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Mechanisms of Calcification in Coccolithophores

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Mechanisms of Calcification in Coccolithophores UNIVERSITY OF SOUTHAMPTON FACULTY OF NATURAL AND ENVIRONMENTAL SCIENCES Ocean and Earth Sciences Mechanisms of Calcification in Coccolithophores Charlotte Elizabeth Walker Thesis for the degree of DOCTOR OF PHILOSOPHY MARCH 2018 UNIVERSITY OF SOUTHAMPTON ABSTRACT FACULTY OF NATURAL AND ENVIRONMENTAL SCIENCES Ocean and Earth Sciences Doctor of Philosophy MECHANISMS OF CALCIFICATION IN COCCOLITHOPHORES By Charlotte Elizabeth Walker Coccolithophores are unicellular marine algae characterised by the production of calcite coccoliths. As a result of their calcification they contribute significantly to global biogeochemical cycles. Comprehensive understanding of the mechanisms behind calcification remains elusive, due in part to the research focus on one species, Emiliania huxleyi; the most globally abundant of all coccolithophores. It is imperative to investigate calcification in other species to better understand this biogeochemically important process, especially as the ecological success of E. huxleyi may be due to certain physiological differences with other species. This study set out to explore differences between species in the mechanisms of calcification in three primary areas. Firstly, the physiological requirement for calcification remains poorly understood, particularly as non-calcifying strains of E. huxleyi grow normally in laboratory culture. This study identified a contrast in the requirement for calcification between E. huxleyi and the ecologically important Coccolithus braarudii. Calcification disruption had no negative impacts on E. huxleyi but resulted in major growth defects in C. braarudii demonstrating an obligate requirement for calcification in this species. Secondly, the previous identification of Si transporters in some coccolithophores was further investigated using a combination of physiological and expression studies to identify that Si plays a role in heterococcolith calcification during their diploid life stage. C. braarudii Si transporters were also found to be regulated in response to available Si and shown to be expressed in natural populations. Finally, coccolith associated polysaccharides (CAPs) are an integral component of the calcification mechanism known to modulate the precipitation of calcite. The data presented here show that extracellular CAPs differ in structure and composition between species and that they also play an important role in the organisation of the coccosphere, expanding upon their role and importance in calcification. These findings mark crucial physiological differences between coccolithophore species. The identification of a requirement for calcification in coccolithophores highlights the importance of maintaining a coccosphere. The requirement for Si in some species suggests major physiological differences between species which may influence their ecology. Consequently, these contrasting physiological characteristics may contribute to significant differences in the response of coccolithophores to future ocean conditions. i List of Contents 1. Introduction 1 1.1 Coccolithophore Introduction 2 1.2 Coccoliths and Calcification 3 1.3 The Evolution of Calcification 7 1.4 The Role of Calcification 11 1.5 Differences Between Species 13 1.6 Current Study 16 2. The Effect of Ge on Coccolithophores 19 2.1 Abstract 20 2.2 Introduction 21 2.3 Materials and Methods 26 2.3.1 Algal strains and culture conditions 26 2.3.2 Physiological Measurements 26 2.4 Results 28 2.4.1 Effect of Ge exposure on Coccolithus braarudii 28 2.4.2 The ratio of Ge/Si 32 2.4.3 Effect of Ge on Coccolithus pelagicus and Calcidiscus leptoporus 34 2.4.4 Effect of Ge on Emiliania huxleyi and Chrysotile carterae 36 2.5 Discussion 39 3. The requirement for Calcification Differs Between Ecologically 45 Important Coccolithophore Species 3.1 Abstract 46 3.2 Introduction 47 3.3 Materials and Methods 50 3.3.1 Algal strains and culture conditions 50 3.3.2 Cell growth and discarded coccoliths 50 3.3.3 Disruption of calcification 50 3.3.4 Measurements of photosynthesis 51 ii 3.3.5 Time-lapse microscopy 52 3.3.6 Fluorescence microscopy 52 3.3.7 Scanning electron microscopy 52 3.3.8 Immunofluorescence microscopy 53 3.4 Results 54 3.4.1 Disruption of calcification in C. braarudii 54 3.4.2 Disruption of calcification inhibits growth in C. braarudii 56 3.4.3 Low Si inhibits growth where coccosphere formation is disrupted 58 3.4.4 Disruption of calcification does not inhibit photosynthesis 60 3.4.5 The role of the coccosphere during cell division 61 3.4.6 Disruption of the coccosphere prevents separation following cell division 63 3.4.7 A polysaccharide-rich organic layer contributes to cell adhesions in the absence 67 of the coccosphere 3.5 Discussion 69 4. Molecular characterisation of Si transporters in Coccolithus 73 braarudii 4.1 Abstract 74 4.2 Introduction 75 4.3 Materials and Methods 79 4.3.1 Algal strains and culture