Voltammetric characterisation of macroalgae-exuded organic ligands (L) in response to Cu and Zn: a source and stimuli for L
Hollydawn Murray A C D , Guillaume Meunier A , Constant M. G. van den Berg B , Rachel R. Cave A and Dagmar B. Stengel C
+ Author Affiliations
- Author Affiliations
A Earth and Ocean Sciences, School of Natural Sciences, National University of Ireland Galway, University Road, Galway, Ireland.
B Oceanography Laboratory, Department of Earth Science, University of Liverpool, Liverpool, Merseyside, L69 72Z, UK.
C Botany and Plant Sciences, School of Natural Sciences, National University of Ireland Galway, University Road, Galway, Ireland.
D Corresponding author. Email: hollydawn.murray@gmail.com
Environmental Chemistry 11(2) 100-113 https://doi.org/10.1071/EN13085
Submitted: 24 April 2013 Accepted: 15 June 2013 Published: 26 September 2013
Environmental context. Identifying the source and stimuli responsible for organic ligands in seawater is crucial to understanding trace metal availability. Voltammetric techniques were employed to characterise the water chemistry of seaweed cultures exposed to low levels of Cu or Zn over 7 days. The results suggest that seaweeds are a potential source of metal complexing ligands and Cu and Zn appear to stimulate ligand production; further research is required to determine if this is applicable to macroalgae and metals outside this study.
Abstract. It is widely accepted that organic ligands control metal speciation in seawater, although little is known about their source, stimuli or identity. To gain insight on the possible environmental controls of metal complexing ligands (L), three brown macroalgae common in Irish waters (Ascophyllum nodosum, Fucus vesiculosus and Laminaria hyperborea) were cultured under low levels of Cu (0, 7.86 or 15.7 nM) or Zn (0, 15.2 or 91.7 nM) exposure. Seaweed chlorophyll-a fluorescence (Fv/Fm), metal speciation (Cu, Zn), complexing ligands (LM), conditional stability constants (log K′LM), glutathione (GSH), cysteine (Cys) and seaweed metal contents were monitored over 7 days. Although there was no effect on the internal seaweed metal concentrations, Cu and Zn additions significantly altered the water chemistry of each culture. Metal additions increased the total dissolved metal concentrations for all three species. Significantly higher [LM] values in cultures with added metals than the relevant controls point to both metals as stimuli of L production. All species released ligands in response to Cu or Zn exposure, indicating each seaweed is a relevant source of L. Comparison of log K′ values to those of previously determined ligands provides little evidence that the ligands reported here belong to the compounds identified as L in the literature.
References
[1] C. S. Lobban, P. J. Harrison, Seaweed Ecology and Physiology 1994 (Cambridge University Press: Cambridge, UK).[2] J. A. DeBoer, Nutrients, in The Biology of Seaweeds (Eds C. S. Lobban, M. J. Wynne) 1981, pp. 356–386 (Blackwell Scientific: Hoboken, NJ).
[3] J. L. Burkhead, K. G. Reynolds, Copper homeostasis. New Phytol. 2009, 182, 799.
| Copper homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvVOgt7g%3D&md5=d0b46edcda5ff114a7e370951168063dCAS | 19402880PubMed |
[4] B. L. Vallee, D. S. Auld, Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry 1990, 29, 5647.
| Zinc coordination, function, and structure of zinc enzymes and other proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXktF2ku70%3D&md5=30d07483696c40b1cd43c477e351612dCAS | 2200508PubMed |
[5] S. Clemens, Molecular mechanisms of plant metal tolerance and homeostasis. Planta 2001, 212, 475.
| Molecular mechanisms of plant metal tolerance and homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhs1Cgtr8%3D&md5=98be5e15d8f68fa3007254dba09ce1b4CAS | 11525504PubMed |
[6] W. G. Sunda, P. A. Tester, S. A. Huntsman, Effects of cupric and zinc ion activities on the survival and reproduction of marine copepods. Mar. Biol. 1987, 94, 203.
| Effects of cupric and zinc ion activities on the survival and reproduction of marine copepods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhslSmt7o%3D&md5=02de29fbca386a8bc6687b6d2219f362CAS |
[7] H. Küpper, I. Šetlík, M. Spiller, Heavy metal induced inhibition of photosynthesis: targets of in vivo heavy metal chlorophyll formation. J. Phycol. 2002, 38, 429.
