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Sodium Homeost Asis and the Production of Saxitoxin In SODIUM HOMEOSTASIS AND THE PRODUCTION OF SAXITOXIN IN CYANOBACTERIA FRANCESCO POMATI A Thesis Submitted in Partial Fulfilment of the Requirements for the Degree of Doctor of Philosophy (Ph.D.) SCHOOL OF BIOTECHNOLOGY AND BIOMOLECULAR SCIENCES THE UNIVERSITY OF NEW SOUTH WALES SYDNEY, AUSTRALIA December, 2003 Certificate of Originality I hereby declare that this submission is my own work and to the best of my knowledge it contains no material previously published or written by another person, nor material which to a substantial extent has been accepted for the award of any other degree or diploma at UNSW or any other educational institution, except where due acknowledgement is made in the thesis. Any contribution made to the research by others, with whom I have worked at UNSW or elsewhere, is explicitly acknowledged in the thesis. I also declare that the intellectual content of this thesis is the product of my own work, except to the extent that assistance from others in the project's design and conception or in style, presentation and linguistic expression is acknowledged. CERTIFICATE OF OIUGINALITY I hereby_ declare that this submission is my own work and to the best of my knowledge it contams no matenals previously published or written by another person nor material wh_ich to a substantial extent has been accepted for the award of any ~!her degree or diploma at UNSW or any other educational institution, except where due acknowledgement is made in the thesis. Any contribution made to the research by others, with whom I have worked at UNSW or elsewhere, is explicitly acknowledged in the thesis. Francesco Pomati I also declare that the intellectual content of this thesis is the product of my own work, except to the extent that assistance from others in.Jru:,pro~£!'s design and conception •• "''" •=-·.. ~-"''? 11 a Valeria, Donate/la, Giancarlo e Matteo vincer potero dentro a me l'ardore ch'i' ebbi a divenir del mondo esperto, e de li vizi umani e del valore; ma misi me per l'alto mare aperto (Dante Alighieri, Inferno, Canto XXVI) 111 TABLE OF CONTENTS Abstract Xll Acknowledgments Xlll List of publications xv List of abbreviations xvn Preface, by RalfKellmann XIX CHAPTER! INTRODUCTION 1 1.1 Overview 1 1.1.1 Harmful algal blooms 1 1.1.2 Cyanobacterial blooms 2 1.2 Cyanobacteria 6 1.2.1 Order Nostocales: genera Anabaena and Cylindrospermopsis 9 l .2.2 Anabaena circinalis l 0 l.2.3 Cylindrospermopsis raciborskii 12 1.3 Cyanobacterial bioactive metabolites 14 1.3.1 Cyanotoxins 15 1.3.2 LPS 15 1.3.3 Cyclic peptides 16 1.3.4 Alkaloids 19 1.3.5 PSP toxins 22 1.3.5.1 Chemistry of PSP toxins 25 1.3.5.2 Pharmacology and toxicology of PSP toxins 28 1.3.5.3 Detection methods for PSP toxins 33 1.3.5.4 Ecology and physiology of PSP toxins 39 1.3.5.5 Biosynthesis and Biodegradation of PSP toxins 42 1.3.5.6 Genetics of PSP toxins 46 IV 1.4 Objectives and scopes 48 1.4.1 Aims 48 1.4.2 Hypothesis 48 CHAPTER2 MATERIALS AND METHODS 49 2.1 Bacterial strains and culturing 49 2.1.1 Cyanobacteria 49 2.1.2 Escherichia coli 50 2.2 Analysis of cyanobacterial growth 51 2.2.1 Measurement of growth 51 2.2.2 Total protein assay 51 2.3 Toxin detection and quantification 51 2.3.1 HPLC analysis 51 2.3.2 Protein phosphatase inhibition assay 52 2.3.3 Toxins standards 52 2.4 Flame photometry analysis 53 2.5 Statistical analyses 53 2.6 Nucleic acid extraction 53 2.6.1 Genomic DNA extraction 53 2.6.2 Total RNA extraction 54 2.7 Suppression subtractive hybridisation (SSH) 55 2. 