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Jun 2 7 1995 CADMIUM: A TOXIN AND A NUTRIENT FOR MARINE PHYTOPLANKTON by Jennifer Grant Lee B.S., Yale University (1986) SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY at the MASSACHUSETTS INSTITUTE OF TECHNOLOGY and the WOODS HOLE OCEANOGRAPHIC INSTITUTION June 1995 @ 1995 Massachusetts Institute of Technology All rights reserved Signature of Author / /oint Program in Oceanography 'Massachusetts Institute of Technology/ Woods Hole Oceanographic Institution Certified by 6 Frangois M.M. Morel Thesis Supervisor Accepted by DanielRepeta Chairman, Joint Committee for Chemical Oceanography Massachusetts Institute of Technology/ MASSACHIS~TT~. INSTITUTE= Woods Hole Oceanographic Institution JUN 2 7 1995 Barer EIn CADMIUM: A TOXIN AND A NUTRIENT FOR MARINE PHYTOPLANKTON by JENNIFER GRANT LEE Submitted to the MIT/WHOI Joint Program in Chemical Oceanography on May 5, 1995 in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Chemical Oceanography Abstract Although cadmium is known to be very toxic, it exhibits nutrient-like vertical concentration profiles in the open ocean. Here I show that cadmium is a nutrient for the marine diatom Thalassiosiraweissflogii, a chlorophyte and some prymnesiophytes at inorganic zinc and cadmium concentrations typical of surface sea water (although cadmium cannot completely replace zinc). Very low concentrations of inorganic cadmium (5pM) that are beneficial under conditions of moderate zinc limitation (3pM) become toxic in cultures severely limited by zinc (0.2pM). The role of cadmium as an algal nutrient is thus observable in a narrow, species-specific range of inorganic zinc and cadmium concentrations. Detailed studies of T. weissflogii show that over a wide range of external inorganic cadmium (5-500pM) and inorganic zinc (2-16pM) concentrations, cadmium uptake kinetics in T. weissflogii are regulated, the maximum uptake rate increasing with decreasing external metal concentrations. The intracellular cadmium quota is maintained at relatively constant levels over this range. At high inorganic cadmium concentrations (5nM), export of cadmium, most likely complexed to the metal-binding polypeptide phytochelatin, also regulates intracellular cadmium concentrations. The efflux of both cadmium and phytochelatin stops when the external inorganic cadmium concentration is reduced to "natural" levels (<7pM). The intracellular pool of cadmium-phytochelatin complex serves as a source of Cd to proteins after the external Cd supply is cut off. The cadmium-phytochelatin complex is not very stable once outside the cell since the exported cadmium appears to be available to T. weissflogii. The same low level of inorganic cadmium that enhances the growth rate of zinc- limited cells restores the activity of carbonic anhydrase, thought to be the key enzyme limiting growth of T. weissflogii at low zinc. Cadmium coelutes with at least one of the multiple isoforms of carbonic anhydrase produced by T. weissflogii and covaries with activity of this isoform (which in turn depends on PCO2). Cadmium may therefore play an essential role in carbon uptake under conditions of zinc limitation. The substitution of cadmium for zinc in carbonic anhydrase links the geochemical cycle of cadmium to those of zinc and carbon. Thesis supervisor: Dr. Franqois