[8] H. D. Nielsen, S. L. Nielsen, Evaluation of imaging and conventional PAM as a measure of photosynthesis in thin- and thick-leaved marine macroalgae. Aquat. Biol. 2008, 3, 121.
| Evaluation of imaging and conventional PAM as a measure of photosynthesis in thin- and thick-leaved marine macroalgae.Crossref | GoogleScholarGoogle Scholar |
[9] E. Pinto, T. S. Kutner, M. Leitão, Heavy metal induced oxidative stress in algae. J. Phycol. 2003, 39, 1008.
| Heavy metal induced oxidative stress in algae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjvVaktA%3D%3D&md5=cb1a0863b0984f53f4f7d0789eefb8e2CAS |
[10] H. D. Nielsen, S. L. Nielsen, Photosynthetic responses to Cu2+ exposure are independent of light acclimation and uncoupled from growth inhibition in Fucus serratus. Mar. Pollut. Bull. 2005, 50, 1675.
| Photosynthetic responses to Cu2+ exposure are independent of light acclimation and uncoupled from growth inhibition in Fucus serratus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1OhsrrI&md5=efd8d97f8c61cf50e0fb9e60c0e39a24CAS | 16112143PubMed |
[11] P. Bond, M. Brown, R. Moate, M. Gledhill, S. Hill, M. Nimmo, Arrested development in Fucus spiralis (Phaeophyceae) germlings exposed to copper. Eur. J. Phycol. 1999, 34, 513.
| Arrested development in Fucus spiralis (Phaeophyceae) germlings exposed to copper.Crossref | GoogleScholarGoogle Scholar |
[12] H. A. Baumann, L. Morrison, D. B. Stengel, Metal accumulation and toxicity measured by PAM chlorophyll fluorescence in seven species of marine macroalgae. Ecotoxicol. Environ. Saf. 2009, 72, 1063.
| Metal accumulation and toxicity measured by PAM chlorophyll fluorescence in seven species of marine macroalgae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXkvVWjsL4%3D&md5=c5c68fabca898f4431a977216d7c6703CAS | 19106005PubMed |
[13] L. C. Rai, J. P. Gaur, H. D. Kumar, Phycology and heavy metal pollution. Biol. Rev. Camb. Philos. Soc. 1981, 56, 99.
| Phycology and heavy metal pollution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXlt1KktL4%3D&md5=f573637faff9167f74998cbbd7878f57CAS |
[14] M. Leal, C. M. G. van den Berg, Evidence for strong copper(I) complexation by organic ligands in seawater. Aquat. Geochem. 1998, 4, 49.
| Evidence for strong copper(I) complexation by organic ligands in seawater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntlSjurs%3D&md5=9379e0af2c3155fd3d10232e03e50fdfCAS |
[15] J. R. Donat, K. W. Bruland, A comparison of two voltammetric techniques for determining zinc speciation in Northeast Pacific Ocean waters. Mar. Chem. 1990, 28, 301.
| A comparison of two voltammetric techniques for determining zinc speciation in Northeast Pacific Ocean waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXit1artLo%3D&md5=203123de2079ad54b84a07e812332957CAS |
[16] M. Ellwood, C. M. G. van den Berg, Zinc speciation in the Northeastern Atlantic Ocean. Mar. Chem. 2000, 68, 295.
| Zinc speciation in the Northeastern Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXptF2kug%3D%3D&md5=bdf77dda451effbe07b3d3c5bcb762c4CAS |
[17] C. M. G. van den Berg, Determination of the complexing capacity and conditional stability constants of complexes of copper(II) with natural organic ligands in seawater by cathodic stripping voltammetry of copper–catechol complex ions. Mar. Chem. 1984, 15, 1.
