group elements remains to be fully elucidated.
Rationale. There is a growing interest for platinum in ecotoxicology, mainly because of its use in automobile exhaust catalysts. When it reaches aquatic ecosystems, platinum can interact with ligands such as natural organic matter. According to the Biotic Ligand Model, the formation of such complexes should reduce metal bioavailability. As a consequence, toxicity should decrease in the presence of organic matter.
Methodology. This study focused on the uptake of platinum by two microalgae species (Chlorella fusca and Chlamydomonas reinhardtii) and its subsequent inhibitory effects on growth (96 h). Cells were exposed to platinum (5–300 µg L−1) at three concentrations (0, 10 and 20 mg C L−1) of standard Suwannee River humic acid (SRHA). Platinum bound to humic acid was determined experimentally using partial ultrafiltration to relate metal uptake and toxicity to speciation.
Results. Unexpectedly, results show that platinum toxicity, expressed as ultrafiltrable Pt (not bound to humic acid) and total Pt concentrations, is enhanced in the presence of humic acid for both algae. For C. fusca, the half maximal effective concentration (EC50) values decreased from 93 to 37 and 35 µg L−1 of ultrafiltrable Pt in the presence of 10 and 20 mg C L−1 SRHA and from 89 to 36 and 0.31 µg L−1 for C. reinhardtii.
Discussion. In contradiction with the Biotic Ligand Model, the results show that the presence of SRHA can significantly and importantly increase platinum uptake and toxicity as determined in two unicellular green algae, C. reinhardtii and C. fusca. The present work raises the issue of the impact of platinum on microalgae under realistic environmental conditions (ubiquitous presence of organic matter), primary producers being of great ecological importance.
Keywords: bioavailability, biotic ligand model, effects, green algae, growth inhibition, metal, natural organic matter, uptake.
References
Adair WS, Snell WJ (1990) The Chlamydomonas reinhardtii cell wall: structure, biochemistry, and molecular biology. In ‘Organization and Assembly of Plant and Animal Extracellular Matrix’. (Eds WS Adair, RP Mecham) pp. 15–84. (Academic Press: San Diego, CA, USA)| Crossref |
Artelt S, Levsen K, König HP, Rosner G (2000) Engine test bench experiments to determine platinum emissions from three-way catalytic converters. In ‘Anthropogenic Platinum-Group Element Emissions: Their Impact on Man and Environment’. (Eds F Zereini, F Alt) pp. 33–44. (Springer: Berlin, Germany)
| Crossref |
Azaroual M, Romand B, Freyssinet P, Disnar JR (2001). Solubility of platinum in aqueous solutions at 25°C and pHs 4 to 10 under oxidizing conditions. Geochimica et Cosmochimica Acta 65, 4453–4466.
| Solubility of platinum in aqueous solutions at 25°C and pHs 4 to 10 under oxidizing conditions.Crossref | GoogleScholarGoogle Scholar |
Azaroual M, Romand B, Freyssinet P, Disnar J-R (2003). Response to the comment by R. H. Byrne on “Solubility of platinum in aqueous solutions at 25°C and pHs 4 to 10 under oxidizing conditions” (2001) Geochim. Cosmochim. Acta 65, 4453–4466. Geochimica et Cosmochimica Acta 67, 2511–2513.
| Response to the comment by R. H. Byrne on “Solubility of platinum in aqueous solutions at 25°C and pHs 4 to 10 under oxidizing conditions” (2001) Geochim. Cosmochim. Acta 65, 4453–4466.Crossref | GoogleScholarGoogle Scholar |
Beckett R, Jue Z, Giddings JC (1987). Determination of molecular weight distributions of fulvic and humic acids using flow field-flow fractionation. Environmental Science & Technology 21, 289–295.
| Determination of molecular weight distributions of fulvic and humic acids using flow field-flow fractionation.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, Le Faucheur S, Fortin C, Campbell PGC (2011). Uptake of lipophilic cadmium complexes by three green algae: influence of humic acid and its pH dependence. Journal of Phycology 47, 784–791.
