Copper uptake, intracellular localization, and speciation in marine microalgae measured by synchrotron radiation X-ray fluorescence and absorption microspectroscopy
Abstract
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 andmore »
- Authors:
-
- 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)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1332944
- Grant/Contract Number:
- AC02-06CH11357
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Environmental Science and Technology
- Additional Journal Information:
- Journal Volume: 50; Journal Issue: 16; Journal ID: ISSN 0013-936X
- Publisher:
- American Chemical Society (ACS)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; Nitzschia closterium; SR-XRF; XANES; glutathione; phytochelatins; phytoplankton; polyphosphate
Citation Formats
Adams, Merrin S., Dillon, Carolyn T., Vogt, Stefan, Lai, Barry, Stauber, Jennifer, and Jolley, Dianne F. Copper uptake, intracellular localization, and speciation in marine microalgae measured by synchrotron radiation X-ray fluorescence and absorption microspectroscopy. United States: N. p., 2016.
Web. doi:10.1021/acs.est.6b00861.
Adams, Merrin S., Dillon, Carolyn T., Vogt, Stefan, Lai, Barry, Stauber, Jennifer, & Jolley, Dianne F. Copper uptake, intracellular localization, and speciation in marine microalgae measured by synchrotron radiation X-ray fluorescence and absorption microspectroscopy. United States. https://doi.org/10.1021/acs.est.6b00861
Adams, Merrin S., Dillon, Carolyn T., Vogt, Stefan, Lai, Barry, Stauber, Jennifer, and Jolley, Dianne F. Wed .
"Copper uptake, intracellular localization, and speciation in marine microalgae measured by synchrotron radiation X-ray fluorescence and absorption microspectroscopy". United States. https://doi.org/10.1021/acs.est.6b00861. https://www.osti.gov/servlets/purl/1332944.
@article{osti_1332944,
title = {Copper uptake, intracellular localization, and speciation in marine microalgae measured by synchrotron radiation X-ray fluorescence and absorption microspectroscopy},
author = {Adams, Merrin S. and Dillon, Carolyn T. and Vogt, Stefan and Lai, Barry and Stauber, Jennifer and Jolley, Dianne F.},
abstractNote = {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.},
doi = {10.1021/acs.est.6b00861},
journal = {Environmental Science and Technology},
number = 16,
volume = 50,
place = {United States},
year = {2016},
month = {7}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 39 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Binding of Nickel and Copper to Fish Gills Predicts Toxicity When Water Hardness Varies, But Free-Ion Activity Does Not
journal, March 1999
- Meyer, Joseph S.; Santore, Robert C.; Bobbitt, Joe P.
- Environmental Science & Technology, Vol. 33, Issue 6
Predicting the Bioavailability of Metals and Metal Complexes: Critical Review of the Biotic Ligand Model
journal, January 2005
- Slaveykova, Vera I.; Wilkinson, Kevin J.
- Environmental Chemistry, Vol. 2, Issue 1
Sensitivity of marine microalgae to copper: The effect of biotic factors on copper adsorption and toxicity
journal, November 2007
- Levy, Jacqueline L.; Stauber, Jennifer L.; Jolley, Dianne F.
- Science of The Total Environment, Vol. 387, Issue 1-3
Uptake and internalisation of copper by three marine microalgae: Comparison of copper-sensitive and copper-tolerant species
journal, August 2008
- Levy, J.; Angel, B.; Stauber, J.
- Aquatic Toxicology, Vol. 89, Issue 2
Copper-induced changes in intracellular thiols in two marine diatoms: Phaeodactylum tricornutum and Ceratoneis closterium
journal, November 2014
- Smith, Cassandra L.; Steele, Jessica E.; Stauber, Jennifer L.