| Determination of the complexing capacity and conditional stability constants of complexes of copper(II) with natural organic ligands in seawater by cathodic stripping voltammetry of copper–catechol complex ions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXlslOjs7g%3D&md5=6f6d8d61744601d6b409a50e7dd959dfCAS |
[18] P. J. M. Buckley, C. M. G. van den Berg, Copper complexation profiles in the Atlantic Ocean. Mar. Chem. 1986, 19, 281.
| Copper complexation profiles in the Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XltVahsbc%3D&md5=9a06932ab8531b8dce54850f62c7ef84CAS |
[19] K. H. Coale, K. W. Bruland, Copper complexation in the Northeast Pacific. Limnol. Oceanogr. 1988, 33, 1084.
| Copper complexation in the Northeast Pacific.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXksVCluw%3D%3D&md5=38e2fc5379a9cb67f6089ad71243ec53CAS |
[20] J. W. Moffett, Temporal and spatial variability of copper complexation by strong chelators in the Sargasso Sea. Deep-Sea Res. 1995, 42, 1273.
| Temporal and spatial variability of copper complexation by strong chelators in the Sargasso Sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xis1CqtA%3D%3D&md5=120e09cfef5202b9d76c21767a205fb1CAS |
[21] K. W. Bruland, Complexation of zinc by natural organic ligands in the central North Pacific. Limnol. Oceanogr. 1989, 34, 269.
| Complexation of zinc by natural organic ligands in the central North Pacific.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXkvVeltrs%3D&md5=fc0e53c5a4afeb00d5f5131607b93523CAS |
[22] Z. Manping, G. Boshu, Z. Zhengbin, L. Liansheng, Heavy metal complexation capacity of the South China Sea water. Chin. J. Ocean. Limnol. 1990, 8, 158.
| Heavy metal complexation capacity of the South China Sea water.Crossref | GoogleScholarGoogle Scholar |
[23] J. Buffle, Complexation Reactions in Aquatic Systems (Ed. R. A. Chalmers) 1988 (Ellis Horwood Ltd.: Chichester, UK).
[24] J. I. Hedges, G. Eglinton, P. G. Hatcher, D. L. Kirchman, The molecularly uncharacterized component of nonliving organic matter in natural environments. Org. Geochem. 2000, 31, 945.
| The molecularly uncharacterized component of nonliving organic matter in natural environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosVGiur4%3D&md5=1d5a549ce663100af4bfe02cb43014e2CAS |
[25] M. T. S. D. Vasconcelos, Antagonistic interactions of Pb and Cd on Cu uptake, growth inhibition and chelator release in the marine algae Emiliania huxleyi. Mar. Chem. 2001, 75, 123.
| Antagonistic interactions of Pb and Cd on Cu uptake, growth inhibition and chelator release in the marine algae Emiliania huxleyi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvVOqsLs%3D&md5=734aabbd6113683db10543e2a6eb725eCAS |
[26] A. R. Manley, L. D. Gruffydd, P. C. Almada-Villela, The effect of copper and zinc on the shell growth of Mytilus edulis measured by a laser diffraction technique. J. Mar. Biol. Assoc. U. K. 1984, 64, 417.
| The effect of copper and zinc on the shell growth of Mytilus edulis measured by a laser diffraction technique.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXksV2ktrw%3D&md5=f41a8fba3b6484ad912168b02c935dc0CAS |
[27] R. H. Crist, J. R. Martin, P. W. Guptill, Interaction of metals and protons with algae. 2. Ion exchange in adsorption and metal displacement by protons. Environ. Sci. Technol. 1990, 24, 337.
| Interaction of metals and protons with algae. 2. Ion exchange in adsorption and metal displacement by protons.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXpsFertw%3D%3D&md5=22689e3d448e56b50d202aab2274c2f0CAS |
[28] L. R. Andrade, R. N. Leal, M. Noseda, M. E. R. Duarte, M. S. Pereira, P. A. S. Mourao, Brown algae overproduce cell wall polysaccharides as a protection mechanism against the heavy metal toxicity. Mar. Pollut. Bull. 2010, 60, 1482.
