Weak organic ligands enhance zinc uptake in marine phytoplankton
Abstract
A recent study of the effect of pH on Zn and Cd bioavailability shows that binding to weak organic ligands can increase the pool of metals available to phytoplankton in the presence of strong chelating agents. We explore the underlying mechanism in laboratory experiments with the model species Emiliania huxleyi and Thalassiosira weissflogii. Additions of L- and D- isomers of cysteine (Cys) result in similar increases in Zn uptake rates in the presence of the strong chelator ethylenediaminetetraacetic acid (EDTA) but decrease it in the absence of EDTA, ruling out uptake by a specific Zn-Cys transporter. The effect of Cys does not result from alleviating diffusion limitation of inorganic Zn. The enhancement of Zn uptake kinetics by weak ligands is consistent with a mechanism involving formation of a transient ternary complex with uptake molecules: (1) the enhancement is most dramatic in Zn limited cells whose high affinity transporters should be most effective at extracting Zn from weak ligands; (2) the enhancement occurs with a variety of weak ligands, demonstrating that the underlying mechanism has little chemical specificity; and (3) no enhancement of uptake is seen when Zn is bound in complexes that would make formation of multiligand complexes with uptake molecules difficult. Weak complexing agents which have received heretofore little attention may play a key role in the bioavailability of metals in natural waters.
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Recent culture work demonstrated that weakly binding organic ligands can increase Zn uptake rates in phytoplankton.
“Consistent with this idea is recent culture work after Xu et al. (2012) and Aristilde et al. (2012), where it was demonstrated that weakly binding organic ligands can in fact increase Zn uptake rates in phytoplankton.”
From Trace elements at the intersection of marine biological and geochemical evolution (2016) · cites this paper as Aristilde et al., 2012
Cites
Diffusion of ions in sea water and in deep-sea sediments
Yuan-Hui, L., & Gregory, S. (1974) · Geochimica et Cosmochimica Acta · doi:10.1016/0016-7037(74)90145-8 · Cited by 2,875 · see citing works
Principles and applications of aquatic chemistry
(1993) · Choice Reviews Online · doi:10.5860/choice.31-0941 · Cited by 1,723 · see citing works
Rue, E. L., & Bruland, K. W. (1995) · Marine Chemistry · doi:10.1016/0304-4203(95)00031-l · Cited by 1,004 · see citing works
Copper complexation in the Northeast Pacific
Coale, K. H., & Bruland, K. W. (1988) · Limnology and Oceanography · doi:10.4319/lo.1988.33.5.1084 · Cited by 496 · see citing works
Complexation of zinc by natural organic ligands in the central North Pacific
Bruland, K. W. (1989) · Limnology and Oceanography · doi:10.4319/lo.1989.34.2.0269 · Cited by 467 · see citing works
Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation
Allen, A. E., LaRoche, J., Maheswari, U., Lommer, M., Schauer, N., Lopez, P. J., Finazzi, G., Fernie, A. R., & Bowler, C. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711370105 · Cited by 437 · see citing works
Sunda, W. G., & Huntsman, S. A. (1998) · The Science of The Total Environment · doi:10.1016/s0048-9697(98)00226-5 · Cited by 407 · see citing works
Chemistry of Marine Ligands and Siderophores
Gauglitz, J. M., & Butler, A. (2008) · Annual Review of Marine Science · doi:10.1146/annurev.marine.010908.163712 · Cited by 358 · see citing works
A general kinetic model for iron acquisition by eukaryotic phytoplankton
Shaked, Y., Kustka, A. B., & Morel, F. M. M. (2005) · Limnology and Oceanography · doi:10.4319/lo.2005.50.3.0872 · Cited by 318 · see citing works
Self-citationAcquisition and Utilization of Transition Metal Ions by Marine Organisms
Butler, A. (1998) · Science · doi:10.1126/science.281.5374.207 · Cited by 289 · see citing works
Feedback interactions between zinc and phytoplankton in seawater
Sunda, W. G., & Huntsman, S. A. (1992) · Limnology and Oceanography · doi:10.4319/lo.1992.37.1.0025 · Cited by 286 · see citing works
