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Dr Jussi Meriluoto, Department of Biosciences / Biochemistry, Åbo Akademi University, Turku, Finland Jussi Meriluoto, PhD, MTheol, is a biochemist of Finnish origin. He has been working in the field of toxic cyanobacteria since the 1980s. The main line of his research deals with instrumental analyses of cyanotoxins and biomarkers in various matrices. He has applied this expertise in the context of environmental and bioaccumulation studies, ecotoxicology, toxinology, drinking water treatment and toxin degradation. He also has an interest in terrestrial cyanobacteria and probiotic bacteria. He is leading Working Group 1 Occurrence of cyanobacteria and cyanotoxins in CYANOCOST, the COST Action responsible for the development of the Handbook. An important incentive in his work is the principle of inclusiveness and the desire to exchange technical and managemental know-how with new actors entering the cyanotoxin field.
Dr Lisa Spoof, Department of Biosciences / Biochemistry, Åbo Akademi University, Turku, Finland Lisa Spoof, PhD, is a Finnish biochemist. She is a specialist on chromatographic and mass spectrometric analyses of cyanotoxins. She has carried out research on analysis, isolation and characterization of bioactive peptides (microcystins, nodularins, anabaenopeptins) in freshwater and brackish-water cyanobacteria since the 1990s. Her personal experience in laboratory work also includes research on cylindrospermopsin and cyanobacterial neurotoxins, and this strong hands-on experience has been useful for the editorial work concerning the practical chapters in this Handbook.
Professor Geoffrey A. Codd, School of Biological and Environmental Sciences, University of Stirling, UK, and, School of Life Sciences, University of Dundee, UK Geoffrey Codd, PhD, FRSE, is a microbiologist and has carried out research on the biochemistry and ecotoxicology of cyanobacteria and cyanotoxins. His research has included the molecular and organismal modes of action of microcystins, development of physico-chemical and antibody-based methods for cyanotoxin analysis and the investigation of waterborne, cyanotoxin-associated human and animal health incidents. Professor Codd is a past President of the British Phycological Society and the Federation of European Phycological Societies and has served on working parties and committees for the assessment and risk management of cyanobacteria and cyanotoxins at national (UK, Australia, USA) and international level (EU, WHO, UNESCO).
List of Contributors xvii
Preface xxvi
Acknowledgements xxviii
Section I Introduction 1
1 Introduction: Cyanobacteria, Cyanotoxins, Their Human Impact, and Risk Management 3Geoffrey A. Codd, Jussi Meriluoto, and James S. Metcalf
1.1 Introduction 3
1.2 Cyanotoxins 4
1.3 Exposure Routes, Exposure Media, and At-Risk Human Activities 6
1.4 Cyanobacterial Blooms and Cyanotoxins in Relation to Human Pressures on Water Resources and Climate Change 7
1.5 Aims of the Handbook 7
References 8
Section II Cyanobacteria 9
2 Ecology of Cyanobacteria 11Jean-François Humbert and Jutta Fastner
2.1 Introduction 11
2.2 Environmental Conditions Leading to Cyanobacterial Blooms 12
2.3 Population Dynamics of Cyanobacteria 13
2.4 Spatial Distribution of Cyanobacteria in Freshwater Ecosystems 15
2.5 Ecology of the Production of Toxins by Cyanobacteria 16
2.6 General Conclusions 17
References 17
3 Picocyanobacteria: The Smallest Cell-Size Cyanobacteria 19Iwona Jasser and Cristiana Callieri