| Brown algae overproduce cell wall polysaccharides as a protection mechanism against the heavy metal toxicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVKit7nL&md5=23fa1cf6693c98a7019b744b1347f15eCAS | 20553858PubMed |
[29] M. Gledhill, M. Nimmo, S. Hill, The release of copper-complexing ligands by the brown alga Fucus vesiculosus (Phaeophyceae) in response to increasing total copper levels. J. Phycol. 1999, 35, 501.
| The release of copper-complexing ligands by the brown alga Fucus vesiculosus (Phaeophyceae) in response to increasing total copper levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksl2hsr8%3D&md5=451193080b81edf2443bcefe03e5a877CAS |
[30] S. Sueur, C. M. G. van den Berg, J. Riley, Measurement of the metal complexing ability of exudates of marine macroalgae. Limnol. Oceanogr. 1982, 27, 536.
| Measurement of the metal complexing ability of exudates of marine macroalgae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38Xkt1Sqtrc%3D&md5=f6b55fc6c68f5d9ff5a22c0597030922CAS |
[31] L. Laglera, C. M. G. van den Berg, Copper complexation by thiol compounds in estuarine waters. Mar. Chem. 2003, 82, 71.
| Copper complexation by thiol compounds in estuarine waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktF2rs7c%3D&md5=a71c4180d001826e600b363d7cf786e0CAS |
[32] D. Tang, K. Warnken, P. Santschi, Organic complexation of copper in surface waters of Galveston Bay. Limnol. Oceanogr. 2001, 46, 321.
| Organic complexation of copper in surface waters of Galveston Bay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtVWgsLY%3D&md5=571c593d71158e38d3156e547959dbb3CAS |
[33] M. Leal, M. Vasconcelos, C. M. G. van den Berg, Copper-induced release of complexing ligands similar to thiols by Emiliania huxleyi in seawater cultures. Limnol. Oceanogr. 1999, 44, 1750.
| Copper-induced release of complexing ligands similar to thiols by Emiliania huxleyi in seawater cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnsVWisLY%3D&md5=2d699ce713e8455eb0a2f81950022d36CAS |
[34] M. Vasconcelos, M. Leal, C. M. G. van den Berg, Influence of the nature of the exudates released by different marine algae on the growth, trace metal uptake, and exudation of Emiliania huxleyi in natural seawater. Mar. Chem. 2002, 77, 187.
| Influence of the nature of the exudates released by different marine algae on the growth, trace metal uptake, and exudation of Emiliania huxleyi in natural seawater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtlSksrk%3D&md5=454761874d1ad3a945d6dd9dcbc72dc6CAS |
[35] R. Town, M. Filella, A comprehensive systematic compilation of complexation parameters reported for trace metals in natural waters. Aquat. Sci. 2000, 62, 252.
| A comprehensive systematic compilation of complexation parameters reported for trace metals in natural waters.Crossref | GoogleScholarGoogle Scholar |
[36] M. Boye, C. M. G. van den Berg, Iron availability and the release of iron-complexing ligands by Emiliania huxleyi. Mar. Chem. 2000, 70, 277.
| Iron availability and the release of iron-complexing ligands by Emiliania huxleyi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktlSlt7Y%3D&md5=d7ab6a0a460cd5de16a63517c07fbb70CAS |
[37] F. Tian, R. D. Frew, S. Sander, K. A. Hunter, M. J. Ellwood, Organic iron(III) speciation in surface transects across a frontal zone: the Chatham Rise, New Zealand. Mar. Fresh. Res. 2006, 57, 533.
| Organic iron(III) speciation in surface transects across a frontal zone: the Chatham Rise, New Zealand.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XntFCnt70%3D&md5=09bff4e566073b674f4780b92e211f35CAS |
[38] M. Pesavento, G. Alberti, R. Biesuz, Analytical methods for determination of free metal ion concentration, labile species fraction and metal complexation capacity of environmental waters: a review. Anal. Chim. Acta 2009, 631, 129.