Metal bioavailability to phytoplankton—applicability of the biotic ligand model
Campbell, P. G. C., Errécalde, O., Fortin, C., Hiriart‐Baer, V. P., & Vigneault, B. (2002) · Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology · doi:10.1016/s1532-0456(02)00104-7 · Cited by 234 · see citing works
A trace metal clean reagent to remove surface-bound iron from marine phytoplankton
Tovar‐Sánchez, A., Sañudo‐Wilhelmy, S. A., Garcı́a-Vargas, M., et al. (2003) · Marine Chemistry · doi:10.1016/s0304-4203(03)00054-9 · Cited by 211 · see citing works
Saito, M. A., & Moffett, J. W. (2001) · Marine Chemistry · doi:10.1016/s0304-4203(01)00025-1 · Cited by 206 · see citing works
Labile Cd Complexes Increase Cd Availability to Plants
Degryse, F., Smolders, E., & Merckx, R. (2005) · Environmental Science & Technology · doi:10.1021/es050894t · Cited by 198 · see citing works
The role of siderophores in iron acquisition by photosynthetic marine microorganisms
Hopkinson, B. M., & Morel, F. M. M. (2009) · BioMetals · doi:10.1007/s10534-009-9235-2 · Cited by 196 · see citing works
Self-citationCarr, J. A., Gentles, A., Smith, E. E., Goleman, W. L., Urquidi, L. J., Thuett, K. A., Kendall, R. J., Giesy, J. P., Gross, T. S., Solomon, K. R., et al. (2003) · Environmental Toxicology and Chemistry · doi:10.1897/1551-5028(2003)022 · Cited by 186 · see citing works
Complexation of cadmium by natural organic ligands in the central North Pacific
Bruland, K. W. (1992) · Limnology and Oceanography · doi:10.4319/lo.1992.37.5.1008 · Cited by 179 · see citing works
Hanikenne, M., Krämer, U., Demoulin, V., & Baurain, D. (2005) · PLANT PHYSIOLOGY · doi:10.1104/pp.104.054189 · Cited by 174 · see citing works
Distinguishing between cellular and Fe-oxide-associated trace elements in phytoplankton
Tang, D., & Morel, F. M. M. (2005) · Marine Chemistry · doi:10.1016/j.marchem.2005.06.003 · Cited by 165 · see citing works
Self-citationPhinney, J. T., & Bruland, K. W. (1994) · Environmental Science & Technology · doi:10.1021/es00060a006 · Cited by 156 · see citing works
Multiple roles of siderophores in free-living nitrogen-fixing bacteria
Kraepiel, A. M. L., Bellenger, J., Wichard, T., & Morel, F. M. M. (2009) · BioMetals · doi:10.1007/s10534-009-9222-7 · Cited by 154 · see citing works
Self-citationGlutathione and other low molecular weight thiols in marine phytoplankton under metal stress
Ahner, B., Wei, L., Oleson, J., et al. (2002) · Marine Ecology Progress Series · doi:10.3354/meps232093 · Cited by 127 · see citing works
Toxicity of copper complexes to the marine diatom Nitzschia closterium
Florence, T. M., & Stauber, J. L. (1986) · Aquatic Toxicology · doi:10.1016/0166-445x(86)90069-x · Cited by 123 · see citing works
Kinetics of trace metal complexation: ligand-exchange reactions
Hering, J. G., & Morel, F. M. M. (1990) · Environmental Science & Technology · doi:10.1021/es00072a014 · Cited by 117 · see citing works
Self-citationVasconcelos, T., Leal, M. F. C., & van den Berg, C. M. G. (2002) · Marine Chemistry · doi:10.1016/s0304-4203(01)00087-1 · Cited by 113 · see citing works
Degryse, F., Smolders, E., & Parker, D. R. (2006) · Plant and Soil · doi:10.1007/s11104-006-9121-4 · Cited by 112 · see citing works
Chemical speciation of chromium and nickel in the western Mediterranean
Achterberg, E. P., & van den Berg, C. M. G. (1997) · Deep Sea Research Part II Topical Studies in Oceanography · doi:10.1016/s0967-0645(96)00086-0 · Cited by 109 · see citing works
(1981) · Elsevier eBooks · doi:10.1016/c2013-0-03311-7 · Cited by 108 · see citing works
van den Berg, C. M. G. (1985) · Marine Chemistry · doi:10.1016/0304-4203(85)90017-9 · Cited by 105 · see citing works
Novel copper‐binding and nitrogen‐rich thiols produced and exuded by Emiliania huxleyi
Dupont, C. L., Nelson, R. K., Bashir, S., et al. (2004) · Limnology and Oceanography · doi:10.4319/lo.2004.49.5.1754 · Cited by 88 · see citing works
ChemInform Abstract: KINETICS AND MECHANISMS OF COMPLEX FORMATION AND LIGAND EXCHANGE
