CSIRO Publishing blank image blank image blank image blank imageBooksblank image blank image blank image blank imageJournalsblank image blank image blank image blank imageAbout Usblank image blank image blank image blank imageShopping Cartblank image blank image blank image You are here: Journals > Environmental Chemistry   
Environmental Chemistry
Journal Banner
  Environmental problems - Chemical approaches
 
blank image Search
 
blank image blank image
blank image
 
  Advanced Search
   

Journal Home
About the Journal
Editorial Boards
Contacts
Content
Online Early
Current Issue
Just Accepted
All Issues
Virtual Issues
Special Issues
Research Fronts
Sample Issue
For Authors
General Information
Notice to Authors
Submit Article
Open Access
For Referees
Referee Guidelines
Review Article
For Subscribers
Subscription Prices
Customer Service

blue arrow e-Alerts
blank image
Subscribe to our Email Alert or RSS feeds for the latest journal papers.

red arrow Connect with us
blank image
facebook twitter youtube

 

Article << Previous     |     Next >>   Contents Vol 11(2)

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

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 http://dx.doi.org/10.1071/EN13085
Submitted: 24 April 2013  Accepted: 15 June 2013   Published: 26 September 2013


 
PDF (510 KB) $25
 Supplementary Material
 Export Citation
 Print
  

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.
CrossRef | CAS | PubMed |

[4]  B. L. Vallee, D. S. Auld, Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry 1990, 29, 5647.
CrossRef | CAS | PubMed |

[5]  S. Clemens, Molecular mechanisms of plant metal tolerance and homeostasis. Planta 2001, 212, 475.
CrossRef | CAS | PubMed |

[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.
CrossRef | CAS |

[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.
CrossRef |

[9]  E. Pinto, T. S. Kutner, M. Leitão, Heavy metal induced oxidative stress in algae. J. Phycol. 2003, 39, 1008.
CrossRef | CAS |

[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.
CrossRef | CAS | PubMed |

[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.
CrossRef |

[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.
CrossRef | CAS | PubMed |

[13]  L. C. Rai, J. P. Gaur, H. D. Kumar, Phycology and heavy metal pollution. Biol. Rev. Camb. Philos. Soc. 1981, 56, 99.
CrossRef | CAS |

[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.
CrossRef | CAS |

[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.
CrossRef | CAS |

[16]  M. Ellwood, C. M. G. van den Berg, Zinc speciation in the Northeastern Atlantic Ocean. Mar. Chem. 2000, 68, 295.
CrossRef | CAS |

[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.
CrossRef | CAS |

[18]  P. J. M. Buckley, C. M. G. van den Berg, Copper complexation profiles in the Atlantic Ocean. Mar. Chem. 1986, 19, 281.
CrossRef | CAS |

[19]  K. H. Coale, K. W. Bruland, Copper complexation in the Northeast Pacific. Limnol. Oceanogr. 1988, 33, 1084.
CrossRef | CAS |

[20]  J. W. Moffett, Temporal and spatial variability of copper complexation by strong chelators in the Sargasso Sea. Deep-Sea Res. 1995, 42, 1273.
CrossRef | CAS |

[21]  K. W. Bruland, Complexation of zinc by natural organic ligands in the central North Pacific. Limnol. Oceanogr. 1989, 34, 269.
CrossRef | CAS |

[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.
CrossRef |

[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.
CrossRef | CAS |

[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.
CrossRef | CAS |

[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.
CrossRef | CAS |

[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.
CrossRef | CAS |

[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.
CrossRef | CAS | PubMed |

[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.
CrossRef | CAS |

[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.
CrossRef | CAS |

[31]  L. Laglera, C. M. G. van den Berg, Copper complexation by thiol compounds in estuarine waters. Mar. Chem. 2003, 82, 71.
CrossRef | CAS |

[32]  D. Tang, K. Warnken, P. Santschi, Organic complexation of copper in surface waters of Galveston Bay. Limnol. Oceanogr. 2001, 46, 321.
CrossRef | CAS |

[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.
CrossRef | CAS |

[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.
CrossRef | CAS |

[35]  R. Town, M. Filella, A comprehensive systematic compilation of complexation parameters reported for trace metals in natural waters. Aquat. Sci. 2000, 62, 252.
CrossRef |