| Analytical methods for determination of free metal ion concentration, labile species fraction and metal complexation capacity of environmental waters: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFWis73L&md5=de2f451da72afe6a35ad02c8c3df2ba8CAS | 19084618PubMed |
[39] L. Gerringa, T. Poortvliet, H. Hummel, Comparison of chemical speciation of copper in the Oosterschelde and Westerschelde estuaries, the Netherlands. Estuar. Coast. Shelf Sci. 1996, 42, 629.
| Comparison of chemical speciation of copper in the Oosterschelde and Westerschelde estuaries, the Netherlands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xjs1Cjtb0%3D&md5=83ce7006dea7886af6cd4f81f0472b59CAS |
[40] L. A. Miller, K. W. Bruland, Competitive equilibration techniques for determining transition metal speciation in natural waters: evaluation using model data. Anal. Chim. Acta 1997, 343, 161.
| Competitive equilibration techniques for determining transition metal speciation in natural waters: evaluation using model data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXis1Wmsr0%3D&md5=a09d743715092384b74137decae3f0b1CAS |
[41] N. Turoczy, J. Sherwood, Modification of the van den Berg/Ruzic method for the investigation of complexation parameters of natural waters. Anal. Chim. Acta 1997, 354, 15.
| Modification of the van den Berg/Ruzic method for the investigation of complexation parameters of natural waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnvVShu74%3D&md5=e5d3580fa77a3cc7d64963d11282acdbCAS |
[42] R. J. M. Hudson, E. L. Rue, K. W. Bruland, Modeling complexometric titrations of natural water samples. Environ. Sci. Technol. 2003, 37, 1553.
| Modeling complexometric titrations of natural water samples.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitVOlsbk%3D&md5=0ac5f47f93a004b3174506a6f2ad03e6CAS |
[43] D. Monticelli, C. Dossi, A. Castelletti, Assessment of accuracy and precision in speciation analysis by competitive ligand equilibration–cathodic stripping voltammetry (CLE-CSV) and application to Antarctic samples. Anal. Chim. Acta 2010, 675, 116.
| Assessment of accuracy and precision in speciation analysis by competitive ligand equilibration–cathodic stripping voltammetry (CLE-CSV) and application to Antarctic samples.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtV2gtLrJ&md5=a84a572a648035167b0d766b916acb8fCAS | 20800722PubMed |
[44] D. R. Kester, I. W. Duedall, D. N. Connors, Preparation of artificial seawater. Limnol. Oceanogr. 1967, 12, 176.
| Preparation of artificial seawater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2sXhtFylur0%3D&md5=2d9c33334bf493dd45a2aab704dc3c48CAS |
[45] M. Kitajima, W. L. Butler, Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochem. Biophys. Acta 1975, 376, 105.
| Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXktVGhtr0%3D&md5=f29acf938d50159cea17c663f070ef98CAS | 1125215PubMed |
[46] L. M. Laglera, C. M. G. van den Berg, Copper complexation by thiol compounds in estuarine waters. Mar. Chem. 2003, 82, 71.
| Copper complexation by thiol compounds in estuarine waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktF2rs7c%3D&md5=a71c4180d001826e600b363d7cf786e0CAS |
[47] M. Lucia, A. M. Campos, C. M. G. van den Berg, Determination of copper complexation in seawater by cathodic stripping voltammetry and ligand competition with salicylaldoxime. Anal. Chim. Acta 1994, 284, 481.
| Determination of copper complexation in seawater by cathodic stripping voltammetry and ligand competition with salicylaldoxime.Crossref | GoogleScholarGoogle Scholar |
[48] C. M. G. van den Berg, Determination of the zinc complexing capacity in seawater by cathodic stripping voltammetry of zinc – APDC complex ions. Mar. Chem. 1985, 16, 121.
