Abstract
Platinum group element levels have increased in natural aquatic environments in the last few decades, in particular as a consequence of the use of automobile catalytic converters on a global scale. Concentrations of Pt over tens of μg L−1 have been observed in rivers and effluents. This raises questions regarding its possible impacts on aquatic ecosystems, as Pt natural background concentrations are extremely low to undetectable. Primary producers, such as microalgae, are of great ecological importance, as they are at the base of the food web. The purpose of this work was to better understand the impact of Pt on a cellular level for freshwater unicellular algae. Two species with different characteristics, a green alga C. reinhardtii and a diatom N. palea, were studied. The bioaccumulation of Pt as well as its effect on growth were quantified. Moreover, the induction or repression factors of 16 specific genes were determined and allowed for the determination of possible intracellular effects and pathways of Pt. Both species seemed to be experiencing copper deficiency as suggested by inductions of genes linked to copper transporters. This is an indication that Pt might be internalized through the Cu(I) metabolic pathway. Moreover, Pt could possibly be excreted using an efflux pump. Other highlights include a concentration-dependent negative impact of Pt on mitochondrial metabolism for C. reinhardtii which is not observed for N. palea. These findings allowed for a better understanding of some of the possible impacts of Pt on freshwater primary producers, and also lay the foundations for the investigation of pathways for Pt entry at the base of the aquatic food web.
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All data used in this work are available at https://doi.org/10.5683/SP3/I3GMF1.
References
Achard M, Baudrimont M, Boudou A, Bourdineaud J (2004) Induction of a multixenobiotic resistance protein (MXR) in the Asiatic clam Corbicula fluminea after heavy metals exposure. Aqua Toxicol 67:347–357. https://doi.org/10.1016/j.aquatox.2004.01.014
Andolfo G, Ruocco M, Di Donato A, Frusciante L, Lorito M, Scala F, Ercolano MR (2015) Genetic variability and evolutionary diversification of membrane ABC transporters in plants. BMC Plant Biol 15:1–15. https://doi.org/10.1186/s12870-014-0323-2
Artelt, S, Levsen, K, König, H, Rosner, G (2000) Engine test bench experiments to determine platinum emissions from three-way catalytic converters. Anthropogenic platinum-group element emissions. Springer, pp. 33-44. https://doi.org/10.1007/978-3-642-59678-0_4.
Bagmet V, Abdullin SR, Mazina S, Nikulin AY, Nikulin VY, Gontcharov A (2020) Life cycle of Nitzschia palea (Kützing) W. Smith (Bacillariophyta). Russian J Dev Biol 51:106–114. https://doi.org/10.1134/S1062360420020022
Barbante C, Veysseyre A, Ferrari C, Van De Velde K, Morel C, Capodaglio G, Cescon P, Scarponi G, Boutron C (2001) Greenland snow evidence of large scale atmospheric contamination for platinum, palladium, and rhodium. Environ Sci Technol 35:835–839. https://doi.org/10.1021/es000146y
Bard SM (2000) Multixenobiotic resistance as a cellular defense mechanism in aquatic organisms. Aqua Toxicol. 48:357–389. https://doi.org/10.1016/S0166-445X(00)00088-6
