Cyanobacterial Toxins of Drinking Water Supplies: Cylindrospermopsins and Microcystins - Chapter 1 pdf

TF1713_half 10/22/04 6:26 PM Page 1 Cyanobacterial Toxins of Drinking Water Supplies Copyright 2005 by CRC Press TF1713_title 11/2/04 10:01 AM Page 1 Cyanobacterial Toxins of Drinking Water Supplies IAN ROBERT FALCONER CRC PRESS Boca Raton London New York Washington, D.C. Cylindrospermopsins and Microcystins Copyright 2005 by CRC Press This book contains information obtained from authentic and highly regarded sources. Reprinted material is quoted with permission, and sources are indicated. A wide variety of references are listed. Reasonable efforts have been made to publish reliable data and information, but the author and the publisher cannot assume responsibility for the validity of all materials or for the consequences of their use. Neither this book nor any part may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, microfilming, and recording, or by any information storage or retrieval system, without prior permission in writing from the publisher. The consent of CRC Press does not extend to copying for general distribution, for promotion, for creating new works, or for resale. Specific permission must be obtained in writing from CRC Press for such copying. Direct all inquiries to CRC Press, 2000 N.W. Corporate Blvd., Boca Raton, Florida 33431. Trademark Notice: Product or corporate names may be trademarks or registered trademarks, and are used only for identification and explanation, without intent to infringe. Visit the CRC Press Web site at www.crcpress.com © 2005 by CRC Press No claim to original U.S. Government works International Standard Book Number 0-415-31879-3 Library of Congress Card Number 2004054551 Printed in the United States of America 1 2 3 4 5 6 7 8 9 0 Printed on acid-free paper Library of Congress Cataloging-in-Publication Data Falconer, Ian R. Cyanobacterial toxins of drinking water supplies : cylindrospermopsins and microcystins Ian R. Falconer. p. cm. Includes bibliographical references and index. ISBN 0-415-31879-3 (alk. paper) 1. Cyanobacterial toxins. 2. Microcystins. 3. Cyanobacteria. 4. Freshwater microbiology. 5. Bacterial pollution of water. I. Title . QP632.C87F34 2004 615.9'52939—dc22 2004054551 TF1713_C000.fm Page 4 Friday, October 29, 2004 2:21 PM Copyright 2005 by CRC Press Preface The importance of cyanobacterial toxins in drinking water sources has been high- lighted by the adoption of a provisional drinking water “Guideline Value” for micro- cystin-LR, one of the most abundant toxins, by the World Health Organization (WHO). A number of nations have now legislated a guideline for microcystins into their drinking water regulations, with the consequent need for monitoring and ana- lytical techniques. The Chemical Safety Committee of the WHO also has under consideration a Guideline Value for cylindrospermopsin, the other most damaging cyanobacterial toxin. The need for careful study of the cyanobacterial toxins, their sources, and their removal from water supplies was emphasized by the substantial death toll among dialysis patients in Brazil who were accidentally treated with water containing these toxins. Consumers of treated drinking water have also suffered injury due to micro- cystins and cylindrospermopsin in the water supply, as have people exposed through recreational activities. Two aspects of cyanobacterial toxicity that require substantial attention are the possible long-term effects on the population of exposure to low doses of the toxins and intermittent exposure to higher doses. In addition, there is increasing experi- mental evidence of tumor promotion and carcinogenesis in rodents due to the toxins. This book assesses the present knowledge