| Determination of the zinc complexing capacity in seawater by cathodic stripping voltammetry of zinc – APDC complex ions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXltV2lt7g%3D&md5=6327250dc1b2626fed9fec61e224accaCAS |
[49] C. M. G. van den Berg, Determination of copper complexation with natural organic ligands in seawater by equilibration with MnO2 I. Theory. Mar. Chem. 1982, 11, 307.
| Determination of copper complexation with natural organic ligands in seawater by equilibration with MnO2 I. Theory.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XlsFShsbc%3D&md5=2a12cdaf73dd8bb581c8ad1f244253dfCAS |
[50] D. R. Turner, M. Whitfield, A. G. Dickson, The equilibrium speciation of dissolved components in freshwater and seawater at 25 °C and 1 atm pressure. Geochim. Cosmochim. Acta 1981, 45, 855.
| The equilibrium speciation of dissolved components in freshwater and seawater at 25 °C and 1 atm pressure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXlsFKisbY%3D&md5=7e8ef20796c275323572dd13b9657334CAS |
[51] C. M. G. van der Berg, S. Dharmvanij, Organic complexation of zinc in estuarine interstitial and surface water samples. Limnol. Oceanogr. 1984, 29, 1025.
| Organic complexation of zinc in estuarine interstitial and surface water samples.Crossref | GoogleScholarGoogle Scholar |
[52] S. Andrade, M. J. Pulido, J. A. Correa, The effect of organic ligands exuded by intertidal seaweeds on copper complexation. Chemosphere 2010, 78, 397.
| The effect of organic ligands exuded by intertidal seaweeds on copper complexation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsFCj&md5=682cf1fa88c4020e19c946cbcc0e0874CAS | 19962173PubMed |
[53] M. T. S. D. Vasconcelos, M. F. C. Leal, Exudates of different marine algae promote growth and mediate trace metal binding in Phaeodactylum tricornutum. Mar. Environ. Res. 2008, 66, 499.
| Exudates of different marine algae promote growth and mediate trace metal binding in Phaeodactylum tricornutum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlaqsrnL&md5=d1bec56a418095f74ec982730489a16cCAS |
[54] S. Connan, D. B. Stengel, Impacts of ambient salinity and copper on brown algae: 2. Interactive effects on phenolic pool and assessment of metal binding capacity of phlorotannin. Aquat. Toxicol. 2011, 104, 1.
| Impacts of ambient salinity and copper on brown algae: 2. Interactive effects on phenolic pool and assessment of metal binding capacity of phlorotannin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsVOksr4%3D&md5=0816a9f2c5cc0b59c6a09a262c336a26CAS | 21543047PubMed |
[55] E. Peña-Vázquez, C. Pérez-Conde, E. Costas, M. C. Moreno-Bondi, Development of a microalgal PAM test method for CuII in waters: comparison of using spectrofluorometry. Ecotoxicology 2010, 19, 1059.
| Development of a microalgal PAM test method for CuII in waters: comparison of using spectrofluorometry.Crossref | GoogleScholarGoogle Scholar | 20354900PubMed |
[56] M. Brown, J. Newman, Physiological responses of Gracilariopsis longissima (S.G. Gmelin) Steentoft, L.M. Irvine and Farnham (Rhodophyceae) to sub-lethal copper concentrations. Aquat. Toxicol. 2003, 64, 201.
| Physiological responses of Gracilariopsis longissima (S.G. Gmelin) Steentoft, L.M. Irvine and Farnham (Rhodophyceae) to sub-lethal copper concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksVGrsbo%3D&md5=26d0249b753f137b5211f81b35dce636CAS | 12799112PubMed |
[57] M. P. Hurst, K. W. Bruland, The effects of the San Francisco Bay plume on trace metal and nutrient distributions in the Gulf of the Farallones. Geochim. Cosmochim. Acta 2008, 72, 395.
| The effects of the San Francisco Bay plume on trace metal and nutrient distributions in the Gulf of the Farallones.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFyqtw%3D%3D&md5=fd13fb1997a7de075d8982a28fcaf73fCAS |
[58] P. Kozelka, K. Bruland, Chemical speciation of dissolved Cu, Zn, Cd, Pb in Narragansett Bay, Rhode Island. Mar. Chem. 1998, 60, 267.