7 .1 Overview 55 2. 7 .2 Driver and tester DNA preparation 58 2.7.3 Subtractive hybridisation 58 2.7.4 PCR amplification 59 2.8 DNA cloning and automated sequencing 59 2.9 DNA microarray design and production 60 2.10 Nucleic acid labelling 61 2.10.1 Preparation of DNA 61 2.10.2 Preparation of total RNA 61 2.10.3 Labelling of genomic DNA and cDNA 61 V 2.11 Microarray hybridisation 62 2.12 Microarray scanning, data acquisition and statistical analysis 62 CHAPTER3 ENHANCEMENT OF INTRACELLULAR SAXITOXIN ACCUMULATION IN Cylindrospermopsis raciborskii T3 BY LIDOCAINE HYDROCHLORIDE 64 3.1 Background 65 3.2 Experimental procedures 66 3.2.1 Reagents 66 3.2.2 Growth conditions and cyanobacterial cultures 66 3.2.3 Extraction for HPLC analysis 67 3.3 Results 67 3 .3 .1 Effect of lidocaine hydrochloride on growth 67 3.3.2 Effect oflidocaine hydrochloride on STX accumulation 71 3.3.3 Time course oflidocaine hydrochloride effect on STX intracellular concentration 72 3.3.4 Effect of pH and Na+ concentration on the lidocaine hydrochloride- induced STX accumulation 73 3 .4 Discussion 75 3.5 Conclusions 77 3.6 Summary 78 CHAPTER4 INTERACTIONS BETWEEN INTRACELLULAR Na+ LEVELS AND SAXITOXIN PRODUCTION IN Cylindrospermopsis raciborskii T3 79 4.1 Background 80 4.2 Experimental procedures 80 4.2.1 Reagents 80 4.2.2 Growth conditions and cyanobacterial cultures 81 4.2.3 Flame photometry analysis 81 4.2.4 Extraction and HPLC analysis 82 VI 4.2.5 Total protein content 82 4.3 Results 83 4.3.1 Effects of pH on Na+-K+ levels and STX content 83 4.3.2 Effect ofNaCl on growth, Na+-K+ levels and STX accumulation 84 4.3.3 Effects of channel-blockers on Na+ _K+ levels and STX accumulation 87 4.4 Discussion 90 4.5 Conclusions 93 4.6 Summary 94 CHAPTERS EFFECTS OF SAXITOXIN AND VERATRIDINE ON BACTERIAL NA+-K+ FLUXES: A PROKARYOTIC-BASED STX BIOASSAY 95 5.1 Background 96 5.2 Experimental procedures 97 5.2.1 Reagents 97 5.2.2 Cyanobacterial strains and culture conditions 97 5.2.3 Total cellular Na+ and K+ content and flame photometry 98 5.2.4 Cyanobacterial cells lysis test 98 5.2.5 Cell titre assay for metabolic activity 99 5.2.6 Luminescent bacteria test 100 5.3 Results 101 5.3.1 Effect of Na+ stress, VTD and STX on total cellular Na+-K+ levels 101 5.3.2 Lysis test with toxic and non-toxic cyanobacteria 102 5.3.3 Effect ofVTD and STX on cyanobacterial metabolic activity 104 5 .3 .4 Effect on bioluminescence by Vi brio fischeri I 05 5 .4 Discussion 107 5.5 Conclusions 110 5.6 Summary 110 vu CHAPTER6 EVIDENCE FOR DIFFERENCES IN THE METABOLISM OF STX AND C1+2 TOXINS IN Cylindrospermopsis raciborskii T3 112 6.1 Background 113 6.2 Experimental procedures 114 6.2.1 Reagents 114 6.2.2 Growth conditions and cyanobacterial cultures 114 6.2.3 In viva experiments 114 6.2.4 In vitro experiments 115 6.2.5 HPLC analysis 116 6.2.6 Protein phosphatase inhibition assay 116 6.2.7 Total protein content 116 6.3 Results 117 6.3.1 Effect of CAM on cyanotoxin accumulation 117 6.3.2 Time course of CAM influence on MCYST and PSP toxin production 118 6.3.3 Effect of substrates on PSP toxins levels 120 6.3.4 In vitro synthesis of PSP toxins under CAM stress and arginine supplementation 