of toxic species of cyanobacteria and their ecology, the chemistry and toxicology of the most relevant toxins, safe con- centrations in drinking and recreational water, monitoring of organisms and toxins, mitigation of reservoir problems, and water treatment technologies. Each of these areas is the subject of considerable recent research, with North America, Europe, Japan, and Australia contributing substantially. This volume is intended to be useful to environmental and public health agencies, water supply utilities, and managers of drinking and recreational water, as well as to researchers in this field. TF1713_C000.fm Page 5 Friday, October 29, 2004 2:21 PM Copyright 2005 by CRC Press Acknowledgments I would like to express my gratitude to my wife, Mary, who has supported my teaching, research, and writing throughout my career and without whose help little would have been achieved. My scientific colleagues Maria Runnegar and Andrew Humpage have, over 30 years, contributed greatly to this research, from its infancy to what is now a rapidly expanding worldwide investigation. Our research collabo- rators and postgraduate students deserve recognition for their systematic contribu- tions to the field, which are evident from the coauthorship of the many papers quoted in this volume. I would like to thank the following publishers, organizations, and individuals for permission to reproduce or modify copyrighted material used in this text: the American Chemical Society for Figures 3.2, 3.3, and 10.2; Australian government for Figure 8.4; Australasian Medical Publishing Company for Figure 5.1; Peter Baker, CRC for Water Quality and Treatment, Salisbury, South Australia, for Figure 4.6; Cyanosite Image Gallery — Dr. Roger Burke, University of California, River- side, and Dr. Mark Schneegurt, Wichita State University — for Figure 2.3; Dr. Bernard Ernst, University of Konstanz, for Figure 2.4d; Dr. Larelle Fabbro for Figure 4.4; Gladstone Area Water Board for Figures 4.2 and 4.5; Journal of the Association of Official Analytical Chemists for Figure 10.1; Royal Society of Chemisty for Figure 8.2; Taylor & Francis Journals for Figure 7.3; Wiley for Figures 2.4, 6.1, and 7.1; and the World Health Organization for Figures 4.1 and 4.3. TF1713_C000.fm Page 7 Friday, October 29, 2004 2:21 PM Copyright 2005 by CRC Press Table of Contents Chapter 1 Introduction 1 References 6 Chapter 2 Toxic Cyanobacteria and Their Identification 9 2.1 The Origins of Cyanobacteria 9 2.2 Cyanobacterial Organisms 10 2.3 Classification and Nomenclature 11 2.4 Molecular Taxonomy 13 References 19 Chapter 3 Toxin Chemistry and Biosynthesis 25 3.1 Chemistry of Cylindrospermopsins 26 3.2 Synthesis of Cylindrospermopsin 28 3.3 Biosynthesis of Cylindrospermopsin 29 3.4 Chemistry of Microcystins 31 3.5 Synthesis of Microcystins 34 3.6 Biosynthesis of Microcystins: Biochemical Approaches 35 3.7 Molecular Genetic Approaches 36 References 39 Chapter 4 Cyanobacterial Ecology 45 4.1 Cyanobacteria in Freshwater 45 4.2 Light 47 4.3 Buoyancy 49 4.4 Nutrients 50 4.4.1 Phosphorus 50 4.4.2 Nitrogen 50 4.5 Distribution of Cylindrospermopsis raciborskii (Nostocales) 51 4.5.1 In Australia 52 4.6 Ecology of Cylindrospermopsis raciborskii 55 4.7 Cylindrospermopsin Production by Cylindrospermopsis raciborskii 57 4.8 Cylindrospermopsin Production by Other Cyanobacterial Species 59 4.9 Production of Other Toxins by Cylindrospermopsis raciborskii 60 4.10 Distribution of Microcystis aeruginosa 60 4.11 Distribution of Other Microcystin-Producing Species of Cyanobacteria 62 4.12 Ecology of Microcystis aeruginosa 62 TF1713_C000.fm Page 9 Friday, October 29, 2004 2:21 PM Copyright 2005 by CRC Press 4.13 Ecology of Planktothrix Species and Anabaena flos-aquae 64 4.14 