Transport of Cadmium Ions and its Complexes with LMWOAs across Phospholipid Bilayer
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1 Transport of Cadmium Ions and its Complexes with LMWOAs across Phospholipid Bilayer IVANA ŠESTÁKOVÁ, TOMÁŠ NAVRÁTIL, AND VLADIMÍR MAREČEK Department of Biophysical Chemistry J. Heyrovský Institute of Physical Chemistry of AS CR, v.v.i. Dolejškova 3, Prague 8 CZECH REPUBLIC tomas.navratil@jh-inst.cas.cz Abstract: - On model solutions of cadmium and selected LMWOAs (oxalic, malic or citric acid) transport conditions in the rhizosphere can be studied within the artificially prepared phospholipid bilayer membrane on the polycarbonate support. Electrochemical impedance spectroscopy (EIS) is used to monitor the formation and stability of phospholipid membrane, whereas voltammetric methods can detect species, which are transferred across the membrane. Key-Words: - Cadmium, Electrochemical impedance spectroscopy (EIS), LMWOAs, Phospholipid bilayers, Voltammetry 1 Introduction In recent years, extensive research has been conducted on estimation of the bioavailability and toxicity of metals in soils. The main routes of human exposure to toxic metals are acute exposure in the working environment (inhalation of dusts and fumes, occasionally oral intake) and acute and chronic exposure of the population through food, air, and water. Uptake of metals by plant roots is the main entry pathway into animal and human food chain. Generally, the uptake by plants depends on the concentration of metal in the soil, but overall, there is no correlation between soil metal content and plant metal content [1-3]. Uptake and toxicity of metals in higher plants best correlate with the activity of the free metal ion as is described in FIAM model from aquatic toxicology, but exceptions concerning some inorganic and also organic complexes were reported [4, 5]. Cadmium is a toxic metal, not having any metabolic role in plants or animals. The Cd damages the photosynthetic apparatus, disturbs the carbohydrate metabolism, and inhibits several enzyme activities. One of general mechanisms for Cd detoxification in plants is the chelation by cysteine-rich compounds (phytochelatins, metallothioneins) followed by the vacuolar compartmentalization. On the other hand, N and O ligands were found by X- ray absorption spectroscopy in plants tissue. [1, 6]. Using experimental setup described earlier we examined transport of cadmium ions and its complexes across model of phospholipid bilayer. We employed EIS, voltammetry and ion selective electrode. 1.1 Bioological Membrane and Cadmium channels Each real cell is surrounded by a membrane, which is mainly composed of phospholipids. Additionally, it contains a wide variety of biological molecules, primarily proteins and lipids, which take part in many cellular processes, such as ion channels, conductance, cell signaling etc. To elucidate such transport processes, synthetically prepared model phospholipid bilayers (PLBs) are utilized, in the form of black membranes, vesicles or supported membranes [7-10] with ion channels incorporated (either artificially synthesized or obtained from real living cells). The biological membrane exists as a surface, at which the hydrophobic parts of phospholipids (PL) are protected from water, while the hydrophilic ones are in contact with the aqueous medium. Only the ends or edges of the bilayer surface are exposed to unfavorable conditions, however, even these exposed regions can be eliminated by bending them underneath the surface whereby a closed edgeless structure is formed. The closed bilayer is impermeable for most of water soluble molecules, as they would be insoluble in the hydrophobic bilayer core [8-10]. The rate of diffusion of organic molecules nonelectrolytes depends on their ISBN:
2 lipid-water distribution coefficient. The higher is the molecular solubility in fats, the faster is the diffusion rate across the membrane. Compounds insoluble in fats are transported across amphipathic proteins and can be dipped into equally oriented lipid bilayer [7-9]. The proteins form channels for ions and small molecules and serve for transport of bigger molecules, which would not be otherwise able to pass across the bilayer. Over the past ten years it was assumed that for Cd 2+ as non-essential metal ion, there would be no specific uptake mechanism and Cd 2+ would enter plant cells via uptake systems for essential cations. Mostly indirect evidences are available now that Cd is taken up into plant cells by Fe 2+, Ca 2+ and Zn 2+ transporters/channels (LCT1, ZIP family of metal transporters, Nramp family). Only exception is Thlaspi caerulescens, where evidences for a Cd specific uptake system were described [11-13]. In the present study, we used the A23187 ionophore (calcimycin), where in our previous research [8, 9] transport of cadmium ions was confirmed. 1.2 Low Molecular Weight Organic Acids Low Molecular Weight Organic Acids (LMWOAs) are encountered mainly as important root exudates, influencing processes in the rhizosphere. They can form different complexes with metals and influence solubility, mobilization and uptake by plant [14] Apart of this, citrate, malate, and oxalate have been implicated in metal transport through the xylem and vacuolar metal sequestration [6, 15, 16]. Voltammetry has been utilized in the study of cadmium and lead complexes with oxalic acid [17-19] and structure of complexes was confirmed with ESI -MS measurement [20-22]. Using voltammetry, we can also confirm the presence of oxalic acid in the solutions after transport across the phospholipid bilayer. 2 Experimental The electrochemical impedance spectroscopy measurements were realized using CHI 650C Electrochemical Analyzer/Workstation, Software: CHI v 8.1 (IJ Cambria Scientific, UK) and Potentiostat No. 283 and FRA No. 1025, No (Princeton Applied Research, USA). The electrochemical impedances were determined using silver/silver chloride electrodes (silver wire, diameter 1 mm, electroplated by silver chloride). Platinum wire, diameter 1 mm, served as the auxiliary electrode. The voltammetric determinations of cadmium ions or its complexes were carried out by the PCcontrolled voltammetric analyzer ECO-TRIBO polarograph (Polaro-Sensors, Prague, Czech Republic), equipped with POLAR.PRO software v. 5.1 and with MultiElchem v. 2.1 software (J. Heyrovský Institute of Physical Chemistry of AS CR, v.v.i., Czech Republic). Pen-type electrode HMDE [23, 24] was used as the working electrode, Ag/AgCl/KCl(3 mol.l -1 ) electrode to which all potentials are referred to and platinum wire served as a counter electrode (both Elektrochemické Detektory, Turnov, Czech Republic). For the determination of cadmium ions, the sample was acidified by addition of HNO 3, Suprapur (Merck, Czech Republic), to ph 1. For the complexes with oxalic acid, ph of the solution was adjusted to desired value ( ) with NaOH. Differential pulse anodic stripping voltammetry (DPASV ) was performed at conditions: E acc = -850 mv, E in = -700 mv, E fin = -200 mv, scan rate 10 mv.s -1, pulse amplitude 50mV. A new drop was used for each record; measurement has been realized in nitrogen atmosphere. Determination of hazardous (heavy) metal ions (Cd 2+, Pb 2+, etc.) and their complexes, transport of which across the PLBs is presented in this manuscript, and of many other organic as well as of inorganic compounds using voltammetric methods with various working electrodes, was many times described in literature and our research group has been developing such analytical methods over many decades (e.g., with hanging mercury drop electrode (e.g., [25-33]). Nevertheless, it has been reported that the solid electrodes can be successfully used for voltammetric determinations of the mentioned transported environmentally important species. Our research team has been dealing with development and application of such types of