Copper uptake, intracellular localization, and speciation in marine microalgae measured by synchrotron radiation X-ray fluorescence and absorption microspectroscopy

Adams, Merrin S.; Dillon, Carolyn T.; Vogt, Stefan; Lai, Barry; Stauber, Jennifer; Jolley, Dianne F.

doi:10.1021/acs.est.6b00861

Title: Copper uptake, intracellular localization, and speciation in marine microalgae measured by synchrotron radiation X-ray fluorescence and absorption microspectroscopy

Journal Article · Wed Jul 20 00:00:00 EDT 2016 · Environmental Science and Technology

DOI:https://doi.org/10.1021/acs.est.6b00861· OSTI ID:1332944

Adams, Merrin S. ^[1]; Dillon, Carolyn T. ^[2]; Vogt, Stefan ^[3]; Lai, Barry ^[3]; Stauber, Jennifer ^[4]; Jolley, Dianne F. ^[2]

CSIRO Land and Water Flagship, Kirrawee, NSW (Australia); Univ. of Wollongong, Wollongong, NSW (Australia)
Univ. of Wollongong, Wollongong, NSW (Australia)
Argonne National Lab. (ANL), Argonne, IL (United States)
CSIRO Land and Water Flagship, Kirrawee, NSW (Australia)

Metal toxicity to aquatic organisms depends on the speciation of the metal and its binding to the critical receptor site(s) (biotic ligand) of the organism. The intracellular nature of the biotic ligand for Cu in microalgal cells was investigated using the high elemental sensitivity of microprobe synchrotron radiation X-ray fluorescence (SR-XRF) and X-ray absorption near-edge spectroscopy (XANES). The marine microalgae, Ceratoneis closterium, Phaeodactylum tricornutum, and Tetraselmis sp. were selected based on their varying sensitivities to Cu (72-h 50% population growth inhibitions of 8–47 μg Cu/L). Intracellular Cu in control cells was similar for all three species (2.5–3.2 × 10–15 g Cu/cell) and increased 4-fold in C. closterium and Tetraselmis sp. when exposed to copper, but was unchanged in P. tricornutum (72-h exposure to 19, 40, and 40 μg Cu/L, respectively). Whole cell microprobe SR-XRF identified endogenous Cu in the central compartment (cytoplasm) of control (unexposed) cells. After Cu exposure, Cu was colocated with organelles/granules dense in P, S, Ca, and Si and this was clearly evident in thin sections of Tetraselmis sp. XANES indicated coexistence of Cu(I) and Cu(II) in control and Cu-exposed cells, with the Cu ligand (e.g., phytochelatin) in P. tricornutum different from that in C. closterium and Tetraselmis sp. Here, this study supports the hypothesis that Cu(II) is reduced to Cu(I) and that polyphosphate bodies and phytochelatins play a significant role in the internalization and detoxification of Cu in marine microalgae.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1332944

Journal Information:: Environmental Science and Technology, Vol. 50, Issue 16; ISSN 0013-936X

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 39 works

Citation information provided by
Web of Science

References (57)