3.1 Introduction 19
3.2 Records of Toxic Picocyanobacteria 21
3.3 Summary 25
References 26
4 Expansion of Alien and Invasive Cyanobacteria 28Mikolaj Kokocinski, Reyhan Akçaalan, Nico Salmaso, Maya Petrova Stoyneva-Gärtner, and Assaf Sukenik
4.1 Introduction 28
4.2 Definition of Invasive/Alien Species: Nomenclature Problems 29
4.2.1 Invasive Species Concept in Cyanobacteria 29
4.3 Occurrence of Invasive and Alien Cyanobacteria 31
4.4 Factors Enhancing the Expansion of Alien Cyanobacteria 33
4.5 Impact of Cyanobacterial Invasion on Ecosystem 34
References 36
Section III Sampling, Monitoring and Risk Management 41
5 Health and Safety During Sampling and in the Laboratory 43Roberta Congestri, James S. Metcalf , Luca Lucentini, and Federica Nigro Di Gregorio
5.1 Introduction 43
5.2 Sampling Safety 43
5.3 Laboratory Safety 44
5.4 Cyanotoxin Production and Application 45
5.5 Contamination due to Equipment, Glassware, and Accidents 45
References 45
6 Basic Guide to Detection and Monitoring of Potentially Toxic Cyanobacteria 46Nico Salmaso, Cécile Bernard , Jean-François Humbert, Reyhan Akçaalan, Meriç Albay, Andreas Ballot , Arnaud Catherine, Jutta Fastner , Kerstin Häggqvist, Mária Horecká, Katarzyna Izydorczyk, Latife Köker , Jirí Komárek, Selma Maloufi, Joanna Mankiewicz-Boczek, James S. Metcalf , Antonio Quesada, Catherine Quiblier , and Claude Yéprémian
6.1 Introduction 47
6.2 Monitoring of Cyanobacteria: Sampling Strategies 48
6.3 Cyanobacterial Identification and Quantification 55
Appendix 6.1 Testing Phytoplankton Distributions: ¿2 Test (Pearson Goodness-of-Fit Test) 63
References 66
7 Case Studies of Environmental Sampling, Detection, and Monitoring of Potentially Toxic Cyanobacteria 70Kerstin Häggqvist, Reyhan Akçaalan, Isidora Echenique-Subiabre, Jutta Fastner , Mária Horecká, Jean-François Humbert, Katarzyna Izydorczyk, Tomasz Jurczak, Mikolaj Kokocinski, Tore Lindholm, Joanna Mankiewicz-Boczek, Antonio Quesada, Catherine Quiblier, and Nico Salmaso
7.1 Introduction 71
7.2 Shallow Lakes 71
7.3 Deep Lakes 74
7.4 Reservoirs 75
7.5 Rivers 77
7.6 The Baltic Sea 78
7.7 Waterbodies Used for Drinking Water Production 79
References 81
8 New Tools for the Monitoring of Cyanobacteria in Freshwater Ecosystems 84Jean-François Humbert and Andrea Törökné
8.1 Introduction 84
8.2 Use of Photosynthetic Pigments for the In Situ Quantification of Cyanobacteria and Other Phytoplankton in Water 85
8.3 Integration of Physicochemical and Fluorescence Sensors in Buoys 86
8.4 New Methods for Automatic Cell Counting in Water Samples 86
References 87
9 Remote Sensing of Cyanobacterial Blooms in Inland, Coastal, and Ocean Waters 89Peter D. Hunter , Mark W. Matthews , Tiit Kutser , and Andrew N. Tyler
9.1 Introduction 89
9.2 Bio-optical Properties of Marine and Inland Waters 90
9.3 Platforms and Sensors 91
9.4 Overview of Approaches 92
9.5 Case Study Examples 95
9.6 Future Prospects 96
References 98
10 The Italian System for Cyanobacterial Risk Management in Drinking Water Chains 100Luca Lucentini, Liliana La Sala , Rossella Colagrossi , and Roberta Congestri
10.1 Introduction 100
10.2 Risk Assessment of Toxic Cyanobacterial Outbreaks in Water for Human Consumption in Italy 101
10.3 Framework of Risk Management of Toxic Cyanobacterial Outbreaks in Water for Human Consumption 102
10.4 Risk Information and Communication 106
References 106
Section IV Toxins and Bioactive/Noxious Compounds from Cyanobacteria 107
11 Microcystins and Nodularins 109Arnaud Catherine, Cécile Bernard, Lisa Spoof , and Milena Bruno