Barefoot R (1997) Determination of platinum at trace levels in environmental and biological materials. Environ Sci Technol 31:309–314. https://doi.org/10.1021/es960712i
Bienvenu, T, Meunier, C, Bousquet, S, Chiron, S, Richard, L, Gautheret-Dejean, A, Rouselle, J, Feldmann, D (1999) Les techniques d’extraction de l’ADN à partir d’un échantillon sanguin. Vol. 57. Annales de Biologie Clinique, pp. 77-84
Blaby-Haas CE, Merchant SS (2012) The ins and outs of algal metal transport. Biochimica et Biophysica Acta 1823:1531–1552. https://doi.org/10.1016/j.bbamcr.2012.04.010
Blaby IK, Blaby-Haas CE, Tourasse N, Hom EF, Lopez D, Aksoy M, Grossman A, Umen J, Dutcher S, Porter M, King S, Witman GB, Stanke M, Harris EH, Goodstein D, Grimwood J, Schmutz J, Vallon O, Merchant SS, Prochnik S (2014) The Chlamydomonas genome project: a decade on. Trends Plants 19:672–680. https://doi.org/10.1016/j.tplants.2014.05.008
Bridges CC, Zalups RK (2005) Molecular and ionic mimicry and the transport of toxic metals. Toxicol Appl Pharmacol 204:274–308. https://doi.org/10.1016/j.taap.2004.09.007
Bukhari S, Tahir M, Akhter N, Anjum F, Anwar H, Mustafa G (2018) Phylogeny and comparative modeling of phytochelatin synthase from Chlorella sp. as an efficient bioagent for detoxification of heavy metals. J Biol Regul Homeos Agents 32:1191–1197
Callahan DL, Baker AJ, Kolev SD, Wedd AG (2006) Metal ion ligands in hyperaccumulating plants. J Biol Inorg Chem 11:2–12. https://doi.org/10.1007/s00775-005-0056-7
Campbell PGC, Hare L (2009) Metal detoxification in freshwater animals. Roles of metallothioneins. Metal Ions Life Sci 5:239–277. https://doi.org/10.1515/9783110436273-014
Colombo C, Oates C, Monhemius A, Plant J (2008) Complexation of platinum, palladium and rhodium with inorganic ligands in the environment. Geochem: Explor, Environ, Anal 8:91–101. https://doi.org/10.1144/1467-7873/07-151
Dey S, Mehta N (2020) Automobile pollution control using catalysis. Resources, Environ Sustain 2:100006. https://doi.org/10.1016/j.resenv.2020.100006
Diehl DB, Gagnon ZE (2007) Interactions between essential nutrients with platinum group metals in submerged aquatic and emergent plants. Water, Air, Soil Poll 184:255–267. https://doi.org/10.1007/s11270-007-9414-0
Ely JC, Neal CR, Kulpa CF, Schneegurt MA, Seidler JA, Jain JC (2001) Implications of platinum-group element accumulation along US roads from catalytic-converter attrition. Environ Sci Technol 35:3816–3822. https://doi.org/10.1021/es001989s
Ferreira M, Costa J, Reis-Henriques MA (2014) ABC transporters in fish species: a review. Front Physiol 5:266. https://doi.org/10.3389/fphys.2014.00266
Glaeser H, Coblenz A, Kruczek R, Ruttke I, Ebert-Jung A, Wolf K (1991) Glutathione metabolism and heavy metal detoxification in Schizosaccharomyces pombe. Curr Genet 19:207–213. https://doi.org/10.1007/bf00336488
Gonzalez P, Baudrimont M, Boudou A, Bourdineaud J-P (2006) Comparative effects of direct cadmium contamination on gene expression in gills, liver, skeletal muscles and brain of the zebrafish (Danio rerio). Biometals 19:225–235. https://doi.org/10.1007/s10534-005-5670-x
Harris, EH (2008) The Chlamydomonas sourcebook: introduction to Chlamydomonas and its laboratory use. Academic Press.