M. M. Morel Title: Professor of Geology, Princeton U. Visiting Professor of Civil and Environmental Engineering, M.I.T. Acknowledgments I would like to gratefully acknowledge the support of Department of Defense N.D.S.E.G. fellowship program, the Woods Hole Oceanographic Institution, the Paul M. Fye book fellowship, the National Science Foundation and the Office of Naval Research. I would also like to thank the members of my committee, Ed Boyle, Jim Moffett, and Ken Bruland for their insight and guidance. I especially would like to thank Frangois Morel, who has been a skillful advisor, a worthy political adversary, and a good friend throughout my graduate years. I am very grateful for the help and companionship of all the past and present members of the Morel lab, especially Neil Price, Beth Ahner, Don Yee, John Reinfelder and Sam Roberts, without which I could never have started my thesis much less completed it. The community of the Parson's lab in general made my tenure in graduate school a pleasure. Finally, I am deeply grateful to my family, Richard, Jacqueline and Debby Lee, who have always tolerated my foibles and nurtured my enthusiasms. I would also like to thank my husband Glenn Moglen, who makes my life joyful and rich and is the best companion in life I could ever wish for. I would like to dedicate my thesis in memory of my father, Richard Dooban Lee. Biographical note Education MIT/WHOI Joint Program in Oceanography, Cambridge, MA. (1989-1995) Ph.D. in Chemical Oceanography. Yale University, New Haven, CT. (1982-1986) B.S. degree in Chemistry. Honors NDSEG Fellowship 1989-1992 Graduated summa cum laude, 1986 Elected to Phi Beta Kappa, 1985 Professionalexperience Research Analyst, Gradient Corp., Cambridge, MA. 1987-1989. Critiqued sampling plans, evaluated analytical work, and performed exposure estimates for hazardous waste sites. Research Analyst, JACA Corp., Fort Washington, PA. 1986-1987. Performed health risk assessments and constructed exposure profiles for OSHA. Collected water and sediment samples for pesticide analysis. Teaching experience Teaching Assistant, M.I.T. 1992. Graded exams, wrote and graded problem sets, held regular office hours and presented lectures in graduate course, "Aquatic Chemistry". Supervision of Undergraduate Research, M.I.T. 1990-1992. Taught undergraduate students culture and trace-metal clean techniques. Supervised project studying metal limitation in marine algae. Publications F. M. M. Morel, J. R. Reinfelder, S. B. Roberts, C. P. Chamberlain, J. G. Lee, and D. Yee. 1994. "Zinc and Carbon Co-limitation of Marine Phytoplankton." Nature 369: 740-742. Lee, J. G., S. B. Roberts, and F. M. M. Morel. In press. "Cadmium: a nutrient for the marine diatom Thalassiosiraweissflogii." Limnol. Oceanogr. Lee, J. G. and F. M. M. Morel. In press. "Replacement of zinc by cadmium in marine phytoplankton." Mar. Ecol. Prog. Ser. Table of Contents TABLE OF CONTENTS 6 LIST OF FIGURES 9 LIST OF TABLES 10 ABBREVIATIONS AND DEFINITIONS 11 CHAPTER 1 INTRODUCTION 13 BACKGROUND 13 OVERVIEW OF THESIS 16 CONCLUSIONS 19 REFERENCES 20 CHAPTER 2 CADMIUM: A NUTRIENT FOR THE MARINE DIATOM THALASSIOSIRA WEISSFLOGII 23 ABSTRACT 23 INTRODUCTION 24 MATERIALS AND METHODS 25 CULTURE MEDIUM 25 GROWTH CONDITIONS 26 CADMIUM QUOTAS 26 CADMIUM FRACTIONATION 27 CADMIUM UPTAKE KINETICS 27 CARBONIC ANHYDRASE (CA) ASSAY 28 RESULTS 30 DISCUSSION 34 REFERENCES 40 CHAPTER 3 REPLACEMENT OF ZINC BY CADMIUM IN MARINE PHYTOPLANKTON 61 ABSTRACT 61 INTRODUCTION 62 METHODS 64 RESULTS 65 DISCUSSION 67 LITERATURE CITED 70 CHAPTER 4 EXPORT OF CADMIUM AND PHYTOCHELATIN BY THE MARINE DIATOM THALASSIOSIRA WEISSFLOGII. 