[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.
CrossRef | CAS |

[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.
CrossRef | CAS |

[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.
CrossRef | CAS | PubMed |

[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.
CrossRef | CAS |

[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.
CrossRef | CAS |

[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.
CrossRef | CAS |

[42]  R. J. M. Hudson, E. L. Rue, K. W. Bruland, Modeling complexometric titrations of natural water samples. Environ. Sci. Technol. 2003, 37, 1553.
CrossRef | CAS |

[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.
CrossRef | CAS | PubMed |

[44]  D. R. Kester, I. W. Duedall, D. N. Connors, Preparation of artificial seawater. Limnol. Oceanogr. 1967, 12, 176.
CrossRef | CAS |

[45]  M. Kitajima, W. L. Butler, Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochem. Biophys. Acta 1975, 376, 105.
CrossRef | CAS | PubMed |

[46]  L. M. Laglera, C. M. G. van den Berg, Copper complexation by thiol compounds in estuarine waters. Mar. Chem. 2003, 82, 71.
CrossRef | CAS |

[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.
CrossRef |

[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.
CrossRef | CAS |

[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.
CrossRef | CAS |

[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.
CrossRef | CAS |

[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.
CrossRef |

[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.
CrossRef | CAS | PubMed |

[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.
CrossRef | CAS |

[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.
CrossRef | CAS | PubMed |

[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.
CrossRef | PubMed |

[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.
CrossRef | CAS | PubMed |

[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.
CrossRef | CAS |

[58]  P. Kozelka, K. Bruland, Chemical speciation of dissolved Cu, Zn, Cd, Pb in Narragansett Bay, Rhode Island. Mar. Chem. 1998, 60, 267.
CrossRef | CAS |

[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.
CrossRef | CAS |

[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.
CrossRef |

[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.
CrossRef | CAS |

[62]  M. H. Zenk, Heavy metal detoxification in higher plants – a review. Gene 1996, 179, 21.
CrossRef | CAS | PubMed |

[63]  J. Moffett, L. Brand, Production of strong, extracellular Cu chelators by marine cyanobacteria in response to Cu stress. Limnol. Oceanogr. 1996, 41, 388.
CrossRef | CAS |

[64]  J. Lee, B. Ahner, F. Morel, Export of cadmium and phytochelatin by the marine diatom Thalassiosira weissflogii. Environ. Sci. Technol. 1996, 30, 1814.
CrossRef | CAS |

[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.
CrossRef | CAS |

[66]  J. M. Sieburth, J. T. Conover, Sargassum tannin, an antibiotic which retards fouling. Nature 1965, 208, 52.
CrossRef |

[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.
CrossRef | CAS |

[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.
CrossRef | CAS |

[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.
CrossRef | CAS |

[70]  R. Yang, C. M. G. van den Berg, Metal complexation by humic substances in seawater. Environ. Sci. Technol. 2009, 43, 7192.
CrossRef | CAS | PubMed |

[71]  R. Al-Farawati, C. M. G. van den Berg, Metal-sulfide complexation in seawater. Mar. Chem. 1999, 63, 331.
CrossRef | CAS |

[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.
CrossRef | CAS |

[73]  M. B. Kogut, B. M. Voelker, Strong copper-binding behavior of terrestrial humic substances in seawater. Environ. Sci. Technol. 2001, 35, 1149.
CrossRef | CAS | PubMed |

[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.
CrossRef | CAS | PubMed |

[75]  J. M. Vraspir, A. Butler, Chemistry of marine ligands and siderophores. Annu. Rev. Mar. Sci. 2009, 1, 43.
CrossRef |

[76]  L. Aristilde, Y. Xu, F. M. M. Morel, Weak organic ligands enhance zinc uptake in marine phytoplankton. Environ. Sci. Technol. 2012, 46, 5438.
CrossRef | CAS | PubMed |

[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.
CrossRef | CAS | PubMed |

[78]  K. Ndungu, Model predictions of copper speciation in coastal water compared to measurements by analytical voltammetry. Environ. Sci. Technol. 2012, 46, 7644.
CrossRef | CAS | PubMed |


   
Subscriber Login
Username:
Password:  

 
    
Legal & Privacy | Contact Us | Help

CSIRO

© CSIRO 1996-2014