| Uptake of lipophilic cadmium complexes by three green algae: influence of humic acid and its pH dependence.Crossref | GoogleScholarGoogle Scholar |
Byrne RH (2003). Comment on “Solubility of platinum in aqueous solutions at 25°C and pHs 4 to 10 under oxidizing conditions” by Mohamed Azaroual, Bruno Romand, Philippe Freyssinet, and Jean-Robert Disnar. Geochimica et Cosmochimica Acta 67, 2509
| Comment on “Solubility of platinum in aqueous solutions at 25°C and pHs 4 to 10 under oxidizing conditions” by Mohamed Azaroual, Bruno Romand, Philippe Freyssinet, and Jean-Robert Disnar.Crossref | GoogleScholarGoogle Scholar |
Campbell PGC, Twiss MR, Wilkinson KJ (1997). Accumulation of natural organic matter on the surfaces of living cells: implications for the interaction of toxic solutes with aquatic biota. Canadian Journal of Fisheries and Aquatic Sciences 54, 2543–2554.
| Accumulation of natural organic matter on the surfaces of living cells: implications for the interaction of toxic solutes with aquatic biota.Crossref | GoogleScholarGoogle Scholar |
Chen Z, Porcher C, Campbell PGC, Fortin C (2013). Influence of humic acid on algal uptake and toxicity of ionic silver. Environmental Science & Technology 47, 8835–8842.
| Influence of humic acid on algal uptake and toxicity of ionic silver.Crossref | GoogleScholarGoogle Scholar |
Colombo C, Oates CJ, Monhemius AJ, Plant JA (2008). Complexation of platinum, palladium and rhodium with inorganic ligands in the environment. Geochemistry: Exploration, Environment, Analysis 8, 91–101.
| Complexation of platinum, palladium and rhodium with inorganic ligands in the environment.Crossref | GoogleScholarGoogle Scholar |
Diehl DB, Gagnon ZE (2007). Interactions between essential nutrients with platinum group metals in submerged aquatic and emergent plants. Water, Air, and Soil Pollution 184, 255–267.
| Interactions between essential nutrients with platinum group metals in submerged aquatic and emergent plants.Crossref | GoogleScholarGoogle Scholar |
Dubiella-Jackowska A, Kudłak B, Polkowska Ż, Namieśnik J (2009). Environmental fate of traffic-derived platinum group metals. Critical Reviews in Analytical Chemistry 39, 251–271.
| Environmental fate of traffic-derived platinum group metals.Crossref | GoogleScholarGoogle Scholar |
Erickson R (2015) Toxicity Relationship Analysis Program (TRAP), (U.S. EPA Mid-Continent Ecology Division). Available at https://archive.epa.gov/med/med_archive_03/web/html/trap.html [Verified 19 April 2022]
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 |
Guéguen C, Cuss CW (2011). Characterization of aquatic dissolved organic matter by asymmetrical flow field-flow fractionation coupled to UV-Visible diode array and excitation emission matrix fluorescence. Journal of Chromatography A 1218, 4188–4198.
| Characterization of aquatic dissolved organic matter by asymmetrical flow field-flow fractionation coupled to UV-Visible diode array and excitation emission matrix fluorescence.Crossref | GoogleScholarGoogle Scholar |
Guo L, Santschi PH (2006) Ultrafiltration and its applications to sampling and characterisation of aquatic colloids. In ‘Environmental Colloids and Particles’. (Eds J Buffle, HP van Leeuwen, KJ Wilkinson, JR Lead) pp. 159–221. (John Wiley and Sons: Chichester, UK)
| Crossref |
Hagelüken C, Buchert M, Stahl H (2005) Materials Flow of Platinum Group Metals. GFMS Number 0-9543293-7-6, London. Available at https://www.researchgate.net/publication/270687039_Materials_Flow_of_Platinum_Group_Metals
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 |
Heck RM, Farrauto RJ, Gulati ST (2009) ‘Catalytic Air Pollution Control: Commercial Technology.’ (John Wiley and Sons: Hoboken, NJ, USA)
Her N, Amy G, Foss D, Cho JW (2002). Variations of molecular weight estimation by HP-size exclusion chromatography with UVA versus online DOC detection. Environmental Science & Technology 36, 3393–3399.
| Variations of molecular weight estimation by HP-size exclusion chromatography with UVA versus online DOC detection.Crossref | GoogleScholarGoogle Scholar |
Huang CP, Fofana M, Chan J, Chang CJ, Howell SB (2014). Copper transporter 2 regulates intracellular copper and sensitivity to cisplatin. Metallomics 6, 654–661.