Pagenkopf, G. K. (1978) · ChemInform · doi:10.1002/chin.197847368 · Cited by 88 · see citing works
Xu, Y., Shi, D., Aristilde, L., & Morel, F. M. M. (2012) · Limnology and Oceanography · doi:10.4319/lo.2012.57.1.0293 · Cited by 87 · see citing works
Self-citationHassler, C. S., & Wilkinson, K. J. (2003) · Environmental Toxicology and Chemistry · doi:10.1002/etc.5620220322 · Cited by 87 · see citing works
Comparison of Cd(II), Cu(II), and Pb(II) Biouptake by Green Algae in the Presence of Humic Acid
Lamelas, C., & Slaveykova, V. I. (2007) · Environmental Science & Technology · doi:10.1021/es063102j · Cited by 78 · see citing works
Errécalde, O., & Campbell, P. G. C. (2000) · Journal of Phycology · doi:10.1046/j.1529-8817.2000.99103.x · Cited by 73 · see citing works
Lane, E., Jang, K., Cullen, J. T., & Maldonado, M. T. (2008) · Limnology and Oceanography · doi:10.4319/lo.2008.53.5.1784 · Cited by 59 · see citing works
Vasconcelos, T., & Leal, M. F. C. (2008) · Marine Environmental Research · doi:10.1016/j.marenvres.2008.07.002 · Cited by 54 · see citing works
Bates, N. R., & Hansell, D. A. (1999) · Marine Chemistry · doi:10.1016/s0304-4203(99)00045-6 · Cited by 52 · see citing works
Phinney, J. T., & Bruland, K. W. (1997) · Environmental Toxicology and Chemistry · doi:10.1002/etc.5620161009 · Cited by 48 · see citing works
Quantitative Structure−Activity Relationships for Aqueous Metal−Siderophore Complexes
Duckworth, O. W., Bargar, J., & Sposito, G. (2008) · Environmental Science & Technology · doi:10.1021/es802044y · Cited by 44 · see citing works
Wang, P., Zhou, D., Luo, X., et al. (2008) · Plant and Soil · doi:10.1007/s11104-008-9769-z · Cited by 40 · see citing works
Characterization of complexing agents in natural waters by copper(II)/copper(I) amperometry
Waite, T. D., & Morel, F. M. M. (1983) · Analytical Chemistry · doi:10.1021/ac00259a020 · Cited by 39 · see citing works
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Trace elements at the intersection of marine biological and geochemical evolution
Robbins, L. J., Lalonde, S. V., Planavsky, N. J., Partin, C. A., Reinhard, C. T., Kendall, B., Scott, C., Hardisty, D. S., Gill, B. C., Alessi, D. S., et al. (2016) · Earth-Science Reviews · doi:10.1016/j.earscirev.2016.10.013 · Cited by 227 · see citing works
Robbins, L. J., Lalonde, S. V., Saito, M. A., Planavsky, N. J., Mloszewska, A. M., Pecoits, E., Scott, C., Dupont, C. L., Kappler, A., & Konhauser, K. O. (2013) · Geobiology · doi:10.1111/gbi.12036 · Cited by 79 · see citing works
Erickson, D. J., Sulzberger, B., Zepp, R. G., & Austin, A. T. (2014) · Photochemical & Photobiological Sciences · doi:10.1039/c4pp90036g · Cited by 69 · see citing works
- Authors
- Aristilde, L., Xu, Y., & Morel, F. M. M.
- Affiliations
- Princeton University (US)
- Corresponding author
- Xu, Yan
- Venue
- Environmental Science & Technology
- Publisher
- American Chemical Society (ACS)
- Published
- 2012-04-26
- Volume
- 46
- Issue
- 10
- Pages
- 5438-5445
- ISSN
- 0013-936X (ISSN-L)
- 1520-5851
- OpenAlex
- W2328200982
- Cited by
- 105
- References
- 43
- Citations by year
- 2026: 1 · 2025: 7 · 2024: 10 · 2023: 5 · 2022: 8 · 2021: 7 · 2020: 8 · 2019: 10 · 2018: 8 · 2017: 5 · 2016: 11 · 2015: 8 · 2014: 10 · 2013: 7
- FWCI
- 5.92
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Environmental Science & Technology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine and coastal ecosystems
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Micronutrient Interactions and Effects
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Environmental Toxicology and Ecotoxicology
- Keywords
- zinc uptake, metal bioavailability, marine phytoplankton, Emiliania huxleyi, Thalassiosira weissflogii, cysteine, EDTA chelation, metal transporters, zinc limitation, diffusion limitation, metal speciation
- MeSH terms
- Biodegradation, Environmental, Cell Membrane, Cysteine, Diffusion, Edetic Acid, Ligands, Organic Chemicals, Phytoplankton, Time Factors, Zinc, Haptophyta, Aquatic Organisms
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