Potentiometric determination of copper complexation by phytoplankton exudates
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1 538 Notes Limnol. Oceanogr., 23(3), 1978, by the American Society of Limnology and Oceanography, Inc. Potentiometric determination of copper complexation by phytoplankton exudates A&tract-Potentiometric copper titrations were done on culture media in which eight algal species, Thalassiosira pseudonana (3H), Ankistrodesmus falcatus, Chlamydomonas sp., Pediastrum sp., Staurastrum gracile,, Tribonema sp., and Cyclotella cryptica were grown to cell concentrations of 105-lo6 cells. ml-. The results demonstrate that only G. gigas produces extracellular organic compounds that can measurably reduce the cupric ion activity in 1 x low6 M total copper. It has been speculated that organic compounds released by phytoplankton might complex trace metals both in culture experiments and in natural waters. Such complexations could result in a conditioning of the cell s external milieu through which essential metals are made available (Johnston 1964; Barber 1973; Barber and Ryther 1969; Barber et al. 1971) or toxic metals are rendered inactive (Fogg and Westlake 1955; Steemann Nielsen and Wium-Andersen 1970; Steemann Nielsen et al. 1969; Davey et al. 1973; Jackson and Morgan 1978). The case for metal availability through complexation has been argued mostly for iron and still lacks positive demonstration. The repression of toxicity by complexing agents has been documented quantitatively in phytoplankton cultures using well characterized artificial chelating agents and copper as the toxicant (Sunda and Guillard 1976; Anderson and Morel 1978). Evidence for repression of toxicity by complexing organic compounds released by phytoplankton rests on interpretation of bioassay experiments (e.g. Huntsman and Barber 1975; Steemann Nielsen and Wium-Andersen 1971). Research supported in part by National Science Foundation grant DES and in part by Office of Sea Grant (NOM) R. R. L. Guillard critically reviewed the manuscript and A. Loeblich and R. R. L. Guillard selected the algal species. Our study was undertaken to measure directly any decrease in cupric ion activity in culture media caused by complexation of copper by exuded extracellular organic compounds. Because of the background work done on the effect of copper and organic chelators on Thalassiosira pseudonana (3H) by Sunda and Guillard (1976), we chose this euryhaline diatom for extensive study. Another euryhaline species (Chlorella sp.) and seven freshwater species (Ankistrodesmus fulcutus, Chlamydomonas sp., Pediustrum sp., S tuurustrum grucile, Gloeocystis gigus, Tribonemu sp., and CycZoteZZu cryptica) known to produce substantial amounts of extracellular organic material were also screened for evidence of the release of Cu( II) complexing organics. The results for Chlorella sp. were u-reproducible and are not included below. The use of the cupric ion selective electrode for mea- suring cupric ion activity precluded the use of seawater medium because of chlo- Table 1. Composition of culture medium. Salts and Nutrients Final Molarity CaClz. 2 Hz0 2.5 x 1O-4 MgS04*7 Hz0 1.5 x 1o-4 NaHC x 1o-5 K,HP x 1o-5 NaNO, 1.0 x 1o-3 NazSi03*9 Hz0 1.0 x 1o-4 Borate (9.6 mg. liter- ) Trace Metals CuSO4.5 Hz0 1.0 x 1o-g (NH,),Mo,0,,~4 HzD 1.5 x 1o-g CoClz* 6 Hz0 2.5 x lo- MnC12.4 Hz0 2.3 x lo- ZnClz.7 Hz0 4.0 x 1o-g FeC13* 6 Hz0 1.0 x 1o-5 Final Vi tamins Concentration Bl, 5.5 x lo- geliter- Biotin 5.0 x lo- g-liter- Thiamine HCL 1.0 x 10v4 g* liter-