11.1 Chemical Characteristics and Diversity of Microcystins and Nodularins 109
11.2 Biosynthesis and Genetics of MC and NOD Production 110
11.3 Occurrence of MCs and NODs 112
11.4 Toxicological Effects and Associated Health Risk 113
11.5 Available Methods for the Analysis of MCs and NODs 117
References 118
12 Cylindrospermopsin and Congeners 127Mikolaj Kokocinski, Ana Maria Cameán, Shmuel Carmeli, Remedios Guzmán-Guillén, Ángeles Jos, Joanna Mankiewicz-Boczek , James S. Metcalf , Isabel Maria Moreno, Ana Isabel Prieto, and Assaf Sukenik
12.1 Chemical Characteristics of Cylindrospermopsin and Congeners 127
12.2 Genes Involved in CYN Biosynthesis 128
12.3 CYN Producers and Distribution 128
12.4 Toxicity of CYN 129
12.5 The Biological Role of CYN 132
12.6 Degradation of CYN 132
12.7 Available Methods for Determining CYN in Waters 132
References 133
13 Anatoxin-a, Homoanatoxin-a, and Natural Analogues 138Milena Bruno, Olivier Ploux, James S. Metcalf , Annick Mejean, Barbara Pawlik-Skowronska, and Ambrose Furey
13.1 Introduction 138
13.2 Chemical Structure, Synthesis, and Reactivity 138
13.3 Biosynthesis of ANTX, HANTX, and dihydroANTX 140
13.4 Occurrence and Producing Strains 140
13.5 Toxicity and Pharmacology 141
13.6 Analytical Methodologies 142
References 144
14 Saxitoxin and Analogues 148Andreas Ballot, Cécile Bernard, and Jutta Fastner
14.1 Introduction 148
14.2 Toxicity of STXs 149
14.3 Occurrence 149
14.4 Genetics and Biosynthesis 150
14.5 Detection Methods 151
14.6 Guidance Values or National Regulations or Recommendations for Managing STXs 152
References 152
15 Anatoxin-a(S) 155James S. Metcalf and Milena Bruno
15.1 Chemical Structure of Anatoxin-a(S) 155
15.2 Biosynthesis 155
15.3 Occurrence and Producing Strains 156
15.4 Toxicology and Pharmacology 156
15.5 Analytical Methods for Determination and Quantification 157
References 158
16 ß-N-Methylamino-l-Alanine and (S)-2,4-Diaminobutyric Acid 160Olivier Ploux, Audrey Combes, Johan Eriksson, and James S. Metcalf
16.1 Historical Overview 160
16.2 Structure, Synthesis, and Molecular Properties 161
16.3 Neurotoxicity 161
16.4 Methods for Identification and Quantification 162
16.5 Occurrence in Cyanobacteria, Plants, and Animals 162
References 163
17 Lipopolysaccharide Endotoxins 165Sílvia Monteiro, Ricardo Santos, Ludek Bláha, and Geoffrey A. Codd
17.1 Lipopolysaccharide Endotoxins: Structure 165
17.2 Occurrence of LPS Endotoxins 167
17.3 Toxic Effects of LPS Endotoxins 168
17.4 Methods for Determination of LPS Endotoxins 169
References 170
18 Cyanobacterial Retinoids 173Kunimitsu Kaya and Tomoharu Sano
18.1 Introduction 173
18.2 Detection of Retinoids Produced by Cyanobacteria 174
18.3 Chemistry and Analysis of Retinoids 175
18.4 Malformations by Cyanobacterial Retinoids 176
18.5 Concluding Remarks 176
References 176
19 Other Cyanobacterial Bioactive Substances 179Tina Elersek, Ludek Bláha, Hanna Mazur-Marzec, Wido Schmidt, and Shmuel Carmeli
19.1 Introduction 179
19.2 Aeruginosins and Spumigins 182
19.3 Anabaenopeptins 184
19.4 Biogenic Amines 185
19.5 Depsipeptides 186
19.6 Endocrine Disruptors and Novel Tumour Promoters 187
19.7 Lyngbyatoxins and Other Toxins Produced by Lyngbya majuscula 188
19.8 Microginins 189
19.9 Microviridins 189
References 190
20 Taste and Odour Compounds Produced by Cyanobacteria 196Triantafyllos Kaloudis, Theodoros M. Triantis, and Anastasia Hiskia
20.1 Cyanobacterial Taste and Odour Compounds in Water Resources 196