Binding of Nickel and Copper to Fish Gills Predicts Toxicity When Water Hardness Varies, But Free-Ion Activity Does Not Meyer, Joseph S.; Santore, Robert C.; Bobbitt, Joe P. Environmental Science & Technology, Vol. 33, Issue 6 https://doi.org/10.1021/es980715q	journal	March 1999
Predicting the Bioavailability of Metals and Metal Complexes: Critical Review of the Biotic Ligand Model Slaveykova, Vera I.; Wilkinson, Kevin J. Environmental Chemistry, Vol. 2, Issue 1 https://doi.org/10.1071/EN04076	journal	January 2005
Sensitivity of marine microalgae to copper: The effect of biotic factors on copper adsorption and toxicity Levy, Jacqueline L.; Stauber, Jennifer L.; Jolley, Dianne F. Science of The Total Environment, Vol. 387, Issue 1-3 https://doi.org/10.1016/j.scitotenv.2007.07.016	journal	November 2007
Uptake and internalisation of copper by three marine microalgae: Comparison of copper-sensitive and copper-tolerant species Levy, J.; Angel, B.; Stauber, J. Aquatic Toxicology, Vol. 89, Issue 2 https://doi.org/10.1016/j.aquatox.2008.06.003	journal	August 2008
Copper-induced changes in intracellular thiols in two marine diatoms: Phaeodactylum tricornutum and Ceratoneis closterium Smith, Cassandra L.; Steele, Jessica E.; Stauber, Jennifer L. Aquatic Toxicology, Vol. 156 https://doi.org/10.1016/j.aquatox.2014.08.010	journal	November 2014
Predicting Copper Toxicity with Its Intracellular or Subcellular Concentration and the Thiol Synthesis in a Marine Diatom Miao, Ai-Jun; Wang, Wen-Xiong Environmental Science & Technology, Vol. 41, Issue 5 https://doi.org/10.1021/es0613963	journal	March 2007
Reversibility of copper-thiol binding in Nitzschia closterium and Chlorella pyrenoidosa Stauber, J. L.; Florence, T. M. Aquatic Toxicology, Vol. 8, Issue 4 https://doi.org/10.1016/0166-445X(86)90074-3	journal	September 1986
Mechanism of toxicity of ionic copper and copper complexes to algae Stauber, J. L.; Florence, T. M. Marine Biology, Vol. 94, Issue 4 https://doi.org/10.1007/BF00431397	journal	January 1987
The use of immobilised metal affinity chromatography (IMAC) to compare expression of copper-binding proteins in control and copper-exposed marine microalgae Smith, Cassandra L.; Stauber, Jennifer L.; Wilson, Mark R. Analytical and Bioanalytical Chemistry, Vol. 406, Issue 1 https://doi.org/10.1007/s00216-013-7452-6	journal	November 2013
Hard X-ray microprobe studies of chromium(VI)-treated V79 Chinese hamster lung cells: intracellular mapping of the biotransformation products of a chromium carcinogen Dillon, Carolyn T.; Lay, Peter A.; Kennedy, Brendan J. JBIC Journal of Biological Inorganic Chemistry, Vol. 7, Issue 6 https://doi.org/10.1007/s00775-002-0343-5	journal	February 2002
Intracellular mapping of the distribution of metals derived from the antitumor metallocenes Waern, Jenny B.; Harris, Hugh H.; Lai, Barry JBIC Journal of Biological Inorganic Chemistry, Vol. 10, Issue 5 https://doi.org/10.1007/s00775-005-0649-1	journal	May 2005
Microprobe XRF Mapping and XAS Investigations of the Intracellular Metabolism of Arsenic for Understanding Arsenic-Induced Toxicity Munro, Kristie L.; Mariana, Anna; Klavins, Andrejs I. Chemical Research in Toxicology, Vol. 21, Issue 9 https://doi.org/10.1021/tx800128d	journal	September 2008
Does cytotoxicity of metallointercalators correlate with cellular uptake or DNA affinity? Davis, Kimberley J.; Carrall, Judith A.; Lai, Barry Dalton Transactions, Vol. 41, Issue 31 https://doi.org/10.1039/c2dt30217a	journal	January 2012
Quantifying Trace Elements in Individual Aquatic Protist Cells with a Synchrotron X-ray Fluorescence Microprobe Twining, Benjamin S.; Baines, Stephen B.; Fisher, Nicholas S. Analytical Chemistry, Vol. 75, Issue 15 https://doi.org/10.1021/ac034227z	journal	August 2003
Exploring Ocean Biogeochemistry by Single-Cell Microprobe Analysis of Protist Elemental Composition Twining, Benjamin S.; Baines, Stephen B.; Vogt, Stefan Journal of Eukaryotic Microbiology, Vol. 55, Issue 3 https://doi.org/10.1111/j.1550-7408.2008.00320.x	journal	May 2008
Characterization of phosphorus, calcium, iron, and other elements in organisms at sub-micron resolution using X-ray fluorescence spectromicroscopy: X-ray spectromicroscopy of organisms Diaz, Julia; Ingall, Ellery; Vogt, Stefan Limnology and Oceanography: Methods, Vol. 7, Issue 1 https://doi.org/10.4319/lom.2009.7.42	journal	January 2009
REINSTATEMENT OF THE GENUS CERATONEIS EHRENBERG AND LECTOTYPIFICATION OF ITS TYPE SPECIMEN: C. CLOSTERIUM EHRENBERG Jahn, Regine; Kusber, Wolf-Henning Diatom Research, Vol. 20, Issue 2 https://doi.org/10.1080/0269249X.2005.9705638	journal	November 2005
Studies of Marine Planktonic Diatoms: i. Cyclotella nana Hustedt, and Detonula Confervacea (Cleve) Gran. Guillard, Robert R. L.; Ryther, John H. Canadian Journal of Microbiology, Vol. 8, Issue 2 https://doi.org/10.1139/m62-029	journal	April 1962