electrodes, e.g., solid amalgam electrodes (silver, copper, etc.) (polished, film, mercury meniscus modified etc.) (e.g., [34-41]), composite solid electrodes (silver, graphite, gold, etc.) (e.g., [35, 42-51]), and solid amalgam composite electrodes for many years (e.g., [35, 47]). The experiments described in this manuscript were realized with 1,2-dipalmitoyl-sn-glycero-3- phosphocholine (lecithin, DPPC, GPCho (16:0/16:0), CAS No ) (Avanti Polar Lipids, Alabaster, USA). The PLBs were formed by self-assembling in the holes of the Isopore Membrane Filters (Millipore, USA) polycarbonate, ISBN:
3 hydrophilic 8.0 µm, and the supporting membrane thickness amounted to 7-22 µm. The area of one pore amounted to 50 µm 2, the experimentally found porosity of the membranes was about %. For determination of CO 2, gas electrode (Monokrystaly Turnov, Czech Republic) was used. 3 Results and Discussion 3.1 Phospholipid Membrane Preparation The 1,2-dipalmitoyl-sn-glycero-3-phosphocholine monohydrate was used for preparation of PLB on porous membranes: The capacity of membranes increases with time after the bilayer formation, until a steady-state value attained some min. later [22]. In our experiments, there were the PLBs formed as self-assembled in the holes of the supporting membrane (Isopore Membrane Filters, Millipore, USA; polycarbonate, hydrophilic, 2.0 or 8.0 µm, and thickness 7-22 µm) by application of 10 µl of phospholipid solutions in n-heptane on the membrane surface. These membranes (supports) were glued on the plastic cup(s) of the polypropylene electrochemical cell, which was together with electrolyte 1 and working electrode inserted into second part of the cell, containing electrolyte 2, reference, and auxiliary electrode [8-10]. Formation of PLB was monitored by ESI measurement. After steady state has been reached, changes of electrolyte 1 were realized (change of ph, addition of metal ions, LMWOA) and to them the PLB was exposed for exactly 1 hour. Subsequently, voltammetric analysis of the electrolyte 2 has been performed. 3.2 Voltammetric Analysis The Cd and Pb complexes with oxalic acid (OA) were detected in model solution of sodium perchlorate, using differential pulse anodic stripping voltammetry and differential pulse cathodic stripping voltammetry. When the ph of the model solutions were adjusted to ph 7 with sodium hydroxide, a mixed complex consisting of Cd, Pb and OA was found, its peak potential varied from to mv (vs. Ag/AgCl/KCl sat.) and depended on the Pb:Cd or Cd:Pb ratio. According to calculated stability constants [19], highest values were obtained for mixed complex Cd-OA-Pb, in comparison with single complexes of OA with Pb and Cd (Pb-OA and Cd-OA). The existence of all focused metal complexes is confined to neutral or weakly acidic medium. In acidic medium (ph 2) in model and soil solutions do not exist any Pb or Cd complexes, all Cd and Pb were presented in free ionic forms [17-19]. The formation of mixed Cd- OA-Pb complex was employed for detection of transport of oxalic acid across the phospholipid membrane, for which the adjustment of electrolyte 1 to ph 7.5 was important. Under such condition, transport of oxalic acid has been proved also by ESI-MS. On the other hand, without presence of oxalic acid, cadmium ions by themselves at ph 7.5 were not transported [20-22]. From those experiments conclusion was made that the contact of oxalic acid in solution of ph 7.5 influences permeability of PLB. Formation of carbon dioxide at ph 7.5 has been confirmed by CO 2 -ISE and possibility of formation of pores in PLB is considered. For other two acids of interest, Cd-malate and Cd- citrate at ph 7.5 exhibited similar influence on PLB in our experimental setup. Composition of electrolyte 1 was M Cd 2 +, M citric or malic or oxalic acid, 0.1 M KCl, ph 7.5 Percentage of Cd found in electrolyte 2 was: 0.3% for Cd-citrate, 0.56% for Cd-malate and 2.6% for Cd-oxalate. This is in agreement with order