20.2 Analytical Methods for Taste and Odour Compounds 197
References 199
Section V Screening and Trace Analysis of Cyanotoxins 203
21 Determination of Cyanotoxins by High-Performance Liquid Chromatography with Photodiode Array 205Anastasia Hiskia, Lisa Spoof , Triantafyllos Kaloudis, and Jussi Meriluoto
21.1 Introduction: Application of High-Performance Liquid Chromatography for Different Classes of Cyanotoxins 205
21.2 HPLC of Microcystins and Nodularins 206
21.3 HPLC of Anatoxins 208
21.4 HPLC of Cylindrospermopsin 208
21.5 Advantages and Disadvantages of HPLC-PDA 208
References 209
22 Determination of Cyanotoxins by High-Performance Liquid Chromatography with Fluorescence Derivatization 212James S. Metcalf and Paulo Baptista Pereira
22.1 Principle of the Technique and Why It Is Used for Cyanotoxins 212
22.2 Types of Reactions for Analysing Paralytic Shellfish Toxins Using High-Performance Liquid Chromatography with Fluorescence Derivatization 213
22.3 Types of Reactions for Analysing ß-N-Methylamino-l-Alanine and Isomers by HPLC-FLD 216
22.4 Need for Confirmatory Techniques with HPLC-FLD 216
References 216
23 Liquid Chromatography-Mass Spectrometry 218Josep Caixach, Cintia Flores, Lisa Spoof , Jussi Meriluoto, Wido Schmidt, Hanna Mazur-Marzec, Anastasia Hiskia, Triantafyllos Kaloudis, and Ambrose Furey
23.1 Introduction 218
23.2 Ion Sources 220
23.3 Types of Mass Analysers 225
23.4 Application of LC-MS in Cyanotoxin Analyses 233
23.5 Overview of Quantitation: Cyanobacterial Toxins 235
23.6 Ion Suppression/Enhancement Considerations 237
23.7 High-Resolution Mass Spectrometry (HRMS) 239
23.8 MS Experiments for the Detection of Unknown Cyanotoxins 242
23.9 Performance Criteria of LC-MS Methods for Identification and Quantification of Cyanotoxins 249
References 251
24 Capillary Electrophoresis of Cyanobacterial Toxins 258Gábor Vasas
24.1 Basic Theory and Introduction of Capillary Electrophoresis 258
24.2 Selection of Separation Methods 259
24.3 Detection Methods 259
24.4 CE Methods of Cyanobacterial Toxins 260
24.5 Future Perspectives 262
References 262
25 Immunoassays and Other Antibody Applications 263James S. Metcalf and Geoffrey A. Codd
25.1 Introduction 263
25.2 Production of Antibodies versus Cyanotoxins 264
25.3 Applications of Cyanotoxin Antibodies 264
25.4 Cyanotoxin Localisation and Quantification Using Antibodies 265
25.5 Other Cyanotoxin Antibody-Related Technologies 265
References 266
26 Protein Phosphatase Inhibition Assays 267James S. Metcalf , Anastasia Hiskia, and Triantafyllos Kaloudis
26.1 Background and Molecular Mechanism of Protein Phosphatase Inhibition 267
26.2 Classes of Compounds that Inhibit Protein Phosphatases 268
26.3 Effects of Microcystins on Cyanobacterial Protein Phosphatases 268
26.4 The Basis of the PPIA Assay for Microcystins and Its Evolution 268
26.5 Comparison of PPIA with Other Analytical Methods for Microcystins 268
26.6 Commercially Available Kits for Microcystins 269
26.7 Improvements to the PPIA Assay to Make It More Specific to Microcystins 269
26.8 Conclusions about the Effectiveness of the PPIA Assay for Microcystins and Nodularins in Different Matrices 269
References 270
27 Bioassay Use in the Field of Toxic Cyanobacteria 272Ludek Bláha, Ana Maria Cameán , Valérie Fessard , Daniel Gutiérrez-Praena , Ángeles Jos , Benjamin Marie , James S. Metcalf , Silvia Pichardo , María Puerto , Andrea Törökné , Gábor Vasas, and Bojana ?egura
27.1 Introduction 272
27.2 Drivers and Objectives for Bioassay Use 273
27.3 Classification and Terminology 274