2 Notes 539 Table 2. Sample details. Y% sample Cell CU*+ concn when Ty compkfiltered titration ation Guillard s collection (WHOI) Thalassiosira pseudonana (3H) 1 x lo6 I,11 - Thalassiosira pseudonana (3H) * I,11 - Chlamydomonas sp. G6 2 x lo! II - Tribonema sp x 105$ II - Cyclotella cryp tica O-3A 1 x lo5 II - Loeblich s collection (Harvard Univ.) IU291 2 x lo5 II + IU291 2 x lo5 II + IU291 2 x lo5 I + Ankistrodesmus falcatus IU x lo6 II - Pediastrum sp x 105$ II - S taurastrum gracile IU562 4 x lo4 II - * Poststationary phase culture. No cells visible under microscope. t lo- M co per added to culture medium. 4 Chain count multiplied by cel1s.c K. au+. Q Clone count multiplied by cells.clone-. ride interference with the electrode (Westall 1977). All algal cultures were grown aseptically in batch under continuous light ( PEin. rnh2. s-l) and constant temperature (20 C). The composition of the culture medium is given in Table 1. The significant feature of this medium is that it contains no artificial chelator. We could grow cultures without added chelator by adding 0.1 ml of freshly prepared M FeC13 to 250 ml of culture medium at the time of inoculation. This may have enhanced the availability of iron, or reduced the availability of toxic metals by their adsorption on precipitated iron hydroxide colloid (Stumm and Morgan 1970). We prepared samples for titration by removing the cells by gentle filtration (<130-mm Hg vacuum) to minimize cell lysis. Table 2 details the samples. Except for the poststationary phase T. pseudonana cultures, all samples were filtered in the stationary growth phase. If we assume that an organic complex x G 10-5 Fig. 1. pcu* vs. total copper for total glycine = 5 x 10e6 M with ph = for full range of titration. ing agent is a weak acid of the form HL, complexation of cupric ion by this compound can be represented by Cu2+ + HL = CuL+ + H+ *KCuL. (1) Two types of potentiometric titrations may be used to study this reaction: one in which ph is varied at constant total copper concentration, the other in which total copper is varied. We used both. Two factors govern the limit of detection of the titration. First, the total ligand concentration has to be within the linear response range of the electrode. With special care this range can be extended down to 1O-7 M; however, in this preliminary study, it has been kept conservatively at Lr > 10m6 M. Second, the difference between the titration of the sample and that of the blank has to be greater than the variability among several blank titrations. This variability is much greater than the electrode noise and of the order of 3 mv. By expressing the mass law for Eq. 1, rearranging, and taking the logarithms, a limiting condition is obtained: log *&ul*lt w+) = 1 (2) Experimental confirmation of these results is shown in Fig. 1, where 5 x 10d6 M glycine can be detected by this meth- I Ill
3 540 Notes Fig. 2. Type I titrations of Thalassiosira pseudonana samples with 4 x 10P6 M total copper. l - Medium blank; x-salt blank; A-stationary phase od (*KcuGLY = 10-l: Sillen and Martell 1971; ph = 6.4). A more complete theoretical treatment of these techniques is given by Sunda (1975) and Westall (1977). Titration method I: Variable ph-a 50-ml sample was adjusted to ph 4 with 0.05 N HN03 and purged of COZ. The titration vessel was closed to the atmosphere and continuously bubbled with N, to exclude CO,. Cupric nitrate solution was added to yield a final copper concentration of 4 x lop6 M and the sample was allowed to equilibrate. Cupric ion activity was measured with a Radiometer Selectrode model F 3000 cupric ion selective electrode and ph with an Orion model glass electrode against an Orion double junction reference electrode. The cupric ion activity was computed from the cupric ion selective electrode reading by -log(cl?