Relationship between ultrastructural changes and EROD activities in liver of fish exposed to Benzo[a]pyrene Au, D. W. T.; Wu, R. S. S.; Zhou, B. S. Environmental Pollution, Vol. 104, Issue 2 https://doi.org/10.1016/S0269-7491(98)00176-6	journal	February 1999
MAPS : A set of software tools for analysis and visualization of 3D X-ray fluorescence data sets Vogt, S. Journal de Physique IV (Proceedings), Vol. 104 https://doi.org/10.1051/jp4:20030160	journal	March 2003
Use and limitations of microbial bioassays for assessing copper bioavailability in the aquatic environment Stauber, J. L.; Davies, C. M. Environmental Reviews, Vol. 8, Issue 4 https://doi.org/10.1139/a00-010	journal	April 2000
Copper and zinc tolerance of two tropical microalgae after copper acclimation Johnson, Hilary L.; Stauber, Jenny L.; Adams, Merrin S. Environmental Toxicology, Vol. 22, Issue 3 https://doi.org/10.1002/tox.20265	journal	January 2007
Development of flow cytometry-based algal bioassays for assessing toxicity of copper in natural waters Franklin, Natasha M.; Stauber, Jennifer L.; Lim, Richard P. Environmental Toxicology and Chemistry, Vol. 20, Issue 1 https://doi.org/10.1002/etc.5620200118	journal	January 2001
Metal bioavailability to phytoplankton—applicability of the biotic ligand model Campbell, Peter G. C.; Errécalde, Olivier; Fortin, Claude Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, Vol. 133, Issue 1-2 https://doi.org/10.1016/S1532-0456(02)00104-7	journal	September 2002
Bioavailability of trace metals to aquatic microorganisms: importance of chemical, biological and physical processes on biouptake Worms, I.; Simon, D. F.; Hassler, C. S. Biochimie, Vol. 88, Issue 11 https://doi.org/10.1016/j.biochi.2006.09.008	journal	November 2006
Influence of N -2-hydroxyethylpiperazine- N ′-2-ethanesulfonic acid pH buffer on the biological response of marine algae Vasconcelos, M. Teresa S. D.; Leal, Maria Fernanda C. Environmental Toxicology and Chemistry, Vol. 21, Issue 2 https://doi.org/10.1002/etc.5620210225	journal	February 2002
Effect of Pseudokirchneriella subcapitata (Chlorophyceae) exudates on metal toxicity and colloid aggregation Koukal, Brahim; Rossé, Patrick; Reinhardt, Alain Water Research, Vol. 41, Issue 1 https://doi.org/10.1016/j.watres.2006.09.014	journal	January 2007
Significance of physicochemical forms of storage in microalgae in predicting copper transfer to filter-feeding oysters (Crassostrea gigas) Amiard-Triquet, Claude; Berthet, Brigitte; Joux, Lamia Environmental Toxicology, Vol. 21, Issue 1 https://doi.org/10.1002/tox.20149	journal	January 2006
Processes regulating cellular metal accumulation and physiological effects: Phytoplankton as model systems Sunda, William G.; Huntsman, Susan A. Science of The Total Environment, Vol. 219, Issue 2-3 https://doi.org/10.1016/S0048-9697(98)00226-5	journal	August 1998
Copper-induced changes of non-protein thiols and antioxidant enzymes in the marine microalga Phaeodactylum tricornutum Morelli, Elisabetta; Scarano, Gioacchino Plant Science, Vol. 167, Issue 2 https://doi.org/10.1016/j.plantsci.2004.04.001	journal	August 2004
Effects of Metal Combinations on the Production of Phytochelatins and Glutathione by the Marine Diatom Phaeodactylum tricornutum Kawakami, Silvia K.; Gledhill, Martha; Achterberg, Eric P. BioMetals, Vol. 19, Issue 1 https://doi.org/10.1007/s10534-005-5115-6	journal	February 2006
Phytochelatin Induction, Cadmium Accumulation, and Algal Sensitivity to free Cadmium ion in Scenedesmus Vacuolatus Le Faucheur, Séverine; Behra, Renata; Sigg, Laura Environmental Toxicology and Chemistry, Vol. 24, Issue 7 https://doi.org/10.1897/04-394R.1	journal	January 2005
Thiols in Scenedesmus vacuolatus upon exposure to metals and metalloids Le Faucheur, Séverine; Schildknecht, Fabian; Behra, Renata Aquatic Toxicology, Vol. 80, Issue 4 https://doi.org/10.1016/j.aquatox.2006.10.002	journal	December 2006
A phytochelatin-based bioassay in marine diatoms useful for the assessment of bioavailability of heavy metals released by polluted sediments Morelli, Elisabetta; Marangi, Maria Luisa; Fantozzi, Laura Environment International, Vol. 35, Issue 3 https://doi.org/10.1016/j.envint.2008.09.012	journal	April 2009
Heavy Metal-Induced Oxidative Stress in Algae1 Pinto, Ernani; Sigaud-kutner, Teresa C. S.; Leitao, Maria A. S. Journal of Phycology, Vol. 39, Issue 6 https://doi.org/10.1111/j.0022-3646.2003.02-193.x	journal	December 2003
Oxidative stress and antioxidant defenses in two green microalgae exposed to copper Sabatini, Sebastián E.; Juárez, Ángela B.; Eppis, Maria R. Ecotoxicology and Environmental Safety, Vol. 72, Issue 4 https://doi.org/10.1016/j.ecoenv.2009.01.003	journal	May 2009