27.4 Bioassays for the Effect Evaluation 275
27.5 Bioassays for Monitoring 276
27.6 Conclusions and Future Perspectives 278
References 278
28 Molecular Tools for the Detection of Toxigenic Cyanobacteria in Natural Ecosystems 280Jean-François Humbert
28.1 Introduction 280
28.2 Molecular Methods for the Monitoring of Potentially Toxic Cyanobacteria 281
28.3 Strengths and Limitation of These Molecular Approaches 282
28.4 Conclusions 282
References 283
Section VI Methodological Considerations 285
29 Method Validation Guidelines for the Analysis of Cyanotoxins 287Theodoros M. Triantis, Triantafyllos Kaloudis, and Anastasia Hiskia
29.1 Introduction: Method Validation as a Requirement for Laboratory Accreditation 287
29.2 Performance Criteria and Validation Protocols for the Analysis of Cyanotoxins in Environmental Studies 288
29.3 Validation Issues Concerning the Analysis of Cyanotoxins 290
References 291
30 Interpretation, Significance, and Reporting of Results 292Geoffrey A. Codd, Jutta Fastner , Tore Lindholm, Jussi Meriluoto, and James S. Metcalf
30.1 Introduction 292
30.2 Interpretation and Significance of Results 293
30.3 Reporting of Results and Maximization of Benefits 294
30.4 Examples, Debriefing 294
References 296
31 Lessons from the U?ice Case: How to Complement Analytical Data 298Zorica Svircev , Damjana Drobac , Nada Tokodi , Dunja Ðenic , Jelica Simeunovic , Anastasia Hiskia , Triantafyllos Kaloudis , Biljana Mijovic , Stamenko suSak , Mladan Protic , Milka Vidovic , Antonije Onjia , Sonja Nybom , Tamara Va?ic , Tamara Palanacki MaleSevic , Tamara Dulic , Dijana Pantelic , Marina VukaSinovic , and Jussi Meriluoto
31.1 Introduction 299
31.2 Vrutci Reservoir and the Cyanobacterial Bloom Detected in December 2013 299
31.3 Analytical Work: Toxin Analyses of Water, Cyanobacterial Biomass, and Fish from Reservoir Vrutci 301
31.4 Complementary Data on Toxicity and Observed Health Problems 302
31.5 Analytical and Supplementary Results Combined: A Plausible Reconstruction of Events in Vrutci Reservoir and the City of U?ice 306
31.6 Conclusions from the U?ice Case 306
References 307
32 Selection of Analytical Methodology for Cyanotoxin Analysis 309Jussi Meriluoto , James S. Metcalf and Geoffrey A. Codd
32.1 Introduction 309
32.2 General Comparison of Physicochemical Analyses, Biochemical Methods, and Bioassays 309
32.3 Guidance for Selecting and Using Standard Operating Procedures Found in this Handbook 310
32.4 Methodology versus Required Response Time 311
32.5 Influence of Waterbody History on the Choice of Methods 312
32.6 Integration of the Results Obtained: Making Sense 312
Section VII Standard Operating Procedures (SOPs) 313
SOP 1 Cyanobacterial Samples: Preservation, Enumeration, and Biovolume Measurements 315Arnaud Catherine, Selma Maloufi, Roberta Congestri, Emanuela Viaggiu, and Renata Pilkaityte
SOP 2 Chlorophyll a Extraction and Determination 331Claude Yéprémian, Arnaud Catherine, Cécile Bernard, Roberta Congestri, Tina Elersek, and Renata Pilkaityte
SOP 3 Phycocyanin Extraction and Determination 335Claude Yéprémian, Arnaud Catherine, Cécile Bernard, Roberta Congestri, Tina Elersek, and Renata Pilkaityte
SOP 4 Analysis of Picocyanobacteria Abundance in Epifluorescence Microscopy 339Iwona Jasser and Cristiana Callieri
SOP 5 Estimation of Cyanobacteria Biomass by Marker Pigment Analysis 343Jean-Pierre Descy
SOP 6 Extraction of Cyanotoxins from Cyanobacterial Biomass 350Leonardo Cerasino, Jussi Meriluoto, Ludek Bláha, Shmuel Carmeli, Triantafyllos Kaloudis, and Hanna Mazur-Marzec