Hassler CS, Slaveykova VI, Wilkinson KJ (2004) Discriminating between intra‐and extracellular metals using chemical extractions. Limnol Oceanogr: Methods 2:237–247. https://doi.org/10.4319/lom.2004.2.237
Hillebrand H, Dürselen CD, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424. https://doi.org/10.1046/j.1529-8817.1999.3520403.x
Hoagland KD, Rosowski JR, Gretz MR, Roemer SC (1993) Diatom extracellular polymeric substances: function, fine structure, chemistry, and physiology. J Phycol 29:537–566. https://doi.org/10.1111/j.0022-3646.1993.00537.x
Holt KB, Bard AJ (2005) Interaction of silver (I) ions with the respiratory chain of Escherichia coli: an electrochemical and scanning electrochemical microscopy study of the antimicrobial mechanism of micromolar Ag+. Biochemistry 44:13214–13223. https://doi.org/10.1021/bi0508542
Hourtané O, Rioux G, Campbell PG, Fortin C (2022) Algal bioaccumulation and toxicity of platinum are increased in the presence of humic acids. Environ Chem 19(4):144–155. https://doi.org/10.1071/EN22037
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. https://doi.org/10.1039/c3mt00331k
Jakupec MA, Galanski M, Keppler BK (2003) Tumour-inhibiting platinum complexes–state of the art and future perspectives. Rev Physiol, Biochem Pharmacol 146:1–54. https://doi.org/10.1007/s10254-002-0001-x
Kim H, Yim B, Kim J, Kim H, Lee Y-M (2017) Molecular characterization of ABC transporters in marine ciliate, Euplotes crassus: Identification and response to cadmium and benzo [a] pyrene. Marine Poll Bull 124:725–735. https://doi.org/10.1016/j.marpolbul.2017.01.046
Kim Tiam S, Feurtet-Mazel A, Delmas F, Mazzella N, Morin S, Daffe G, Gonzalez P (2012) Development of q-PCR approaches to assess water quality: effects of cadmium on gene expression of the diatom Eolimna minima. Water Res 46:934–942. https://doi.org/10.1016/j.watres.2011.11.005
Kim Tiam, S, Lavoie, I, Doose, C, Hamilton, PB, Fortin, C (2018) Morphological, physiological and molecular responses of Nitzschia palea under cadmium stress. Ecotoxicology. https://doi.org/10.1007/s10646-018-1945-1
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. Environ Poll 305:119311. https://doi.org/10.1016/j.envpol.2022.119311
Kociolek, P (2011) Nitzschia palea. Diatoms of North America. https://diatoms.org/species/nitzschia_palea Accessed 21 August 2023
Lavoie M, Campbell PG, 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. Environ Sci Technol 48:1222–1229. https://doi.org/10.1021/es402630z
Lavoie M, Le Faucheur S, Fortin C, Campbell PG (2009) Cadmium detoxification strategies in two phytoplankton species: metal binding by newly synthesized thiolated peptides and metal sequestration in granules. Aqua Toxicol 92:65–75. https://doi.org/10.1016/j.aquatox.2008.12.007
Lee JG, Ahner BA, Morel FM (1996) Export of cadmium and phytochelatin by the marine diatom Thalassiosira weissflogii. Environ Sci Technol 30:1814–1821. https://doi.org/10.1021/es950331p
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. Sci Tot Environ 345:141–152. https://doi.org/10.1016/j.scitotenv.2004.11.007
Li T, Lin X, Yu L, Lin S, Rodriguez IB, Ho T-Y (2020) RNA-seq profiling of Fugacium kawagutii reveals strong responses in metabolic processes and symbiosis potential to deficiencies of iron and other trace metals. Sci Tot Environ 705:135767. https://doi.org/10.1016/j.scitotenv.2019.135767
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernandez E, Fukuzawa H, Gonzalez-Ballester D, Gonzalez-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riano-Pachon DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martinez D, Ngau WC, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS, Grossman AR (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245–250. https://doi.org/10.1126/science.1143609