Ecology of Microcystin Production 66 4.15 Nodularia spumigena and Nodularin Production 68 References 68 Chapter 5 Cyanobacterial Poisoning of Livestock and People 77 5.1 Livestock and Wildlife Poisoning by Cyanobacterial Toxins 78 5.2 Human Poisoning by Cyanobacterial Toxins 80 5.3 Waterborne Poisoning in Brazil 80 5.4 Gastrointestinal Illness Associated with Cyanobacteria in the U.S 82 5.5 Gastroenteritis Associated with Cyanobacteria in Africa 83 5.6 Liver Damage Associated with Microcystis aeruginosa in Australia 84 5.7 Recreational Poisoning in the U.K. and U.S 86 5.8 The Dialysis Tragedy in Brazil 87 5.9 Palm Island Poisoning by Cylindrospermopsin in Australia 88 5.10 Conclusions 90 References 90 Chapter 6 Cylindrospermopsin Toxicity 95 6.1 Toxicity of Cylindrospermopsin: Whole-Animal Studies 95 6.2 Oral Toxicity of Cylindrospermopsin: Studies of the No Observed Adverse Effect Level 97 6.3 Cylindrospermopsin Uptake and Excretion 98 6.4 Mechanism of Cylindrospermopsin Toxicity 99 6.5 Inhibition of Protein Synthesis 100 6.6 Cytochrome P450 in Cylindrospermopsin Toxicity 102 6.7 DNA Damage, Chromosome Damage, and Carcinogenicity 104 6.8 Micronucleus Formation in the Presence of Cylindrospermopsin 104 6.9 Whole-Animal Carcinogenicity 105 6.10 Assessment of Carcinogenicity 106 6.11 Teratogenicity, Immunotoxicity, and Reproductive Injury 106 References 106 Chapter 7 Microcystin Toxicity 109 7.1 Acute Toxicity of Microcystin to Rodents 109 7.2 Subchronic and Chronic Toxicity 110 7.3 Determination of the No Observed Adverse Effect Level for Microcystin in Mice 111 7.4 Large-Animal Toxicity 111 7.5 Determination of the No Observed Adverse Effect Level of Microcystin in Pigs 112 7.6 Toxicokinetics of Microcystin 113 7.7 Conjugation and Excretion of Microcystin 118 TF1713_C000.fm Page 10 Friday, October 29, 2004 2:21 PM Copyright 2005 by CRC Press 7.8 Studies with Isolated Hepatocytes 119 7.9 Mechanisms of Microcystin Toxicity 121 7.10 Microcystin and Phosphatase Inhibition 121 7.11 Cytoskeletal Effects 123 7.12 Nuclear Actions of Microcystin 124 7.13 Microcystin and Apoptosis 124 7.14 Cell-Cycle Effects of Microcystin 126 7.15 Tumor Promotion by Microcystin 128 7.16 Carcinogenesis, Liver Damage, and Cancer in China 131 7.17 Microcystin, Teratogenesis, and Reproductive Toxicity 132 7.18 Conclusion 133 References 134 Chapter 8 Risk and Safety of Drinking Water: Are Cyanobacterial Toxins in Drinking Water a Health Risk? 141 8.1 Risk Assessment and Legislation 142 8.2 What Is a Risk, and How Can It Be Assessed? 145 8.3 Risk Management 146 8.4 Risk and Chemical Safety in Drinking Water — Cyanobacterial Toxins as Toxic Chemicals 146 8.5 The Tolerable Daily Intake 149 8.6 Determination of a Guideline Value for Cylindrospermopsin 150 8.7 The Tolerable Daily Intake and Drinking Water Guideline Value for Microcystin 152 8.8 Cylindrospermopsins and Microcystins as Carcinogens? 153 8.9 Cylindrospermopsin — Is It a Carcinogen? 158 8.10 Microcystins and Nodularins — Are They Carcinogens? 160 8.11 Chronic Lifetime Dose, Intermittent Acute Doses, and Recreational Exposures 161 References 163 Chapter 9 Monitoring of Reservoirs for Toxic Cyanobacteria and Analysis of Nutrients in Water 167 9.1 Monitoring Sites 168 9.2 Monitoring Frequency 169 9.3 Parameters for Monitoring — Predictive Parameters 170 9.4 Parameters for Monitoring — Identity and Number of Cyanobacterial Cells 173 9.5 Sampling 174 9.6 Cell Counting, Measurement, and Chlorophyll- a Analysis 175 9.7 Chlorophyll- a Analysis 178 9.8 Fluorescence Measurement of Cyanobacterial Concentration in Reservoirs 179 TF1713_C000.fm Page 11 Friday, October 29, 2004 2:21 PM Copyright 2005 by CRC Press 9.9 Monitoring by Genetic Methods 180 References 180 Chapter 10 Detection and