| Copper transporter 2 regulates intracellular copper and sensitivity to cisplatin.Crossref | GoogleScholarGoogle Scholar |
Kochoni E, Doose C, Gonzalez P, Fortin C (2022). Role of iron in gene expression and in the modulation of copper uptake in a freshwater alga: Insights on Cu and Fe assimilation pathways. Environmental Pollution 305, 119311
| Role of iron in gene expression and in the modulation of copper uptake in a freshwater alga: Insights on Cu and Fe assimilation pathways.Crossref | GoogleScholarGoogle Scholar |
Kümmerer K, Helmers E (1997). Hospital effluents as a source for platinum in the environment. Science of the Total Environment 193, 179–184.
| Hospital effluents as a source for platinum in the environment.Crossref | GoogleScholarGoogle Scholar |
Laegreid M, Alstad J, Klaveness D, Seip HM (1983). Seasonal variation of cadmium toxicity toward the alga Selenastrum capricornutum Printz in two lakes with different humus content. Environmental Science & Technology 17, 357–361.
| Seasonal variation of cadmium toxicity toward the alga Selenastrum capricornutum Printz in two lakes with different humus content.Crossref | GoogleScholarGoogle Scholar |
Lamelas C, Wilkinson KJ, Slaveykova VI (2005). Influence of the composition of natural organic matter on Pb bioavailability to microalgae. Environmental Science & Technology 39, 6109–6116.
| Influence of the composition of natural organic matter on Pb bioavailability to microalgae.Crossref | GoogleScholarGoogle Scholar |
Lamelas C, Pinheiro JP, Slaveykova VI (2009). Effect of humic acid on Cd(II), Cu(II), and Pb(II) uptake by freshwater algae: Kinetic and cell wall speciation considerations. Environmental Science & Technology 43, 730–735.
| Effect of humic acid on Cd(II), Cu(II), and Pb(II) uptake by freshwater algae: Kinetic and cell wall speciation considerations.Crossref | GoogleScholarGoogle Scholar |
Lavoie M, Campbell PGC, Fortin C (2012). Extending the biotic ligand model to account for positive and negative feedback interactions between cadmium and zinc in a freshwater alga. Environmental Science & Technology 46, 12129–12136.
| Extending the biotic ligand model to account for positive and negative feedback interactions between cadmium and zinc in a freshwater alga.Crossref | GoogleScholarGoogle Scholar |
Lavoie M, Campbell PGC, Fortin C (2014). Predicting cadmium accumulation and toxicity in a green Alga in the presence of varying essential element concentrations using a Biotic Ligand Model. Environmental Science & Technology 48, 1222–1229.
| Predicting cadmium accumulation and toxicity in a green Alga in the presence of varying essential element concentrations using a Biotic Ligand Model.Crossref | GoogleScholarGoogle Scholar |
Leguay S, Campbell PGC, Fortin C (2016). Determination of the free-ion concentration of rare earth elements by an ion-exchange technique: implementation, evaluation and limits. Environmental Chemistry 13, 478–488.
| Determination of the free-ion concentration of rare earth elements by an ion-exchange technique: implementation, evaluation and limits.Crossref | GoogleScholarGoogle Scholar |
Lenz K, Hann S, Koellensperger G, Stefanka Z, Stingeder G, Weissenbacher N, Mahnik SN, Fuerhacker M (2005). Presence of cancerostatic platinum compounds in hospital wastewater and possible elimination by adsorption to activated sludge. Science of The Total Environment 345, 141–152.
| Presence of cancerostatic platinum compounds in hospital wastewater and possible elimination by adsorption to activated sludge.Crossref | GoogleScholarGoogle Scholar |
Li Y-H, Gregory S (1974). Diffusion of ions in sea water and in deep-sea sediments. Geochimica et Cosmochimica Acta 38, 703–714.
| Diffusion of ions in sea water and in deep-sea sediments.Crossref | GoogleScholarGoogle Scholar |
Loos E, Meindl D (1982). Composition of the cell wall of Chlorella fusca. Planta 156, 270–273.
| Composition of the cell wall of Chlorella fusca.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 |
Macoustra G, Holland A, Stauber J, Jolley DF (2019). Effect of various natural dissolved organic carbon on copper lability and toxicity to the tropical freshwater microalga Chlorella sp. Environmental Science & Technology 53, 2768–2777.
| Effect of various natural dissolved organic carbon on copper lability and toxicity to the tropical freshwater microalga Chlorella sp.Crossref | GoogleScholarGoogle Scholar |
Mebane CA, Chowdhury MJ, De Schamphelaere KAC, Lofts S, Paquin PR, Santore RC, Wood CM (2020). Metal bioavailability models: current status, lessons learned, considerations for regulatory use, and the path forward. Environmental Toxicology and Chemistry 39, 60–84.