- Aquatic Toxicology, Vol. 156
Predicting Copper Toxicity with Its Intracellular or Subcellular Concentration and the Thiol Synthesis in a Marine Diatom
journal, March 2007
- Miao, Ai-Jun; Wang, Wen-Xiong
- Environmental Science & Technology, Vol. 41, Issue 5
Reversibility of copper-thiol binding in Nitzschia closterium and Chlorella pyrenoidosa
journal, September 1986
- Stauber, J. L.; Florence, T. M.
- Aquatic Toxicology, Vol. 8, Issue 4
Mechanism of toxicity of ionic copper and copper complexes to algae
journal, January 1987
- Stauber, J. L.; Florence, T. M.
- Marine Biology, Vol. 94, Issue 4
The use of immobilised metal affinity chromatography (IMAC) to compare expression of copper-binding proteins in control and copper-exposed marine microalgae
journal, November 2013
- Smith, Cassandra L.; Stauber, Jennifer L.; Wilson, Mark R.
- Analytical and Bioanalytical Chemistry, Vol. 406, Issue 1
Hard X-ray microprobe studies of chromium(VI)-treated V79 Chinese hamster lung cells: intracellular mapping of the biotransformation products of a chromium carcinogen
journal, February 2002
- Dillon, Carolyn T.; Lay, Peter A.; Kennedy, Brendan J.
- JBIC Journal of Biological Inorganic Chemistry, Vol. 7, Issue 6
Intracellular mapping of the distribution of metals derived from the antitumor metallocenes
journal, May 2005
- Waern, Jenny B.; Harris, Hugh H.; Lai, Barry
- JBIC Journal of Biological Inorganic Chemistry, Vol. 10, Issue 5
Microprobe XRF Mapping and XAS Investigations of the Intracellular Metabolism of Arsenic for Understanding Arsenic-Induced Toxicity
journal, September 2008
- Munro, Kristie L.; Mariana, Anna; Klavins, Andrejs I.
- Chemical Research in Toxicology, Vol. 21, Issue 9
Does cytotoxicity of metallointercalators correlate with cellular uptake or DNA affinity?
journal, January 2012
- Davis, Kimberley J.; Carrall, Judith A.; Lai, Barry
- Dalton Transactions, Vol. 41, Issue 31
Quantifying Trace Elements in Individual Aquatic Protist Cells with a Synchrotron X-ray Fluorescence Microprobe
journal, August 2003
- Twining, Benjamin S.; Baines, Stephen B.; Fisher, Nicholas S.
- Analytical Chemistry, Vol. 75, Issue 15
Exploring Ocean Biogeochemistry by Single-Cell Microprobe Analysis of Protist Elemental Composition
journal, May 2008
- Twining, Benjamin S.; Baines, Stephen B.; Vogt, Stefan
- Journal of Eukaryotic Microbiology, Vol. 55, Issue 3
Characterization of phosphorus, calcium, iron, and other elements in organisms at sub-micron resolution using X-ray fluorescence spectromicroscopy: X-ray spectromicroscopy of organisms
journal, January 2009
- Diaz, Julia; Ingall, Ellery; Vogt, Stefan
- Limnology and Oceanography: Methods, Vol. 7, Issue 1
REINSTATEMENT OF THE GENUS CERATONEIS EHRENBERG AND LECTOTYPIFICATION OF ITS TYPE SPECIMEN: C. CLOSTERIUM EHRENBERG
journal, November 2005
- Jahn, Regine; Kusber, Wolf-Henning
- Diatom Research, Vol. 20, Issue 2
Studies of Marine Planktonic Diatoms: i. Cyclotella nana Hustedt, and Detonula Confervacea (Cleve) Gran.
journal, April 1962
- Guillard, Robert R. L.; Ryther, John H.
- Canadian Journal of Microbiology, Vol. 8, Issue 2
Relationship between ultrastructural changes and EROD activities in liver of fish exposed to Benzo[a]pyrene
journal, February 1999
- Au, D. W. T.; Wu, R. S. S.; Zhou, B. S.