Moisset, S, Kim Tiam, S, Feurtet-Mazel, A, Morin, S, Delmas, F, Mazzella, N, Gonzalez, P (2015) Genetic and physiological responses of three freshwater diatoms to realistic diuron exposures. Environ Sci Poll Res 4046–4055. https://doi.org/10.1007/s11356-014-3523-2
Moldovan M, Rauch S, Gómez M, Antonia Palacios M, Morrison GM (2001) Bioaccumulation of palladium, platinum and rhodium from urban particulates and sediments by the freshwater isopod Asellus aquaticus. Water Res 35:4175–4183. https://doi.org/10.1016/S0043-1354(01)00136-1
Morton O, Puchelt H, Hernández E, Lounejeva E (2001) Traffic-related platinum group elements (PGE) in soils from Mexico City. J Geochem Explor 72:223–227. https://doi.org/10.1016/S0375-6742(01)00163-7
Nowicka B (2022) Heavy metal–induced stress in eukaryotic algae—mechanisms of heavy metal toxicity and tolerance with particular emphasis on oxidative stress in exposed cells and the role of antioxidant response. Environ Sci Poll Res 29:16860–16911. https://doi.org/10.1007/s11356-021-18419-w
Odiyo JO, Bapela HM, Mugwedi R, Chimuka L (2005) Metals in environmental media: A study of trace and platinum group metals in Thohoyandou, South Africa. Water SA 31:581-588. https://doi.org/10.4314/wsa.v31i4.5148
Osborn HL, Hook SE (2013) Using transcriptomic profiles in the diatom Phaeodactylum tricornutum to identify and prioritize stressors. Aqua Toxicol 138:12–25. https://doi.org/10.1016/j.aquatox.2013.04.002
Palacios MA, Gómez MM, Moldovan M, Morrison G, Rauch S, McLeod C, Ma R, Laserna J, Lucena P, Caroli S, Alimonti A, Petrucci F, Bocca B, Schramel P, Lustig S, Zischka M, Wass U, Stenbom B, Luna M, Saenz JC, Santamarı́a J, Torrens JM (2000) Platinum-group elements: quantification in collected exhaust fumes and studies of catalyst surfaces. Sci Tot Environ 257:1–15. https://doi.org/10.1016/S0048-9697(00)00464-2
Paolucci C, Ponti J, Fabbri M, Breda D, Sabbioni E, Burastero S (2007) Platinum group elements enhance the allergic immune response by acting on dendritic cells. Allerg Immunol 143:225–236. https://doi.org/10.1159/000099466
Pearson, RG (1993) Chemical hardness—A historical introduction. Chemical hardness. Springer, pp. 1-10. https://doi.org/10.1007/BFb0036796
Pearson, SA, Cowan, J (2021) Glutathione-coordinated metal complexes as substrates for cellular transporters. Metallomics. 13. https://doi.org/10.1093/mtomcs/mfab015
Rauch S, Morrison GM (1999) Platinum uptake by the freshwater isopod Asellus aquaticus in urban rivers. Sci Tot Environ 235:261–268. https://doi.org/10.1016/S0048-9697(99)00203-X
Rauch S, Paulsson M, Wilewska M, Blanck H, Morrison GM (2004) Short-term toxicity and binding of platinum to freshwater periphyton communities. Arch Environ Contamination Toxicol 47:290–296. https://doi.org/10.1007/s00244-004-3197-8
Ravindra K, Bencs L, Van Grieken R (2004) Platinum group elements in the environment and their health risk. Sci Tot Environ 318:1–43. https://doi.org/10.1016/s0048-9697(03)00372-3
Reedijk J (2016) Metal-ion nucleic-acid interactions: A personal account. Inorganica Chimica Acta 452:268–272. https://doi.org/10.1016/j.ica.2015.12.011
Shi B, Huang Z, Xiang X, Huang M, Wang W-X, Ke C (2015) Transcriptome analysis of the key role of GAT2 gene in the hyper-accumulation of copper in the oyster Crassostrea angulata. Scientific Rep 5:17751. https://doi.org/10.1038/srep17751
Sies H (1986) Biochemistry of Oxidative Stress. Angewandte Chemie International Edition in English 25:1058–1071. https://doi.org/10.1002/anie.198610581
Soyol-Erdene TO, Huh Y, Hong S, Hur SD (2011) A 50-year record of platinum, iridium, and rhodium in Antarctic snow: volcanic and anthropogenic sources. Environ Sci Technol 45:5929–5935. https://doi.org/10.1021/es2005732