+) = pcu* = 4 + I$$ (3) where E is the electrode reading for 10e4 M copper addition in that experiment (it varied <5 mv among experiments) and 29 mv is the slope of the electrode, observed to be constant within 1 mv. When both electrode responses were stable (~2 mv* h-l drift), an increment of carbonatefree 0.05 N NaOH (Skoog and West 1963) was added and the sample was allowed Fig. 3. Type II titrations of Thalassiosira pseudonana samples. At initial ph 6: O-salt blank; O-medium blank; D-stationary phase culture; x-poststationary phase culture. At initial ph 7: A-medium blank; +-stationary phase culture. to re-equilibrate. Equilibration took up to 2 h in the neighborhood of the break point. In this manner a pcu* vs. ph curve was generated. Titration method II: Variable pcu- The same C02-free system was used. After the purge of CO2 at ph 4, the sample ph was adjusted upward with carbonatefree base to ph 6-7. The choice of ph was a compromise between optimizing the condition of Eq. 2 and avoiding the complications arising from formation of copper hydrolysis species. After equilibration, CU(NO~)~ was added incrementally to give a total copper concentration ranging from 1 x lop6 M to 1 x 10e4 M. Again the sample was allowed to re-equilibrate between additions. No buffering of these samples was attempted because of the possibility that buffers in this range would themselves complex copper. Consequently, ph decreased by as much as one ph unit during the course of the titrations. This method was therefore used only to screen samples for evidence of copper complexation; any positive result was confirmed by the more time-consuming titration method I. Figures 2 and 3 show the results for T. pseudonana (3H). The type I titrations presented in Fig. 2 were performed on a
4 Notes 541 PC a.0 - \ I I I I I I I I I a 9 PH Fig. 5. Type I titrations of Gloeocystis gigus sample and salt blank with 4 x 1O-6 M total copper: x-salt blank; O--G. gigus (III).,.,c,,,,, / / 11,,,,, l l rj I o-6 10-S 10-4 Fig. 4. Type II titrations of samples of freshwater species at initial ph 6.4: O-Ankistrodesmus fulcutus; l -Tribonemu sp.; A-Chlamydomonas sp.; A-Stuurustrum grucile; x-pediustrum sp.; +-CycZoteZZu cryptica; +-medium blank; CI- Gloeocystis gigus (I); W-G. gigus (II). stationary phase culture, a salt blank consisting of 10m3 M KN03 solution, and a medium blank consisting of sterile culture medium. No evidence of copper complexation, which would have caused the curve to break at lower ph, was found in the sample. The results of the type II titrations for T. pseudonana at initial ph 6 and 7 are given in Fig. 3. Again no evidence of copper complexation was found at either ph. Variations in the initial electrode potentials arise from small variations in initial ph. Type II titrations of the other species at initial ph 6.4 are presented in Fig. 4. There is evidence of substantial complexation only in the culture of G. gigas. The break in the type I titration curve (Fig. 5) occurs at a lower ph in the sam- ple than in the salt blank, indicating complexation by a species other than OH-. Although preliminary, this work presents direct evidence that certain phytoplankters can produce extracellular organic compounds capable of appreciably complexing copper. From the data of Figs. 4 and 5, the complexing agent released by G. gigas is calculated to be present at a concentration of about 5 x 10e6 M and has a formation constant for copper *Kc,, = 1 (compared with the weak chelator, glycine: Fig. 1). Under the culture conditions (ph = 7, Alk = lo- ), Cu(I1) is computed to exist predominantly as the organic complex. The ratio of total copper to the free cupric ion activity is of the order of 10. Free cupric ion activity may be further reduced by adsorption on ferric hydroxide. In culture media containing strong artificial chelating agents (EDTA, NTA, etc.), the influence of the exuded organic material would be negligible. In natural waters, where the algal densities are likely to be lower than the stationary phase value of 2 x lo5 cells*mlll in the experiments, the extent of complexation would presumably decrease proportionally. Although our results with G. gigas warrant further study, we can speculate that the complexation is only a by-product of the release of large amounts of mucilageneous material. It is worth emphasizing that out of eight phytoplankton species selected for their known release of copious organic material, only one significantly altered copper speciation in the culture medium. Complexing agents in concentrations below 1 PM would not have been detected by the titrations,
