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The Origin of Coelenterate Bioluminescence

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The Origin of Coelenterate Bioluminescence THE REGULATION AND ORIGIN OF BIOLUMINESCENCE IN THE HYDROID OBELIA Valerie Jane Morse A thesis submitted to Cardiff University in accordance with the requirements for the degree of Philosophiae Doctor December 2013 Cardiff University School of Pharmacy and Pharmaceutical Sciences Redwood Building King Edward VII Avenue Cardiff CF10 3NB i “For see, the glow-worm lights her amorous fire! Thus, ere night’s veil had half obscured the sky, The impatient damsel hung her lamp on high: True to her signal, by love’s meteor led, Leander hasten’d to his Hero’s bed.” The Rev Gilbert White, 1902. ii Summary There are many questions associated with the understanding of the origin and regulation of bioluminescence. A key question underlying this thesis was why coelenterazine evolved as the most common marine luciferin. Another problem addressed was the coelenterazine source of the bioluminescent hydroid Obelia, which is unknown. Coelenterazine is an integral part of Obelia’s photoprotein, triggered by Ca2+. The thesis also investigated the uncertainty over how Ca2+ enters Obelia’s photocytes. Obelia is considered to have four species, but they have been misidentified. Green fluorescent protein (GFP) acts as a fluor in Obelia producing green light. The selective advantage of this green bioluminescence requires confirmation. Results showed that Obelia geniculata cultures rapidly lost their bioluminescence, indicating Obelia requires a dietary supply of coelenterazine. Adding coelenterazine to Obelia briefly restored its bioluminescence. Levels of obelin dropped in Obelia geniculata cultures. Obelia longissima had a lower level of coelenterazine and bioluminescence than Obelia geniculata. Coelenterazine was detected in species living on Obelia and, three non luminous species of copepod. A range of species were identified in zooplankton, as possible coelenterazine sources. Ratios of obelin to apoobelin changed in older colonies. The problem of misidentification of Obelia species was solved by utilising the fluorescent patterns of Obelia’s photocytes. GFP was recorded for the first time in the hydrotheca and tentacles of Obelia dichotoma. Fluorescence maxima for Obelia geniculata and Obelia dichotoma iii were different. GFP in Obelia was found to photobleach far slower than GFP in EGFP. This supports the hypothesis that Obelia has a molecular mechanism which protects its GFP from photobleaching. Light emission from Obelia geniculata was different from Obelia longissima. This suggests that the mode of entry of Ca2+ into the photocytes of these two species is different. To investigate the exact pathway by which initial stimulation of Obelia causes Ca2+ to enter the photocytes, experiments were conducted using K+ channel blockers. The potassium ion channel blockers tetraethyl ammonium chloride and 4-aminopyridine both produced a bioluminescent response in Obelia geniculata. This suggested that the pathway included K+channels. In a polar solvent coelenterazine produced low chemiluminescence, which increased with increasing luciferin concentration. Human albumin and BSA increased this effect. This supported the solvent cage hypothesis that bioluminescent proteins originally evolved as primitive oxygenase enzymes. iv DECLARATION This work has not been submitted in substance for any other degree or award at this or any other university or place of learning, nor is being submitted concurrently in candidature for any degree or other award. Signed 19.12.13 STATEMENT 1 This thesis is being submitted in partial fulfilment of the requirements for the degree of PhD Signed Date 19.12.13 STATEMENT 2 This thesis is the result of my own independent work/investigation, except where otherwise stated. Other sources are acknowledged by explicit references. The views expressed are my own. Signed. (Candidate) Date 19.12.13 v STATEMENT 3 I hereby give consent for my thesis, if accepted, to be available for photocopying and for inter-library loan, and for the title and summary to be made available to outside organisations. Signed (Candidate) Date 19.12.13 vi CONTENTS CHAPTER 1 – Introduction 1.1 Marine bioluminescence 2 1.1.1 Bioluminescence and chemiluminescence 3 1.1.2 Photoluminescence 4 1.1.3 The components of a chemiluminescent reaction 5 1.1.4 The early history of bioluminescence 6 1.1.5 The biochemistry of marine bioluminescence 8 1.1.6 The occurrence of bioluminescence 12 1.2 The five classes of luciferins 15 1.2.1 Imidazolopyrazines 15 1.3 Coelenterate bioluminescence 17 1.3.1 Bioluminescent Zoophytes 17 1.3.2 Bioluminescent Cnidaria 18 1.3.2.1 Bioluminescent Hydrozoans 19 1.3.2.2 Bioluminescent Anthozoans 25 1.3.2.3 Bioluminescent Scyphozoans 29 1.3.3 Bioluminescent Ctenophora 31 1.4 Applications of bioluminescence 32 1.4.1 The functions of marine bioluminescence 31 1.4.1.1 