SOP 7 Solid-Phase Extraction of Microcystins and Nodularin from Drinking Water 354Theodoros M. Triantis, Triantafyllos Kaloudis, Sevasti-Kiriaki Zervou, and Anastasia Hiskia
SOP 8 Extraction of Microcystins from Animal Tissues 358Ondrej Adamovský and Ludek Bláha
SOP 9 Analysis of Microcystins by Online Solid Phase Extraction-Liquid Chromatography Tandem Mass Spectrometry 362Cintia Flores and Josep Caixach
SOP 10 Determination of Microcystins and Nodularin in Filtered and Drinking Water by LC-MS/MS 372Theodoros M. Triantis, Triantafyllos Kaloudis, Sevasti-Kiriaki Zervou, and Anastasia Hiskia
SOP 11 Analysis of Microcystins and Nodularin by Ultra High-Performance Liquid Chromatography Tandem Mass Spectrometry 379Leonardo Cerasino
SOP 12 Analysis of Microcystins in Animal Tissues Using LC-MS/MS 385Jirí Kohoutek and Ludek Bláha
SOP 13 Quantitative Screening of Microcystins and Nodularin in Water Samples with Commercially Available ELISA Kits 390Triantafyllos Kaloudis, Theodoros M. Triantis, and Anastasia Hiskia
SOP 14 Quantitative Screening of Microcystins and Nodularin in Water Samples with Commercially Available PPIA Kits 393Triantafyllos Kaloudis, Theodoros M. Triantis, and Anastasia Hiskia
SOP 15 Solid-Phase Extraction of Cylindrospermopsin from Filtered and Drinking Water 396Theodoros M. Triantis, Triantafyllos Kaloudis, and Anastasia Hiskia
SOP 16 Determination of Cylindrospermopsin in Filtered and Drinking Water by LC-MS/MS 399Theodoros M. Triantis, Triantafyllos Kaloudis, and Anastasia Hiskia
SOP 17 Solid-Phase Extraction of Anatoxin-a from Filtered and Drinking Water 405Theodoros M. Triantis, Triantafyllos Kaloudis, and Anastasia Hiskia
SOP 18 Determination of Anatoxin-a in Filtered and Drinking Water by LC-MS/MS 408Theodoros M. Triantis, Triantafyllos Kaloudis, and Anastasia Hiskia
SOP 19 Analysis of Anatoxin-a and Cylindrospermopsin by Ultra High-Performance Liquid Chromatography Tandem Mass Spectrometry 413Leonardo Cerasino
SOP 20 Extraction and Chemical Analysis of Saxitoxin and Analogues in Water 418Lutz Imhof and Wido Schmidt
SOP 21 Extraction of BMAA from Cyanobacteria 432James S. Metcalf, Sandra A. Banack, and Paul A. Cox
SOP 22 Analysis of ß-N-Methylamino-l-Alanine by UHPLC-MS/MS 435James S. Metcalf, William B. Glover, Sandra A. Banack, and Paul A. Cox
SOP 23 Extraction and LC-MS/MS Analysis of Underivatised BMAA 439Elisabeth J. Faassen
SOP 24 Extraction, Purification, and Testing of LPS from Cyanobacterial Samples 447Lucie Bláhová and Ludek Bláha
SOP 25 Extraction and Chemical Analysis of Planktopeptin and Anabaenopeptins 452Hanna Mazur-Marzec, Tina Elersek, and Agata Blaszczyk
SOP 26 Thamnocephalus Test 462Andrea Törökné
SOP 27 Determination of Geosmin and 2-Methylisoborneol in Water by HS-SPME-GC/MS 469Triantafyllos Kaloudis, Theodoros M. Triantis, and Anastasia Hiskia
SOP 28 Rapid Analysis of Geosmin and 2-Methylisoborneol from Aqueous Samples Using Solid-Phase Extraction and GC-MS 475Christine Edwards, Craig McKenzie, Carlos Joao Pestana, Kyari Yates, and Linda A. Lawton
SOP 29 Basic Validation Protocol for the Analysis of Cyanotoxins in Environmental Samples 481Triantafyllos Kaloudis, Theodoros M. Triantis, and Anastasia Hiskia
Section VIII Appendices 487
Appendix 1 Cyanobacterial Species and Recent Synonyms 489
Appendix 2 Cyanobacteria Associated With the Production of Cyanotoxins 501
Appendix 3 Tables of Microcystins and Nodularins 526
Index 538
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