- Environmental Pollution, Vol. 104, Issue 2
MAPS : A set of software tools for analysis and visualization of 3D X-ray fluorescence data sets
journal, March 2003
- Vogt, S.
- Journal de Physique IV (Proceedings), Vol. 104
Use and limitations of microbial bioassays for assessing copper bioavailability in the aquatic environment
journal, April 2000
- Stauber, J. L.; Davies, C. M.
- Environmental Reviews, Vol. 8, Issue 4
Copper and zinc tolerance of two tropical microalgae after copper acclimation
journal, January 2007
- Johnson, Hilary L.; Stauber, Jenny L.; Adams, Merrin S.
- Environmental Toxicology, Vol. 22, Issue 3
Development of flow cytometry-based algal bioassays for assessing toxicity of copper in natural waters
journal, January 2001
- Franklin, Natasha M.; Stauber, Jennifer L.; Lim, Richard P.
- Environmental Toxicology and Chemistry, Vol. 20, Issue 1
Metal bioavailability to phytoplankton—applicability of the biotic ligand model
journal, September 2002
- Campbell, Peter G. C.; Errécalde, Olivier; Fortin, Claude
- Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, Vol. 133, Issue 1-2
Bioavailability of trace metals to aquatic microorganisms: importance of chemical, biological and physical processes on biouptake
journal, November 2006
- Worms, I.; Simon, D. F.; Hassler, C. S.
- Biochimie, Vol. 88, Issue 11
Influence of N -2-hydroxyethylpiperazine- N ′-2-ethanesulfonic acid pH buffer on the biological response of marine algae
journal, February 2002
- Vasconcelos, M. Teresa S. D.; Leal, Maria Fernanda C.
- Environmental Toxicology and Chemistry, Vol. 21, Issue 2
Effect of Pseudokirchneriella subcapitata (Chlorophyceae) exudates on metal toxicity and colloid aggregation
journal, January 2007
- Koukal, Brahim; Rossé, Patrick; Reinhardt, Alain
- Water Research, Vol. 41, Issue 1
Significance of physicochemical forms of storage in microalgae in predicting copper transfer to filter-feeding oysters (Crassostrea gigas)
journal, January 2006
- Amiard-Triquet, Claude; Berthet, Brigitte; Joux, Lamia
- Environmental Toxicology, Vol. 21, Issue 1
Processes regulating cellular metal accumulation and physiological effects: Phytoplankton as model systems
journal, August 1998
- Sunda, William G.; Huntsman, Susan A.
- Science of The Total Environment, Vol. 219, Issue 2-3
Copper-induced changes of non-protein thiols and antioxidant enzymes in the marine microalga Phaeodactylum tricornutum
journal, August 2004
- Morelli, Elisabetta; Scarano, Gioacchino
- Plant Science, Vol. 167, Issue 2
Effects of Metal Combinations on the Production of Phytochelatins and Glutathione by the Marine Diatom Phaeodactylum tricornutum
journal, February 2006
- Kawakami, Silvia K.; Gledhill, Martha; Achterberg, Eric P.
- BioMetals, Vol. 19, Issue 1
Phytochelatin Induction, Cadmium Accumulation, and Algal Sensitivity to free Cadmium ion in Scenedesmus Vacuolatus
journal, January 2005
- Le Faucheur, Séverine; Behra, Renata; Sigg, Laura
- Environmental Toxicology and Chemistry, Vol. 24, Issue 7
Thiols in Scenedesmus vacuolatus upon exposure to metals and metalloids
journal, December 2006
- Le Faucheur, Séverine; Schildknecht, Fabian; Behra, Renata
- Aquatic Toxicology, Vol. 80, Issue 4
A phytochelatin-based bioassay in marine diatoms useful for the assessment of bioavailability of heavy metals released by polluted sediments
journal, April 2009
- Morelli, Elisabetta; Marangi, Maria Luisa; Fantozzi, Laura
- Environment International, Vol. 35, Issue 3
Heavy Metal-Induced Oxidative Stress in Algae1
journal, December 2003
- Pinto, Ernani; Sigaud-kutner, Teresa C. S.; Leitao, Maria A. S.