81 ABSTRACT 81 INTRODUCTION 82 METHODS 83 GROWTH CONDITIONS FOR RESUSPENSION AND DTPA EXPERIMENTS 83 TOTAL PARTICULATE "°9CD CONCENTRATIONS 84 TOTAL PARTICULATE PHYTOCHELATIN CONCENTRATIONS 84 CELLULAR CD FRACTIONATION 84 EXIPORT OF PHYTOCHELATIN 85 BIOASSAY FOR SPECIATION OF RELEASED CD 85 RESULTS 87 RESUSPEN2SION AT 4.6 NM CD' 87 RESUSPENSION IN MEDIUM WITHOUT CD AND ADDITION OF DTPA 88 CHANGES IN CELLULAR CD FRACTIONATION 90 EFFLUX OF PHYTOCHELATIN 90 BIOASSAY FOR SPECIATION OF RELEASED CD 91 DISCUSSION 93 CD EXPORT RATE 93 CHANGES IN CD FRACTIONATION BETWEEN THE MEMBRANE AND CYTOPLASM 95 EXPORT OF CD AS A PHYTOCHELATIN COMPLEX 96 EFFECT OF CD-PHYTOCHELATIN EXPORT ON NATURAL WATERS CHAPTER 5 CADMIUM IN CARBONIC ANHYDRASE: CHANGES WITH PCOz.115 INTRODUCTION 115 METHODS 116 GROWTH CONDITIONS 116 SHORT-TERM EFFECTS OF LOWERING PCO 2 116 CADMIUM QUOTAS 117 CADMIUM FRACTIONATION 117 CELLULAR PHYTOCHELATIN CONCENTRATION 118 CARBONIC ANHYDRASE ASSAY 118 RESULTS AND DISCUSSION 120 REFERENCES 124 CHAPTER 6 DTPA WASH METHOD FOR MEASURING INTRACELLULAR CD133 RATIONALE USED TO DEVELOP METHOD 133 DETAILS OF METHOD 134 REFERENCES 135 List of Figures FIGURE 2-1. EFFECT OF VARYING ZN' ON GROWTH RATE IN THE PRESENCE AND ABSENCE, OF CD. 44 FIGURE 2-2. EFFICT OF VARYING CD' ON GROWTH RATE, CD QUOTAS, AND CELLULAR CD FRACTIONATION AT HIGH AND LOW ZN'. 46 FIGURE 2-3. SHORT TERM CD UPTAKE RATES AT VARYING ZN'. 50 FIGURE 2-4. KINETICS OF CD UPTAKE IN CELLS ACCLIMATED AT VARYING CD' AND ZN'. 52 FIGURE 2-5. EFFCT OF CD/ZN REPLACEMENT ON CARBONIC ANHYDRASE ACTIVITY.54 FIGURE 2-6. COMPARISON OF CD AND CARBONIC ANHYDRASE ELUTION PROFILES. 55 FIGURE 2-7. CD' AND ZN' IN THE CENTRAL NORTH PACIFIC. 56 FIGURE 3-1. EFFICT OF CD ON GROWTH OF MARINE PHYTOPLANKTON AT LOW INORGANIC ZN. 74 FIGURE 3-2. GROWTH CURVES OF CULTURES WHERE CD HAD A BENEFICIAL EFFECT. 76 FIGURE 4-1. RESUSPENSION IN EDTA-BUFFERED MEDIUM WITH 4.6 NM CD'. 100 FIGURE 4-2. RESUSPENSION IN EDTA-BUFFERED MEDIUM CONTAINING NO ADDED CD.102 FIGURE 4-3. ADDITION OF DTPA TO REDUCE CD'. 104 FIGURE 4-4. CADMIUM FRACTIONATION BETWEEN MEMBRANES AND CYTOPLASM FOLLOWING ADDITION OF DTPA TO REDUCE CD' LEVELS IN THE MEDIUM. 106 FIGURE 4-5. EFFLUX OF PHYTOCHELATIN FROM CELLS FOLLOWING REFSUSPENSION IN EDTA-BUFFTERED MEDIUM WITH AND WITHOUT CD. 108 FIGURE 5-1. GROWTH, CELLULAR CD, CELLULAR PHYTOCIIHELATIN, AND CD FRACTIONATION AT VARYING PCO2. 126 FIGURE 5-2. CA ACTIVITY AT VARYING PCO 2. 128 FIGURE 5-3. CD CONTENT OF CA AT VARYING PCO2. 129 FIGURE 5-4. SHORT TERM CO2 EFFECTS ON GROWTH, CELLULAR CD, AND TOTAL PARTICULATE CD. 130 FIGURE 6-1. THE EFFECT OF INCREASING DTPA WASH TIMES ON MEASURED CELLULAR CD CONCENTRATION. 136 List of Tables TABLE 2-1. GROWTH CONDITIONS OF EXPERIMENTS. 58 TABLE 2-2. GROWTH RATES AT HIGH AND LOW EDTA. 59 TABLE 3-1. LIST OF SPECIES OF MARINE PHYTOPLANKTON IN THIS STUDY. 79 TABLE 4-1. GROWTH RATES OF CULTURES BEFORE AND AFTER CHANGE IN CD' 110 TABLE 4-2. RESULTS OF BIOASSAY FOR SPECIATION OF RELEASED CD 111 TABLE 4-3.
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