Why Is Metal Bioaccumulation So Variable? Biodynamics as a Unifying Concept Luoma, Samuel N.; Rainbow, Philip S. Environmental Science & Technology, Vol. 39, Issue 7 https://doi.org/10.1021/es048947e	journal	April 2005
Copper Immobilization in Fouling Diatoms Daniel, G. F.; Chamberlain, A. H. L. Botanica Marina, Vol. 24, Issue 4 https://doi.org/10.1515/botm.1981.24.4.229	journal	January 1981
Uptake of heavy metals by Plectonema boryanum (cyanophyceae) into cellular components, especially polyphosphate bodies: An X-ray energy dispersive study Jensen, Thomas E.; Baxter, Mike; Rachlin, Joseph W. Environmental Pollution Series A, Ecological and Biological, Vol. 27, Issue 2 https://doi.org/10.1016/0143-1471(82)90104-0	journal	February 1982
Copper resistance in Anabaena variabilis: Effects of phosphate nutrition and polyphosphate bodies Hashemi, F.; Leppard, G. G.; Kushnert, D. J. Microbial Ecology, Vol. 27, Issue 2 https://doi.org/10.1007/BF00165815	journal	January 1994
Influence of Phosphorus Nutrition on Copper Toxicity to Three Strains of Scenedesmus Acutus (Chlorophyceae)1 Twiss, Michael R.; Nalewajko, Czeslawa Journal of Phycology, Vol. 28, Issue 3 https://doi.org/10.1111/j.0022-3646.1992.00291.x	journal	June 1992
Cysteine Enhances Bioavailability of Copper to Marine Phytoplankton Walsh, Michael J.; Goodnow, Sarah D.; Vezeau, Grace E. Environmental Science & Technology, Vol. 49, Issue 20 https://doi.org/10.1021/acs.est.5b02112	journal	September 2015
Response of the phytoplanctonic alga Tetraselmis suecica to copper and silver exposure: vesicular metal bioaccumulation and lack of starch bodies Ballan-Dufrançais, Christiane; Marcaillou, Christiane; Amiard-Triquet, Claude Biology of the Cell, Vol. 72, Issue 1-2 https://doi.org/10.1016/0248-4900(91)90084-Z	journal	January 1991
The rise of ROS Scandalios, John G. Trends in Biochemical Sciences, Vol. 27, Issue 9 https://doi.org/10.1016/S0968-0004(02)02170-9	journal	September 2002
Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants Mendoza-Cózatl, David; Loza-Tavera, Herminia; Hernández-Navarro, Andrea FEMS Microbiology Reviews, Vol. 29, Issue 4 https://doi.org/10.1016/j.femsre.2004.09.004	journal	September 2005
Heavy metals toxicity in plants: An overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants Yadav, S. K. South African Journal of Botany, Vol. 76, Issue 2 https://doi.org/10.1016/j.sajb.2009.10.007	journal	April 2010
Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple Schafer, Freya Q.; Buettner, Garry R. Free Radical Biology and Medicine, Vol. 30, Issue 11 https://doi.org/10.1016/S0891-5849(01)00480-4	journal	June 2001
Analysis of Glutathione Endpoints for Measuring Copper Stress in Chlamydomonas Reinhardtii Stoiber, Tasha L.; Shafer, Martin M.; Perkins, Dawn A. Karner Environmental Toxicology and Chemistry, Vol. 26, Issue 8 https://doi.org/10.1897/06-534R.1	journal	January 2007
Reactive oxygen species: response of algal cells Mallick, Nirupama; Mohn, Friedrich Helmuth Journal of Plant Physiology, Vol. 157, Issue 2 https://doi.org/10.1016/S0176-1617(00)80189-3	journal	August 2000
Phytochelatins: The Principal Heavy-Metal Complexing Peptides of Higher Plants Grill, E.; Winnacker, E. -L.; Zenk, M. H. Science, Vol. 230, Issue 4726 https://doi.org/10.1126/science.230.4726.674	journal	November 1985
P HYTOCHELATINS AND M ETALLOTHIONEINS : Roles in Heavy Metal Detoxification and Homeostasis Cobbett, Christopher; Goldsbrough, Peter Annual Review of Plant Biology, Vol. 53, Issue 1 https://doi.org/10.1146/annurev.arplant.53.100301.135154	journal	June 2002
The Heavy Metal-Binding Peptides of Plants Steffens, J. C. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 41, Issue 1 https://doi.org/10.1146/annurev.pp.41.060190.003005	journal	June 1990
Cadmium sequestration in Chlamydomonas reinhardtii Hu, Shengxi; Lau, Ken W. K.; Wu, Madeline Plant Science, Vol. 161, Issue 5 https://doi.org/10.1016/S0168-9452(01)00501-5	journal	October 2001
Synthesis and stability of phytochelatins induced by cadmium and lead in the marine diatom Phaeodactylum tricornutum Morelli, E.; Scarano, G. Marine Environmental Research, Vol. 52, Issue 4 https://doi.org/10.1016/S0141-1136(01)00093-9	journal	October 2001
Copper K-edge XANES of Cu(I) and Cu(II) oxide mixtures Gaur, A.; Shrivastava, B. D.; Joshi, S. K. Journal of Physics: Conference Series, Vol. 190 https://doi.org/10.1088/1742-6596/190/1/012084	journal	November 2009
Synthesis and structural analysis of copper(II) cysteine complexes Dokken, Kenneth M.; Parsons, Jason G.; McClure, John Inorganica Chimica Acta, Vol. 362, Issue 2 https://doi.org/10.1016/j.ica.2008.04.037	journal	January 2009
Speciation of copper in a range of food types by X-ray absorption spectroscopy Ceko, Melanie J.; Aitken, Jade B.; Harris, Hugh H. Food Chemistry, Vol. 164 https://doi.org/10.1016/j.foodchem.2014.05.018	journal	December 2014