- Journal of Phycology, Vol. 39, Issue 6
Oxidative stress and antioxidant defenses in two green microalgae exposed to copper
journal, May 2009
- Sabatini, Sebastián E.; Juárez, Ángela B.; Eppis, Maria R.
- Ecotoxicology and Environmental Safety, Vol. 72, Issue 4
Why Is Metal Bioaccumulation So Variable? Biodynamics as a Unifying Concept
journal, April 2005
- Luoma, Samuel N.; Rainbow, Philip S.
- Environmental Science & Technology, Vol. 39, Issue 7
Copper Immobilization in Fouling Diatoms
journal, January 1981
- Daniel, G. F.; Chamberlain, A. H. L.
- Botanica Marina, Vol. 24, Issue 4
Uptake of heavy metals by Plectonema boryanum (cyanophyceae) into cellular components, especially polyphosphate bodies: An X-ray energy dispersive study
journal, February 1982
- Jensen, Thomas E.; Baxter, Mike; Rachlin, Joseph W.
- Environmental Pollution Series A, Ecological and Biological, Vol. 27, Issue 2
Copper resistance in Anabaena variabilis: Effects of phosphate nutrition and polyphosphate bodies
journal, January 1994
- Hashemi, F.; Leppard, G. G.; Kushnert, D. J.
- Microbial Ecology, Vol. 27, Issue 2
Influence of Phosphorus Nutrition on Copper Toxicity to Three Strains of Scenedesmus Acutus (Chlorophyceae)1
journal, June 1992
- Twiss, Michael R.; Nalewajko, Czeslawa
- Journal of Phycology, Vol. 28, Issue 3
Cysteine Enhances Bioavailability of Copper to Marine Phytoplankton
journal, September 2015
- Walsh, Michael J.; Goodnow, Sarah D.; Vezeau, Grace E.
- Environmental Science & Technology, Vol. 49, Issue 20
Response of the phytoplanctonic alga Tetraselmis suecica to copper and silver exposure: vesicular metal bioaccumulation and lack of starch bodies
journal, January 1991
- Ballan-Dufrançais, Christiane; Marcaillou, Christiane; Amiard-Triquet, Claude
- Biology of the Cell, Vol. 72, Issue 1-2
The rise of ROS
journal, September 2002
- Scandalios, John G.
- Trends in Biochemical Sciences, Vol. 27, Issue 9
Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants
journal, September 2005
- Mendoza-Cózatl, David; Loza-Tavera, Herminia; Hernández-Navarro, Andrea
- FEMS Microbiology Reviews, Vol. 29, Issue 4
Heavy metals toxicity in plants: An overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants
journal, April 2010
- Yadav, S. K.
- South African Journal of Botany, Vol. 76, Issue 2
Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple
journal, June 2001
- Schafer, Freya Q.; Buettner, Garry R.
- Free Radical Biology and Medicine, Vol. 30, Issue 11
Analysis of Glutathione Endpoints for Measuring Copper Stress in Chlamydomonas Reinhardtii
journal, January 2007
- Stoiber, Tasha L.; Shafer, Martin M.; Perkins, Dawn A. Karner
- Environmental Toxicology and Chemistry, Vol. 26, Issue 8
Reactive oxygen species: response of algal cells
journal, August 2000
- Mallick, Nirupama; Mohn, Friedrich Helmuth
- Journal of Plant Physiology, Vol. 157, Issue 2
Phytochelatins: The Principal Heavy-Metal Complexing Peptides of Higher Plants
journal, November 1985
- Grill, E.; Winnacker, E. -L.; Zenk, M. H.