of massiveness of CO 2 evolution in ESI-MS measurement [14]. For Cd-oxalate at ph 7.5 under same Cd concentration ( M Cd 2+ ) linear increase of % Cd passed through PLB was detected in the dependence on the amount of added oxalic acid into electrolyte 1 (R 2 = 0.788). In the following experiment, the ionophore A23187 (Fig.1) has been incorporated into PLB. When steady state of PLB has been reached, solution of 0.1 M KCl as electrolyte1 was changed for CdOA at ph 6.5, where presence of the Cd complex has been confirmed by voltammetry. After 1 hour of exposition, in electrolyte 2 both, Cd and oxalic acid were detected (Fig.2) In this case, no CO 2 development takes place and therefore, using ionophore A23187, passage of whole complex CdOA seems plausible. Further experiments with citric and malic acids are in progress. Fig.1 Formula of the ionophore calcimycin ISBN:
4 Fig.2 (a) model solution of 0.1 M KCl with M OA, M Cd 2+ and M Pb 2+ ; (b) electrolyte 2 from experiment with ionophore A23187, addition of M Pb Conclusion Two possible ways of cadmium complexes with LMWOAs transport across the phospholipid membrane were found. One of them requires ph above 7.5, under which condition CO 2 is released from LMWOAs. The transport of cadmium oxalate was realized using ionophore calcimycin, incorporated into the membrane. Acknowledgements The authors gratefully acknowledge financial support by the Grant Agency of the Academy of Sciences of the Czech Republic (project No. IAA ) and by the Czech Science Foundation (project No. P206/11/1638). References: [1] S. Clemens, Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants, Biochimie, Vol. 88, No. 11, 2006, pp [2] V. M. Nurchi and I. Villaescusa, Agricultural biomasses as sorbents of some trace metals, Coordination Chemistry Reviews, Vol. 252, No , 2008, pp [3] S. Sauve, W. A. Norvell, M. McBride, and W. Hendershot, Speciation and complexation of cadmium in extracted soil solutions, Environmental Science & Technology, Vol. 34, No. 2, 2000, pp [4] M. Megharaj, G. S. R. Krishnamurti, and R. Naidu, Bioavailability of cadmium-organic complexes to soil alga - An exception to the free ion model, Journal of Agricultural and Food Chemistry, Vol. 52, No. 12, 2004, pp [5] A. L. Nolan, E. Lombi, and M. J. McLaughlin, Metal bioaccumulation and toxicity in soils - Why bother with speciation?, Australian Journal of Chemistry, Vol. 56, No. 2-3, 2003, pp [6] Z. G. Wei, J. W. Wong, F. H. Hong, H. Y. Zhao, H. X. Li, and F. Hu, Determination of inorganic and organic anions in xylem saps of two contrasting oilseed rape (Brassica juncea L.) varieties: Roles of anions in long-distance transport of cadmium, Microchemical Journal, Vol. 86, No. 1, 2007, pp [7] L. Rose and A. T. A. Jenkins, The effect of the ionophore valinomycin on biomimetic solid supported lipid DPPTE/EPC membranes, Bioelectrochemistry, Vol. 70, No. 2, 2007, pp [8] T. Navratil, I. Sestakova, J. Jaklova Dytrtova, M. Jakl, and V. Marecek, in 7th WSEAS International Conference on Environment, Ecosystems and Development 2009 Eds: M. Otesteanu, S. Celikyay, N. Mastorakis, S. Lache, and F. K. Benra), World Scientific and Engineering Acad. and Soc., Puerto de la Cruz, SPAIN, pp [9] T. Navratil, I. Sestakova, J. Jaklova Dytrtova, M. Jakl, and V. Marecek, Study of charged particles transport across model and real phospholipid bilayers, WSEAS Transactions on Environment and Development, Vol. 6, No. 3, 2010, pp [10] T. Navratil, I. Sestakova, K. Stulik, and V. Marecek, Electrochemical Measurements on Supported Phospholipid Bilayers: Preparation, Properties and Ion Transport Using Incorporated Ionophores, Electroanalysis, Vol. 22, No , 2010, pp [11] E. Lombi, F. J. Zhao, S. P. McGrath, S. D. Young, and G. A. Sacchi, Physiological evidence for a high-affinity cadmium transporter highly expressed in a Thlaspi caerulescens ecotype, New Phytologist, Vol. 149, No. 1, 2001, pp ISBN:
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