Cited By (7)

Physiological and metabolic responses of Scenedesmus quadricauda (Chlorophyceae) to nickel toxicity and warming Yong, Wai-Kuan; Sim, Kae-Shin; Poong, Sze-Wan 3 Biotech, Vol. 9, Issue 8 https://doi.org/10.1007/s13205-019-1848-8	journal	July 2019
Effects of LaCoO ₃ perovskite nanoparticle on Daphnia magna : accumulation, distribution and biomarker responses Zhou, Tingting; Zhang, Lili; Wang, Ying RSC Advances, Vol. 9, Issue 42 https://doi.org/10.1039/c9ra03513c	journal	January 2019
Environmental Concentrations of Copper, Alone or in Mixture With Arsenic, Can Impact River Sediment Microbial Community Structure and Functions Mahamoud Ahmed, Ayanleh; Lyautey, Emilie; Bonnineau, Chloé Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01852	journal	August 2018
Pyrenoidal sequestration of cadmium impairs carbon dioxide fixation in a microalga Penen, Florent; Isaure, Marie‐Pierre; Dobritzsch, Dirk Plant, Cell & Environment, Vol. 43, Issue 2 https://doi.org/10.1111/pce.13674	journal	November 2019
Experimental Warming Differentially Influences the Vulnerability of Phototrophic and Heterotrophic Periphytic Communities to Copper Toxicity Pesce, Stéphane; Lambert, Anne-Sophie; Morin, Soizic Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01424	journal	July 2018
Functional CTR-type Cu(I) transporters in an oceanic diatom: CTR-type Cu(I) transporters in an oceanic diatom Kong, Liangliang; Price, Neil M. Environmental Microbiology, Vol. 21, Issue 1 https://doi.org/10.1111/1462-2920.14428	journal	October 2018
Toxicity, Physiological, and Ultrastructural Effects of Arsenic and Cadmium on the Extremophilic Microalga Chlamydomonas acidophila Díaz, Silvia; De Francisco, Patricia; Olsson, Sanna International Journal of Environmental Research and Public Health, Vol. 17, Issue 5 https://doi.org/10.3390/ijerph17051650	journal	March 2020