- Science, Vol. 230, Issue 4726
P HYTOCHELATINS AND M ETALLOTHIONEINS : Roles in Heavy Metal Detoxification and Homeostasis
journal, June 2002
- Cobbett, Christopher; Goldsbrough, Peter
- Annual Review of Plant Biology, Vol. 53, Issue 1
The Heavy Metal-Binding Peptides of Plants
journal, June 1990
- Steffens, J. C.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 41, Issue 1
Cadmium sequestration in Chlamydomonas reinhardtii
journal, October 2001
- Hu, Shengxi; Lau, Ken W. K.; Wu, Madeline
- Plant Science, Vol. 161, Issue 5
Synthesis and stability of phytochelatins induced by cadmium and lead in the marine diatom Phaeodactylum tricornutum
journal, October 2001
- Morelli, E.; Scarano, G.
- Marine Environmental Research, Vol. 52, Issue 4
Copper K-edge XANES of Cu(I) and Cu(II) oxide mixtures
journal, November 2009
- Gaur, A.; Shrivastava, B. D.; Joshi, S. K.
- Journal of Physics: Conference Series, Vol. 190
Synthesis and structural analysis of copper(II) cysteine complexes
journal, January 2009
- Dokken, Kenneth M.; Parsons, Jason G.; McClure, John
- Inorganica Chimica Acta, Vol. 362, Issue 2
Speciation of copper in a range of food types by X-ray absorption spectroscopy
journal, December 2014
- Ceko, Melanie J.; Aitken, Jade B.; Harris, Hugh H.
- Food Chemistry, Vol. 164
Works referencing / citing this record:
Physiological and metabolic responses of Scenedesmus quadricauda (Chlorophyceae) to nickel toxicity and warming
journal, July 2019
- Yong, Wai-Kuan; Sim, Kae-Shin; Poong, Sze-Wan
- 3 Biotech, Vol. 9, Issue 8
Effects of LaCoO 3 perovskite nanoparticle on Daphnia magna : accumulation, distribution and biomarker responses
journal, January 2019
- Zhou, Tingting; Zhang, Lili; Wang, Ying
- RSC Advances, Vol. 9, Issue 42
Environmental Concentrations of Copper, Alone or in Mixture With Arsenic, Can Impact River Sediment Microbial Community Structure and Functions
journal, August 2018
- Mahamoud Ahmed, Ayanleh; Lyautey, Emilie; Bonnineau, Chloé
- Frontiers in Microbiology, Vol. 9
Pyrenoidal sequestration of cadmium impairs carbon dioxide fixation in a microalga
journal, November 2019
- Penen, Florent; Isaure, Marie‐Pierre; Dobritzsch, Dirk
- Plant, Cell & Environment, Vol. 43, Issue 2
Experimental Warming Differentially Influences the Vulnerability of Phototrophic and Heterotrophic Periphytic Communities to Copper Toxicity
journal, July 2018
- Pesce, Stéphane; Lambert, Anne-Sophie; Morin, Soizic
- Frontiers in Microbiology, Vol. 9
Functional CTR-type Cu(I) transporters in an oceanic diatom: CTR-type Cu(I) transporters in an oceanic diatom
journal, October 2018
- Kong, Liangliang; Price, Neil M.
- Environmental Microbiology, Vol. 21, Issue 1
Experimental Warming Differentially Influences the Vulnerability of Phototrophic and Heterotrophic Periphytic Communities to Copper Toxicity
journal, July 2018
- Pesce, Stéphane; Lambert, Anne-Sophie; Morin, Soizic
- Frontiers in Microbiology, Vol. 9
Toxicity, Physiological, and Ultrastructural Effects of Arsenic and Cadmium on the Extremophilic Microalga Chlamydomonas acidophila
journal, March 2020
- Díaz, Silvia; De Francisco, Patricia; Olsson, Sanna
- International Journal of Environmental Research and Public Health, Vol. 17, Issue 5