Bioluminescence and fluorescence in Obelia 32 1.4.2 The evolution of bioluminescent proteins 38 1.4.3 The hypothesis for coelenterazine synthesis 39 1.5 Key problems 40 1.6 Strategy 40 CHAPTER 2 – Materials and Methods 2.1 Materials 43 2.1.1 General reagents 43 2.1.1.1 Chemicals 43 2.1.1.2 Solvents 43 2.1.2 Composition of reagents and buffers 2.2 The measurement of chemiluminescence 44 2.2.1 The Chemiluminometer 44 2.2.1.1 Optimisation of the chemiluminometer 48 2.2.1.2 Measuring the bioluminescence of hydroids 50 2.2.2 The Photek imaging system 50 2.2.2.1 Measuring spectra 53 2.2.2.2 The Photek colour palette 53 2.2.2.3 Calculating odd area set data 54 2.2.3 Olympus bioluminescence imaging system 57 2.2.4 The extraction of obelin 60 2.2.5 Measuring the activity of obelin 60 vii 2.3 Measuring and photographing fluorescence 60 2.3.1 FLIM 61 2.4 Measuring water quality 61 2.4.1 Measuring oxygen levels 62 2.4.2 Measuring nitrate levels 62 2.4.3 Measuring salinity 62 2.5 Preservation of hydroid specimens 62 2.6 Measuring bioluminescence in a culture of Obelia 63 2.6.1 Measuring obelin activity in culture 63 2.6.2 Measuring apoobelin levels 63 2.7.1 Apoaequorin 63 2.7.2 The coelenterazine assay 63 2.7.3 Extraction of coelenterazine 63 CHAPTER 3 – Identification and distribution of Obelia 3.1 Introduction 63 3.1.1 Historical review and species identification 63 3.1.2 Obelia species 64 3.1.3 Cnidarians 66 3.1.4 Obelia habitats 68 3.1.5 Obelia life cycle 68 3.1.6 Obelia structure 70 3.1.7 Bioluminescence 73 3.1.7.1 Photocytes in Obelia 73 3.1.7.2 Obelin 74 3.1.8 Identifying Obelia species 78 3.1.9 GFP locations 82 3.1.10 Aims and strategy 85 3.2 Methods 86 3.2.1 Measuring GPS 86 3.2.2 Bioluminescent marine organisms 86 3.2.3 Sample sites in Plymouth 86 3.2.4 Sample sites in Pembrokeshire 87 3.2.5 Measuring water quality 92 3.2.6 Measuring and photographing fluorescence 92 92 3.3 Results 97 3.3.1 Pembrokeshire hydroid sample sites 97 3.3.2 Water quality at key sample sites 100 3.3.3 Fluorescent photocyte patterns in Obelia species 100 3.3.4 Bioluminescence of Obelia 105 3.4 Discussion and future work 110 viii CHAPTER 4 – How is light emitted in Obelia? 4.1 Introduction 122 4.1.1 How light emission is triggered 122 4.2 Methods 129 4.2.1 Varying potassium ion concentration 129 4.2.2 The effect of ion channel blockers 129 4.2.3 Calculating odd area set data 129 4.3 Results 130 4.3.1 Relative mean bioluminescence of Obelia species 130 4.3.2 Effect of varying K+ concentration on bioluminescence 136 4.3.3 Photek imaging of bioluminescence 138 4.3.3 Effect of ion channel blockers on bioluminescence 152 4.4 Discussion and future work 155 CHAPTER 5 – How is coelenterazine obtained by Obelia? 5.1 Introduction 162 5.1.1 Diet verses synthesis of coelenterazine 162 5.1.2 Evidence for dietary source 163 5.1.3 Evidence for synthesis 166 5.2 Methods 169 5.2.1 Culturing Obelia 169 5.2.2 Zooplankton sampling 171 5.2.3 Photographing zooplankton 172 5.2.4 Measuring bioluminescence in culture 173 5.2.6 Activity of obelin 173 5.2.7 Measuring apoobelin level 174 5.2.8 GE of apoaequorin 173 5.2.5 Extraction of obelin 175 5.2.9 Coelenterazine assay 176 5.2.10 Extraction of coelenterazine 177 5.3 Results 178 5.3.1 Experiments on Obelia cultures 178 5.3.2 Species identified in zooplankton 181 5.3.3 Coelenterazine content in zooplankton 191 5.3.4 Apo obelin/obelin ratios in Obelia 194 5.4 Discussion and future work 195 CHAPTER 6 - The effect of GFP on the wavelength of light emitted by Obelia 6.1 Introduction 206 6.1.1 Colours of bioluminescence 206 6.1.2 GFP 207 ix 6.1.3 Photobleaching 210 6.1.3.1 Photobleaching in Obelia 211 6.2 Methods 213 6.2.1 Confocal microscopy 213 6.2.2 Confocal fluorescent microscopy 214 6.2.3 Photek spectra 214 6.2.4 Dual wavelength chemiluminometry 215 6.2.5 RGB fluorescent images 215 6.2.6 Photobleaching 216 6.2.7 Calculating half-life 217 6.2.8 EGFP 217 6.3 Results 218 6.3.1 Confocal fluorescent microscopy 218 6.3.2 Dual wavelength chemiluminometry 219 6.3.3 Colour ratios for fluorescence in Hydrozoans 220 6.3.4 Photobleaching 224 6.4 Discussion and future work 242 CHAPTER 7 – Evolution of bioluminescence 7.1 Introduction 248 7.2 Methods and materials 250 7.2.1 Coelenterazine 250 7.2.2 Measurement of chemiluminescence 250 7.2.3 Sequence similarities 251 7.3 Results 251 7.3.1 Sequence similarities 251 7.3.2 Protein experiments 255 7.4 Discussion and future work 258 CHAPTER 8 – Bioluminescence in education 8.1 Introduction 263 8.2 Methods 270 8.3 Results 274 8.4 Discussion and future work 283 CHAPTER 9 – General discussion 9.1 Summary of main findings 287 9.2 Future studies 291 References 294 x Appendices 307 (i) Publication relevant to this thesis 307 (ii) Presentations & posters given 307 (iii) Training courses attended 308 xi Acknowledgements I am thankful to both my supervisors Prof Anthony Campbell and Prof Ken Wann who have guided and supported me throughout this doctoral degree.
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