Sprowl JA, Ness RA, Sparreboom A (2013) Polymorphic transporters and platinum pharmacodynamics. Drug metabolism and pharmacokinetics 28:19–27. https://doi.org/10.2133/dmpk.DMPK-12-RV-073
Sunda WG, Huntsman SA (1998) Processes regulating cellular metal accumulation and physiological effects: phytoplankton as model systems. Sci Tot Environ 219:165–181. https://doi.org/10.1016/S0048-9697(98)00226-5
Sures B, Thielen F, Baska F, Messerschmidt J, von Bohlen A (2005) The intestinal parasite Pomphorhynchus laevis as a sensitive accumulation indicator for the platinum group metals Pt, Pd, and Rh. Environ Res 98:83–88. https://doi.org/10.1016/j.envres.2004.05.010
Vannini C, Domingo G, Marsoni M, Fumagalli A, Terzaghi R, Labra M, De Mattia F, Onelli E, Bracale M (2011) Physiological and molecular effects associated with palladium treatment in Pseudokirchneriella subcapitata. Aqua Toxicol 102:104–113. https://doi.org/10.1016/j.aquatox.2011.01.002
Windler M, Bova D, Kryvenda A, Straile D, Gruber A, Kroth PG (2014) Influence of bacteria on cell size development and morphology of cultivated diatoms. Phycol Res 62:269–281. https://doi.org/10.1111/pre.12059
Wortelboer HM, Balvers MG, Usta M, van Bladeren PJ, Cnubben NH (2008) Glutathione-dependent interaction of heavy metal compounds with multidrug resistance proteins MRP1 and MRP2. Environ Toxicol Pharmacol 26:102–108. https://doi.org/10.1016/j.etap.2008.02.006
Yan A, Chen Z (2019) Impacts of silver nanoparticles on plants: a focus on the phytotoxicity and underlying mechanism. Int J Mol Sci 20:1003. https://doi.org/10.3390/ijms20051003
Zimmermann S, Wolff C, Sures B (2017) Toxicity of platinum, palladium and rhodium to Daphnia magna in single and binary metal exposure experiments. Environ Poll 224:368–376. https://doi.org/10.1016/j.envpol.2017.02.016
Acknowledgements
This work has been carried out with the financial support of the Natural Sciences and Engineering Research Council of Canada, Strategic project grant number STPGP 521467 – 18 entitled “Terrestrial-aquatic mobility of technology critical elements in a changing Canadian environment (TAMTeC) in collaboration with Environment and Climate Change Canada (project number GCXE17S011). O. Hourtané was supported by an EcotoQ scholarship (FRQNT strategic network grant 309016). The authors would like to thank the Functional Ecology & Environment Lab (LEFE UMR 5245 CNRS/INPT/UPS) of ENSAT (Ecole Nationale Supérieure Agronomique de Toulouse), France, which sequenced the complete genome of the diatom N. palea and allowed us to use it in collaboration. We would also like to thank Pierre-Yves Gourves for the GFAAS analysis, Julie Perreault for technical support in the use of ICP-MS, Vincent Laderriere for performing mineralization tests on diatoms, Jean-Paul Maalouf for his advice on statistical analyses and Scott Hepditch for language assistance in the preparation of this manuscript.
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Claude Fortin, Patrice Gonzalez, and Agnès Feurtet-Mazel contributed to the study conception and design as well as supervision. Material preparation, data collection and analysis were performed by Océane Hourtané and Emeric Kochoni. The first draft of the manuscript was written by Océane Hourtané and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Hourtané, O., Gonzalez, P., Feurtet-Mazel, A. et al. Potential cellular targets of platinum in the freshwater microalgae Chlamydomonas reinhardtii and Nitzschia palea revealed by transcriptomics. Ecotoxicology 33, 281–295 (2024). https://doi.org/10.1007/s10646-024-02746-y
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DOI: https://doi.org/10.1007/s10646-024-02746-y