Analysis of Cylindrospermopsins and Microcystins 185 10.1 Toxin Concentration 186 10.2 In Vivo Rodent Toxicity Assays 186 10.2.1 Methods for Mouse Tests — Intact Cells 187 10.2.2 Senescent or Lysed Samples 188 10.2.3 Ethics Permission 189 10.3 Cylindrospermopsin Bioassay and Analysis 189 10.3.1 Bioassays for Cylindrospermopsin 190 10.4 Cell-Based and Cell-Free Toxicity Measurement of Cylindrospermopsin 191 10.5 ELISA of Cylindrospermopsin 192 10.6 Instrument-Based Techniques for Cylindrospermopsin 193 10.6.1 High-Performance Liquid Chromatography (HPLC) 193 10.7 Microcystins and Nodularins: Bioassay and Analysis 194 10.8 Sample Collection and Handling for Microcystins 195 10.9 Bioassays for Microcystins and Nodularins 196 10.9.1 Cell-Based Assays for Microcystins 197 10.9.2 Bacterial Luminescence Assays 197 10.10 ELISA for Microcystins and Nodularins 197 10.10.1 Polyclonal Antibodies 197 10.10.2 Monoclonal Antibodies 199 10.10.3 Phage Library Antibodies 199 10.10.4 Immunofluorimetric Assays 199 10.11 Protein Phosphatase Inhibition Assay for Microcystins and Nodularins 200 10.11.1 Methodology 200 10.12 HPLC for Microcystins and Nodularins 201 10.12.1 Advanced Instrument Techniques 202 10.13 Microcystins and Nodularins in Tissue Samples 203 10.14 Analytical Problems and Challenges 204 References 206 Chapter 11 Prevention, Mitigation, and Remediation of Cyanobacterial Blooms in Reservoirs 213 11.1 Nutrient Reduction 215 11.2 Phosphorus Reduction 216 11.2.1 Reduction to Inflow 216 11.2.2 Phosphorus Stripping 217 11.2.3 Wetlands 217 11.2.4 Low-Flow Effects 218 11.2.5 Agricultural Land 219 11.3 Catchment Management 220 TF1713_C000.fm Page 12 Friday, October 29, 2004 2:21 PM Copyright 2005 by CRC Press 11.4 Nitrogen Reduction 221 11.5 Reservoir Remediation 222 11.6 Destratification 223 11.7 Flow 225 11.8 Phosphorus Precipitation, Sediment Capping, and Dredging 226 11.9 Algicides 227 11.9.1 Copper 227 11.9.2 Problems with the Use of Copper 227 11.9.3 Oxidants and Herbicides 229 11.10 Biological Remediation 229 11.10.1 Fish Population 230 11.10.2 Straw 231 11.10.3 Phage 231 References 231 Chapter 12 Water Treatment 237 12.1 Processes for Removing Cyanobacterial Toxins from Drinking Water Supplies 240 12.1.1 Control of Abstraction 240 12.1.2 Bank Filtration 241 12.2 Water Filtration, Coagulation, and Clarification 242 12.3 Activated Carbon 245 12.3.1 Biological Activated Carbon 246 12.3.2 Powdered Activated Carbon 247 12.4 Ozonation and Chlorination 248 12.4.1 Chlorine 250 12.5 Titanium Dioxide Photocatalysis 250 12.6 Slow Sand Filtration 251 12.7 Membrane Filtration 252 12.8 Conclusions 253 References 254 Chapter 13 Emerging Issues 259 13.1 Ecological Issues 259 13.2 Health Issues 261 13.3 Water Treatment 262 References 263 TF1713_C000.fm Page 13 Friday, October 29, 2004 2:21 PM Copyright 2005 by CRC Press [...]... effects of cyanobacterial toxins REFERENCES Carmichael, W W., D F Biggs, et al (19 79) Pharmacology of anatoxin-a produced by the freshwater cyanophyte Anabaena flos-aquae NRC-4 4 -1 Toxicon 17 : 229–236 Carmichael, W W and I R Falconer (19 93) Diseases related to freshwater blue-green algal toxins, and control measures Algal Toxins in Seafood and Drinking Water I R Falconer, ed London, Academic Press: 18 7–209... alkaloids and peptides (Chapter 3) The 1 Copyright 2005 by CRC Press TF1 713 _C0 01. fm Page 2 Thursday, November 4, 2004 10 :14 AM 2 Cyanobacterial Toxins of Drinking Water Supplies FIGURE 1. 