| Metal bioavailability models: current status, lessons learned, considerations for regulatory use, and the path forward.Crossref | GoogleScholarGoogle Scholar |
Mueller K, Fortin C, Campbell PGC (2012). Spatial variation in the optical properties of dissolved organic matter (DOM) in lakes on the Canadian Precambrian Shield and links to watershed characteristics. Aquatic Geochemistry 18, 21–44.
| Spatial variation in the optical properties of dissolved organic matter (DOM) in lakes on the Canadian Precambrian Shield and links to watershed characteristics.Crossref | GoogleScholarGoogle Scholar |
Odiyo JO, Bapela HM, Mugwedi R, Chimuka L (2006). Metals in environmental media: a study of trace and platinum group metals in Thohoyandou, South Africa. Water SA 31, 581–588.
| Metals in environmental media: a study of trace and platinum group metals in Thohoyandou, South Africa.Crossref | GoogleScholarGoogle Scholar |
Parent L, Twiss MR, Campbell PGC (1996). Influences of natural dissolved organic matter on the interaction of aluminum with the microalga Chlorella: a test of the free-ion model of trace metal toxicity. Environmental Science & Technology 30, 1713–1720.
| Influences of natural dissolved organic matter on the interaction of aluminum with the microalga Chlorella: a test of the free-ion model of trace metal toxicity.Crossref | GoogleScholarGoogle Scholar |
Rauch S, Peucker-Ehrenbrink B (2015) Sources of platinum group elements in the environment. In ‘Platinum Metals in the Environment’. pp. 3–17. (Springer: Heidelberg, Germany)
Rauch S, Paulsson M, Wilewska M, Blanck H, Morrison GM (2004). Short-term toxicity and binding of platinum to freshwater periphyton communities. Archives of Environmental Contamination and Toxicology 47, 290–296.
| Short-term toxicity and binding of platinum to freshwater periphyton communities.Crossref | GoogleScholarGoogle Scholar |
Roberts K (1974). Crystalline glycoprotein cell walls of algae: their stucture, composition and assembly. Philosophical Transactions of the Royal Society of London. B, Biological Sciences 268, 129–146.
| Crystalline glycoprotein cell walls of algae: their stucture, composition and assembly.Crossref | GoogleScholarGoogle Scholar |
Schecher WD, McAvoy D (2001) MINEQL+: a chemical equilibrium modeling system. Environmental Research Software, Hallowell, ME, USA
Slaveykova VI, Wilkinson KJ, Ceresa A, Pretsch E (2003). Role of fulvic acid on lead bioaccumulation by Chlorella kesslerii. Environmental Science & Technology 37, 1114–1121.
| Role of fulvic acid on lead bioaccumulation by Chlorella kesslerii.Crossref | GoogleScholarGoogle Scholar |
Sures B, Zimmermann S (2007). Impact of humic substances on the aqueous solubility, uptake and bioaccumulation of platinum, palladium and rhodium in exposure studies with Dreissena polymorpha. Environmental Pollution 146, 444–451.
| Impact of humic substances on the aqueous solubility, uptake and bioaccumulation of platinum, palladium and rhodium in exposure studies with Dreissena polymorpha.Crossref | GoogleScholarGoogle Scholar |
Takeda H (1991). Sugar composition of the cell wall and the taxonomy of Chlorella (Chlorophyceae). Journal of Phycology 27, 224–232.
| Sugar composition of the cell wall and the taxonomy of Chlorella (Chlorophyceae).Crossref | GoogleScholarGoogle Scholar |
Thurman EM (1985) Aquatic humic substances. In ‘Organic Geochemistry of Natural Waters’. p. 497. (Martinus Nijhoff/Dr W. Junk Publishers: Boston, MA, USA)
Tipping E (2002) ‘Cation Binding by Humic Substances.’ (Cambridge University Press: Cambridge, UK)
Vigneault B, Percot A, Lafleur M, Campbell PGC (2000). Permeability changes in model and phytoplankton membranes in the presence of aquatic humic substances. Environmental Science & Technology 34, 3907–3913.
| Permeability changes in model and phytoplankton membranes in the presence of aquatic humic substances.Crossref | GoogleScholarGoogle Scholar |
Zereini F, Wiseman CL (2015) ‘Platinum Metals in the Environment.’ (Springer Berlin Heidelberg: Berlin, Germany)