Similar Records

Host selection and stochastic effects influence bacterial community assembly on the microalgal phycosphere

Journal Article · Sat Jun 01 00:00:00 EDT 2019 · Algal Research · OSTI ID:1332944

Kimbrel, Jeffrey A.; Samo, Ty J.; Ward, Christopher; +6 more

DISCOVR Strain Screening Pipeline - Part III: Strain Evaluation in Outdoor Raceway Ponds

Journal Article · Tue Jan 31 00:00:00 EST 2023 · Algal Research · OSTI ID:1332944

Gao, Song; Edmundson, Scott; Huesemann, Michael; +5 more

DISCOVR strain screening pipeline – Part III: Strain evaluation in outdoor raceway ponds

Journal Article · Wed Mar 01 00:00:00 EST 2023 · Algal Research · OSTI ID:1332944

Gao, Song; Edmundson, Scott; Huesemann, Michael; +5 more

Related Subjects

54 ENVIRONMENTAL SCIENCES
Nitzschia closterium
SR-XRF
XANES
glutathione
phytochelatins
phytoplankton
polyphosphate

Title: Copper uptake, intracellular localization, and speciation in marine microalgae measured by synchrotron radiation X-ray fluorescence and absorption microspectroscopy

Citation Formats

References (57)

Cited By (7)

Similar Records

Related Subjects