1 Alkaloid neurotoxins from cyanobacteria toxins are formed as secondary metabolites, not as parts of metabolic pathways leading to other compounds The toxins remain with the cells to a variable extent, with the alkaloid toxins. .. with the presence of toxins The magnitude of the problem of toxic cyanobacteria in drinking water sources relates to two major world issues (Chapter 13 ) These are population growth and global warming Population growth results in increased demand for drinking water, coupled with an increased likelihood of eutrophication of previously clean water Copyright 2005 by CRC Press TF1 713 _C0 01. fm Page 6 Thursday,... Toxicology 16 (2): 19 2 19 5 Francis, G (18 78) Poisonous Australian lake Nature (London) 2 May: 11 12 Humpage, A R., J Rositano, et al (19 93) Paralytic shellfish poisons from freshwater bluegreen algae Medical Journal of Australia 15 9: 423 Humpage, A R., J Rositano, et al (19 94) Paralytic shellfish poisons from Australian cyanobacterial blooms Australian Journal of Marine and Freshwater Research 45: 7 61 7 71 Mahmood,... A and W W Carmichael (19 87) Anatoxin-a(s), an anticholinesterase from the cyanobacterium Anabaena flos-aquae NRC-52 5 -1 7 Toxicon 25: 12 21 12 27 Copyright 2005 by CRC Press TF1 713 _C0 01. fm Page 7 Thursday, November 4, 2004 10 :14 AM Introduction 7 Padisak, J (19 97) Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and. .. Australia (Francis 18 78) The cyanobacteria still occur in the lake, which is used as Copyright 2005 by CRC Press TF1 713 _C0 01. fm Page 4 Thursday, November 4, 2004 10 :14 AM 4 Cyanobacterial Toxins of Drinking Water Supplies Microcystin Nodularin FIGURE 1. 3 Cyclic peptide hepatotoxins from cyanobacteria a human drinking water source for several small towns and is carefully monitored for cell numbers of the organism... the water bloom of Anabaena circinalis, which covered about 10 00 km of the Darling River in Australia in the summer of 19 90 This caused the deaths of more than a thousand livestock and also contaminated the drinking water supply of several towns (Humpage, Rositano et al 19 93, 19 94) Another tricyclic guanidinium alkaloid, of quite different structure and toxicity, is cylindrospermopsin (Figure 1. 2)... November 4, 2004 10 :14 AM 6 Cyanobacterial Toxins of Drinking Water Supplies supplies As the population of cities grows, the intensity of land use in the water catchments supplying the cities rises, with nutrients from agriculture and human waste increasing in the reservoirs One of the early consequences of this population increase is seasonal blooms of toxic cyanobacteria in drinking water reservoirs...TF1 713 _C0 01. fm Page 1 Thursday, November 4, 2004 10 :14 AM 1 Introduction In many parts of the world, surface waters are used for the drinking water supply The quality of these surface waters is very variable both within and between countries In developed countries, this water is treated through purification processes; in less developed areas, many people have to rely on untreated water Toxic... cyanobacteria are a normal part of the phytoplankton of surface waters and therefore can present a hazard to consumers if they are present in sufficient numbers The toxins from cyanobacteria are resistant to boiling and can also pass through conventional water treatment plants The understanding of cyanobacteria and their toxins and measures for the control of both has expanded greatly in recent years . Reduction 216 11 .2 .1 Reduction to Inflow 216 11 .2.2 Phosphorus Stripping 217 11 .2.3 Wetlands 217 11 .2.4 Low-Flow Effects 218 11 .2.5 Agricultural Land 219 11 .3 Catchment Management 220 TF1 713 _C000.fm. 230 11 .10 .2 Straw 2 31 11. 10.3 Phage 2 31 References 2 31 Chapter 12 Water Treatment 237 12 .1 Processes for Removing Cyanobacterial Toxins from Drinking Water Supplies 240 12 .1. 1 Control of. TF1 713 _half 10 /22/04 6:26 PM Page 1 Cyanobacterial Toxins of Drinking Water Supplies Copyright 2005 by CRC Press TF1 713 _title 11 /2/04 10 : 01 AM Page 1 Cyanobacterial Toxins of Drinking Water