5 542 Notes even if they depressed the cupric ion ac- complexation capacity of seawater. Limnol. tivity appreciably under the culture con- Oceanogr. 18: ditions. Such ligands in the 10e8 to 10e6 FoGG,G. E., AND D.F. WESTLAKE Theimportance of extracellular products of algae in M range would have to be relatively fresh water. Int. Ver. Theor. Angew. Limnol. strong complexing agents (K*cuL z lo"), Verh. 12: stronger, for example, than any amino HUNTSMAN, S. A.,AND R. T. BARBER Modacid. There is evidence of release of ification of phytoplankton growth by excreted compounds in low-density populations. J. Phystrong iron complexing agents by blue- col. 11: green algae (Murphy et al. 1976), but this JACKSON, G. A., AND J. J. MORGAN Trace result can hardly be generalized to other metal-chelator interactions and phytoplankton metals and to eukaryotic algae. The ques- growth in seawater media: Theoretical analysis tion of the release of strong copper com- and comparison with reported observations. Limnol. Oceanogr. 23: plexing agents under conditions of cop- JOHNSTON, R Seawater, the natural medium per toxicity remains open. phytoplankton. 2. Trace metals and chelation, and general discussion. J. Mar. Biol. Assoc. K. C. Swallow U.K. 44: J. C. Westall MURPHY, T. P., D. R. LEAN, AND C. NALEWAJKO Blue-green algae: Their excretion of Department of Chemistry iron-selective chelators enables them to domi- Massachusetts Institute of nate other algae. Science 192: Technology SILL~N, L.G., AN; A.E. MARTELL Stability Cambridge constants of metal ion complexes. Suppl. 1. Chem. Sot. Lond. Spec. Publ. 25. D. M. McKnight SKOOG, D. A., AND D. M. WEST Fundamen- N. M. L. Morel tals of analytical chemistry. Holt, Rinehart and Winston. F. M. M. Morel STEEMANN NIELSEN, E.,L. KAMP-NIELSEN,AND S. Ralph M. Parsons Laboratory for Water WIUM-ANDERSEN The effect of deleterious concentrations of copper on the photosyn- Resources and Hydrodynamics Department of Civil Engineering Massachusetts Institute of Technology References ANDERSON, D. M., AND F. M. MOREL Copper sensitivity of Gonyaulux tamarensis. Limnol. Oceanogr. 23: BARBER, R. T Organic ligands and phytoplankton growth in nutrient-rich seawater, p Zn P. Singer [ed.], Trace metals and metal organic interaction in natural waters. Ann Arbor Sci. -, R. C. DUGDALE, J.J. MACISAAC, AND R. L. SMITH Variations in phytoplankton growth associated with the source and conditioning of upwelling water. Invest. Pesq. 35: AND J. H. RYTHER Organic chelatois: Factors affecting primary production in the Cromwell Current Upwelling. J. Exp. Mar. thesis of Chlorella pyrenoidosu. Physiol. Plant. 22: AND S. WIUM-ANDERSEN Copper ions as poison in the sea and in freshwater. Mar. Biol. 6: ,AND The influence of copper on photosynthesis and growth in diatoms. Physiol. Plant. 24: STUMM, W., AND J. J. MORGAN Aquatic chemistry. Wiley-Interscience. SUNDA, W. G The relationship between cupric ion activity and the toxicity of copper to phytoplankton. Ph.D. thesis, Woods Hole Oceanogr. Inst. and Mass. Inst. Technol., Woods Hole and Cambridge. -, AND R. R. GUILLARD The relationship between cupric ion activity and the toxicity of copper to phytoplankton. J. Mar. Res. 34: WESTALL, J. C Chemical methods for the study of metal-ligand interactions in aquatic environments. Ph.D. thesis, Mass. Inst. Technol., Cambridge. Biol. Ecol. 3: DAVEY, E. W.,J. J. MORGAN, AND S. J. ERICKSON. Submitted: 21 March A biological measurement of the copper Accepted: 28 July 1977
Release of weak and strong copper-complexing
Limnol. Oceanogr., 24(5), 1979, 823-837 @I 1979, by the American Society of Limnology and Oceanography, Inc. Release of weak and strong copper-complexing agents by algae1 Diane M. McKnight and Fruncois
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