123 6.4 Discussion 124 6.5 Conclusions 126 6.6 Summary 127 CHAPTER 7 IDENTIFICATION OF A Na+ DEPENDENT TRANSPORTER ASSOCIATED WITH SAXITOXIN PRODUCING STRAINS OF Anabaena circinalis 128 7 .1 Background 129 7 .2 Experimental procedures 130 7.2.1 Cyanobacteria 130 7 .2.2 DNA extraction 130 7.2.3 PCR amplifications and DNA sequencing 131 Vlll 7.2.4 SSH 132 7.2.5 Microarray design and production 133 7.2.6 Genomic DNA labelling and hybridisation 133 7.2.7 Microarray scanning, data acquisition and statistical analyses 133 7.2.8 Nucleotide sequence accession numbers 134 7.3 Results 134 7.3.1 HIPl genomic polymorphism 134 7.3.2 SSH ofHIPl genomic libraries 137 7.3.3 Microarray hybridisation 141 7.3.4 Amplification of genes encoding Na+ dependent transporters 141 7.3.5 Phylogeny of Na+ dependent transporter proteins 142 7.3.6 Screening for STX-producing A. circinalis by multiplex PCR 143 7.4 Discussion 14 7 7.5 Conclusions 150 7.6 Summary 151 CHAPTERS PCR-BASED POSITIVE HYBRIDISATION TO DETECT GENOMIC DIVERSITY ASSOCIATED WITH BACTERIAL SECONDARY METABOLISM 152 8.1 Background 153 8.2 Experimental procedures 155 8.2.1 Cyanobacterial strains and growth conditions 155 8.2.2 DNA extraction 155 8.2.3 SSH 155 8.2.4 PPH 157 8.2.5 PCR amplifications 159 8.2.6 Microarray design and production 160 8.2.7 Labelling of genomic DNA 160 8.2.8 Microarray hybridisation 160 8.2.9 Microarray scanning, data acquisition and statistical analyses 160 8.2.10 Nucleotide sequence accession numbers 161 lX 8.3 Results 161 8.3.1 Suppression subtractive hybridisation 161 8.3.2 PCR-based positive hybridisation 168 8.3.3 DNA microarray analysis of SSH and PPH libraries 168 8.3.4 PCR amplification of putative unsubtracted PPH toxic-specific sequences 169 8.4 Discussion 170 8.5 Conclusions 172 8.6 Summary 173 CHAPTER9 TRANSCRIPTIONAL ANALYSIS IN Anabaena circinalis USING THE BGGM1 DNA-MICROARRAY: A COMPARATIVE STUDY OF TOXIC AND NON-TOXIC STRAINS AND THE EFFECTS OF LIDOCAINE HYDROCHLORIDE 174 9.1 Background 175 9.2 Experimental procedures 176 9.2.1 Cyanobacterial strains and growth conditions 176 9.2.2 Total RNA extraction 176 9.2.3 Labelling of total RNA 176 9.2.4 Microarray hybridisation 177 9.2.5 Microarray scanning, data acquisition and statistical analyses 177 9.3 Results 177 9.3.1 Comparative analysis of gene expression in toxic and non-toxic strains 177 9.3.2 Effect of lidocaine on gene expression using BGGM1 DNA microarray 178 9 .4 Discussion 185 9.5 Conclusions 188 9.6 Summary 189 X CHAPTERl0 DISCUSSION 190 10.1 General discussion 191 10.2 The physiology of STX production in cyanobacteria 193 10.3 The molecular biology of STX production in cyanobacteria 194 10.4 STX "genes" and STX "enzymes" 195 10.5 Conclusions and significance 198 10.6 Future directions 199 APPENDIX A CYANOBACTERIAL STRAINS USED IN THIS STUDY 202 APPENDIXB GROWTH MEDIA PREPARATION 203 APPENDIXC C.1) PCR-BASED GENOMIC SUBTRACTION ADAPTOR AND PRIMER SEQUENCES 207 C.2) PCR PRIMERS USED IN THIS STUDY 208 APPENDIXD BGGM1 DNA MICROARRAY GENE LIST 209 APPENDIXE EXAMINATION OF COMBINED MICROARRAY DATA SETS 219 APPENDIXF NUCLEOTIDE SEQUENCE GENBANK ACCESSION NUMBERS 221 REFERENCES 223 Xl ABSTRACT Saxitoxin (STX) is the most potent representative among the paralytic shellfish poisoning (PSP) toxins, that are lethal natural Na+ channel-blocking alkaloids.
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