conditions 79 4.3.2 SITL expression analysis 79 4.3.3 C. braarudii SITL expression in natural populations 82 4.4 Results 84 4.4.1 Uptake of [dSi] by coccolithophores 84 4.4.2 SITL expression during changing Si availability 85 4.4.3 SITL expression changes in response to life cycle stage 87 4.4.4 SITL expression in natural populations 88 4.5 Discussion 91 5. Investigating Coccolith Associated Polysaccharides 95 5.1 Abstract 96 5.2 Introduction 97 5.3 Materials and Methods 101 5.3.1 Algal strains and culture conditions 101 iii 5.3.2 Decalcification of coccolithophores 101 5.3.3 Staining and confocal microscopy 101 5.3.4 Electron microscopy 101 5.3.5 Coccolith preparation 102 5.3.6 Polysaccharide extractions 102 5.3.7 GC-MS preparation and analysis 102 5.4 Results 104 5.4.1 Localisation of extracellular polysaccharides using lectin FITC-conA 104 5.4.2 Localisation of extracellular polysaccharides using lectin FITC-WGA 107 5.4.3 Polysaccharide extraction and composition analysis 109 5.4.4 Production and role of extracellular polysaccharides in C. braarudii 111 5.5 Discussion 114 6. General Discussion 119 6.1 Introduction 120 6.2 Discussion the role of calcification 121 6.2.1 Importance of the coccosphere in C. braarudii 121 6.2.2 Calcification as a potential carbon concentrating mechanisms 122 6.3 Introducing Si as a new component to the calcification mechanism 123 6.4 The evolution of calcification 125 6.4.1 Holococcolith formation 125 6.4.2 Si transporters 127 6.4.3 Obligate requirement for calcification 127 6.5 Ecological Impacts 128 6.5.1 Environmental conditions at the time of coccolithophore evolution 128 6.5.2 Current coccolithophore ecology 129 6.5.3 Response to future ocean scenarios 131 6.6 Concluding remarks 132 Appendices 135 References 169 iv List of Tables and Figures 1. Introduction Figure 1.1 Coccolithophores 2 Figure 1.2 Schematic of coccolithophore calcification 5 Figure 1.3 Coccolithophore phylogeny 10 2. The Effect of Ge on Coccolithophores Figure 2.1 The structure and distribution of SITs and SITLs in coccolithophores 22 Figure 2.2 Effect of Ge on C. braarudii 29 Figure 2.3 Morphological effect of Ge on C. braarudii 30 Figure 2.4 Longer-term effects of Ge on C. braarudii 31 Figure 2.5 The effect of changing Ge/Si ratio on C. braarudii 33 Figure 2.6 The effect of Ge on C. pelagicus 35 Figure 2.7 The effect of Ge on C. leptoporus 36 Figure 2.8 The effect of Ge on E. huxleyi 37 Figure 2.9 The effect of Ge on C. carterae 37 Figure 2.10 The distribution of SIT/Ls in coccolithophores correlated with their 38 sensitivity Ge. 3. The requirement for Calcification Differs Between Ecologically Important Coccolithophore Species Figure 3.1 Disruption of calcification in C. braarudii 55 Figure 3.2 Disruption of calcification leads to a reduction in growth in C. braarudii 57 Figure 3.3 Disruption of calcification by limiting Si availability 59 Figure 3.4 Disruption of calcification with low Ca2+ does not inhibit photosynthetic 60 activity Figure 3.5 Rearrangement of the coccosphere during cell division 62 Figure 3.6 Immunofluorescence microscopy of tubulin in dividing cells 63 Figure 3.7 Paired cells accumulate in cells with disrupted calcification 64 Figure 3.8 Progressive disruption of the coccosphere in C. braarudii cells treated 66 with Ge v Figure 3.9 A structured polysaccharide layer is involved in organisation of the 68 coccosphere 4. The Molecular Characterisation of Si Transporters in Coccolithus braarudii Figure 4.1 The structure and distribution of SITs and SITLs in coccolithophores 76 Figure 4.2. Uptake of [dSi] by T. weissflogii, C. braarudii and E. huxleyi 84 Figure 4.3 The expression of SITLs in response to Si reduction 86 Figure 4.4 Expression of SITLs in response to Si replenishment 87 Figure 4.5 The expression of SITL, EFL and RPS1 genes in haploid C. braarudii 88 Figure 4.6 Expression of SITLs in natural coccolithophore populations 90 81 Table 4.1 Primer details for qPCR Table 4.2 Standard Curve Reaction Efficiencies 82 5. Investigating Coccolith Associated Polysaccharides Figure 5.1 Scanning electron microscopy images of coccolithophore species in 104 this study Figure 5.2 Polysaccharide layer found on the cell surface of decalcified 105 coccolithophores Figure 5.3 Polysaccharide layer associated with coccosphere 107 Figure 5.4 Wheat germ agglutinin staining in S. apsteinii 108 Figure 5.5 Differential localisation of lectin stains in S. apsteinii 109 Figure 5.6 Coccolith polysaccaride composition 111 Figure 5.7 The extracellular polysaccharide is associated with the coccoliths in C. 112 braarudii Figure 5.8 The localisation of coccolith associated polysaccharides 114 100 Table 5.1 Coccolith Associated Polysaccharide Extraction Fractions Table 5.2 Results of polysaccharide lectin staining in coccolithophores 106 vi 1. General Discussion Figure 6.1 Key Findings 120 Figure 6.2 Distribution of holococcoliths, Si-transporters and calcification state in 126 culture vii List of Appendices Appendix I: Chapter 2 Supplementary Information Durak et al.
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