| Chemical speciation of dissolved Cu, Zn, Cd, Pb in Narragansett Bay, Rhode Island.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXivVWgsb8%3D&md5=871f76f3f7b09b774833b8cfd2be8fe1CAS |
[59] M. J. A. Rijkenberg, C. F. Powell, M. Dall‘Osto, M. C. Neilsdottir, M. D. Patey, P. G. Hill, A. R. Baker, T. D. Jickells, R. M. Harrison, E. P. Achterberg, Changes in Fe speciation following a Saharan dust event in the tropical North Atlantic Ocean. Mar. Chem. 2008, 110, 56.
| Changes in Fe speciation following a Saharan dust event in the tropical North Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXls1KqtrY%3D&md5=2104929ac1f82d5bdb2bfdcada60419aCAS |
[60] C. E. Thuróczy, L. J. A. Gerringa, M. B. Klunder, R. Middag, P. Laan, K. R. Timmermans, H. J. W. De Baar, Speciation of Fe in the Eastern North Atlantic Ocean. Deep-Sea Res. Part I Oceanogr. Res. Pap. 2010, 57, 1444.
| Speciation of Fe in the Eastern North Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar |
[61] F. L. L. Muller, Evaluation of the effects of natural dissolved and colloidal organic ligands on the electrochemical lability of Cu, Pb, and Cd in the Arran Deep, Scotland. Mar. Chem. 1999, 67, 43.
| Evaluation of the effects of natural dissolved and colloidal organic ligands on the electrochemical lability of Cu, Pb, and Cd in the Arran Deep, Scotland.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmt1Sgs7s%3D&md5=ec8bf2de0677d899013581c6fc301548CAS |
[62] M. H. Zenk, Heavy metal detoxification in higher plants – a review. Gene 1996, 179, 21.
| Heavy metal detoxification in higher plants – a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xnt1WisL0%3D&md5=d81175e57f8d6c907c1750cbe58378aeCAS | 8955625PubMed |
[63] J. Moffett, L. Brand, Production of strong, extracellular Cu chelators by marine cyanobacteria in response to Cu stress. Limnol. Oceanogr. 1996, 41, 388.
| Production of strong, extracellular Cu chelators by marine cyanobacteria in response to Cu stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XkvFKhtrk%3D&md5=d5b5da071173f67dc2551a21255eb0d8CAS |
[64] J. Lee, B. Ahner, F. Morel, Export of cadmium and phytochelatin by the marine diatom Thalassiosira weissflogii. Environ. Sci. Technol. 1996, 30, 1814.
| Export of cadmium and phytochelatin by the marine diatom Thalassiosira weissflogii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XisFagsbc%3D&md5=0255cc19dd48881b08d51becd2c4feb7CAS |
[65] R. T. Barber, J. H. Ryther, Organic chelators: factors affecting primary production in the cromwell current upwelling. J. Exp. Mar. Biol. Ecol. 1969, 3, 191.
| Organic chelators: factors affecting primary production in the cromwell current upwelling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1MXksFegur4%3D&md5=5e9533ecae7552fb7ccfe79449007bc3CAS |
[66] J. M. Sieburth, J. T. Conover, Sargassum tannin, an antibiotic which retards fouling. Nature 1965, 208, 52.
| Sargassum tannin, an antibiotic which retards fouling.Crossref | GoogleScholarGoogle Scholar |
[67] S. Lau, P. Y. Qian, Phlorotannins and related compounds as larval settlement inhibitors of the tube-building polychaete Hydroides elegans. Mar. Ecol. Prog. Ser. 1997, 159, 219.
| Phlorotannins and related compounds as larval settlement inhibitors of the tube-building polychaete Hydroides elegans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjsVertQ%3D%3D&md5=0c18b49a61d87ed802082fc0b1451ba8CAS |
[68] H. Pavia, G. Cervin, A. Lindgren, P. Aberg, Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum. Mar. Ecol. Prog. Ser. 1997, 157, 139.
| Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXntFynu74%3D&md5=4f9959ea23bd2510cab295913ed801b4CAS |
[69] K. Moebus, K. M. Johnson, J. M. Sieburth, Rehydration of desiccated intertidal brown algae: release of dissolved organic carbon and water uptake. Mar. Biol. 1974, 26, 127.
| Rehydration of desiccated intertidal brown algae: release of dissolved organic carbon and water uptake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXht1Wksb8%3D&md5=b23f4190ac4bcd26eb558171d5e6aae6CAS |
[70] R. Yang, C. M. G. van den Berg, Metal complexation by humic substances in seawater. Environ. Sci. Technol. 2009, 43, 7192.
| Metal complexation by humic substances in seawater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvFOisr8%3D&md5=4dd523dbc1cfe796a24499d8fbb032b6CAS | 19848121PubMed |
[71] R. Al-Farawati, C. M. G. van den Berg, Metal-sulfide complexation in seawater. Mar. Chem. 1999, 63, 331.
| Metal-sulfide complexation in seawater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnslKiu78%3D&md5=9238e0979633742728be7a60f554d81fCAS |
[72] B. M. Voelker, M. B. Kogut, Interpretation of metal speciation data in coastal waters: the effects of humic substances on copper binding as a test case. Mar. Chem. 2001, 74, 303.
| Interpretation of metal speciation data in coastal waters: the effects of humic substances on copper binding as a test case.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjt12mt7Y%3D&md5=af9a238f9498170e64d2df44f738e5f1CAS |
[73] M. B. Kogut, B. M. Voelker, Strong copper-binding behavior of terrestrial humic substances in seawater. Environ. Sci. Technol. 2001, 35, 1149.
| Strong copper-binding behavior of terrestrial humic substances in seawater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtFyns74%3D&md5=0084b73a3b7401a8277c1e57ddf326dbCAS | 11347927PubMed |
[74] S. Karavoltsos, A. Sakellari, S. Strecki, M. Plavsic, E. Ioannou, V. Roussis, M. Dassenakis, M. Scoullos, Copper complexing properties of exudates and metabolites of macroalgae from the Aegean Sea. Chemosphere 2013, 91, 1590.
| Copper complexing properties of exudates and metabolites of macroalgae from the Aegean Sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFGjt74%3D&md5=e7a009c8ba757c1a34e3ff87257bcfc3CAS | 23352148PubMed |
[75] J. M. Vraspir, A. Butler, Chemistry of marine ligands and siderophores. Annu. Rev. Mar. Sci. 2009, 1, 43.
| Chemistry of marine ligands and siderophores.Crossref | GoogleScholarGoogle Scholar |
[76] L. Aristilde, Y. Xu, F. M. M. Morel, Weak organic ligands enhance zinc uptake in marine phytoplankton. Environ. Sci. Technol. 2012, 46, 5438.
| Weak organic ligands enhance zinc uptake in marine phytoplankton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xltl2ht7c%3D&md5=34f50b10c57612e063736722b5c5a687CAS | 22494184PubMed |
[77] S. Meylan, R. Behra, L. Sigg, Influence of metal speciation in natural freshwater on bioaccumulation of copper and zinc in periphyton: a microcosm study. Environ. Sci. Technol. 2004, 38, 3104.
| Influence of metal speciation in natural freshwater on bioaccumulation of copper and zinc in periphyton: a microcosm study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjs1ensLg%3D&md5=96ca2b557e6d6ae2e50918cdba18400fCAS | 15224742PubMed |
[78] K. Ndungu, Model predictions of copper speciation in coastal water compared to measurements by analytical voltammetry. Environ. Sci. Technol. 2012, 46, 7644.
| Model predictions of copper speciation in coastal water compared to measurements by analytical voltammetry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XptVWmsrg%3D&md5=444517042c1aa281b640d7e89fd1c0b4CAS | 22724636PubMed |
