造礁珊瑚與單細胞渦鞭毛藻所形成的胞內共生現象，即建立在代謝營養物質交換的互利關係上，而胞內共生細胞間的代謝分子交換則是支撐起此成功的海洋生態系的關鍵；研究珊瑚宿主與共生藻的代謝產物間交互作用有助於更深入了解胞內共生機制。先前研究發現在造礁珊瑚內胚層的脂質體(LBs)是調節維繫胞內共生的關鍵胞器，當共生現象因內在或外在環境消長時，脂質體亦隨之變化；而在日夜週期下，觀察到脂質體在數量、形態上的週期性韻律變化，也認為它是一個動態胞器，並且發現其脂質成份在共生機制間的生物生理代謝具有重要的功能。
此研究收集日夜週期下的珊瑚觸手，並將珊瑚內胚層分離出各個細胞組成：珊瑚動物宿主細胞、脂質體及共生藻，進一步分析其脂質及脂肪酸成分，提出了以往未發現的脂質生合成動態變化。首先，從不同細胞組成分離出六種主要脂質種類（蠟酯、固醇酯、三酸甘油酯、膽固醇、游離脂肪酸、磷酯質）各自顯示出其不同的晝夜變化。第二，各細胞組成在脂質含量、飽和及不飽和脂肪酸的比例
隨著時間而改變，而其相關性及差異性顯示出宿主與共生藻脂質代謝關係中，脂質體作為一個脂質生合成及代謝交流的中樞胞器。第三，脂質體與宿主細胞的脂質種類及脂肪酸組成變化，在不同時間點間皆有著較為相近的關係，顯示脂質體的起源可能來自於動物宿主細胞，實驗結果也指出脂質體具有自我合成代謝部分脂質成分的功能。
此外，利用光合作用抑制劑實驗結果，再次證明共生關係中，宿主細胞、脂質體以及共生藻各自所扮演的角色及其重要性，並指出珊瑚動物宿主及脂質體的脂質成分及含量，受到共生藻的影響。最後，以次世代定序分析日夜週期下的珊瑚基因體發現，其脂質、脂肪酸代謝及脂質體生合成相關的基因表現隨著日夜週期而變化，並顯示於這些脂質相關基因，珊瑚宿主於日出後具有較高比例的基因表現，而多數共生藻基因則是在中午後表現量增加。
綜上所述，本研究對於脂質體在共生關係間的調控，其關鍵定位也有更多實驗證據支持，也發現珊瑚宿主及脂質體在脂質生合成與共生藻脂質代謝間的動態關聯；並指出珊瑚胞內共生關係，是由動態的共生機制所調控，包含各個分子層次，其中脂質分子及基因調控下日夜週期的變化，進一步提供了在脂質體及基因體學的實驗證據，證明了脂質體為一珊瑚與共生藻胞內共生能量交換及共生機制調控的樞紐。

Reef-building corals engage in symbiosis with single-celled dinoflagellate algae (genus Symbiodinium), from which they acquire photosynthetically-fixed organic carbon that supports most of their energetic needs. Metabolic exchange is central to the ecological success of the coral-dinoflagellate endosymbiosis, and elucidating the metabolic dialogue between host coral and Symbiodinium will be critical to ultimately revealing the molecular mechanisms that bind these evolutionarily distant taxa together. It has been proposed that lipid bodies (LBs) in the gastrodermal tissues of reef corals are key organelles in the regulation of this endosymbiosis. The fact that there are temporal changes in LB distribution, composition, and morphology suggests that the host-Symbiodinium endosymbiosis is quite dynamic over the diel cycle with respect to metabolite production and catabolism.
Herein, we provide lipidome-scale evidence to shed further light on the metabolic relationship between host tissues, LBs, and Symbiodinium, with a particular focus on the different fatty acid moieties found in each of these three compartments. First, the concentrations of all major lipid classes (wax esters [WE]. sterol esters [SE], triacylglycerols [TAG], cholesterols [Col], free fatty acids [FFA], and phospholipids [PL]) exhibited diel fluctuations in all compartments, and the patterns of diel variability were compartment-specific. Secondly, the concentration of various fatty acid moieties and ratio of saturated to polyunsaturated fatty acids in these compartments varied over time, resulting in dynamic lipid profiles. The diel relevance of these differences in the lipidomes indicated that the LB is a marker organelle of lipogenesis in coral-Symbiodinium metabolism. Thirdly, the acyl pool profiles of the individual LB lipid classes were more similar, but not equal to, those of the host gastrodermal cells in which they were located, indicating partially autonomous lipid metabolism in these LBs.
Furthermore, an imbalance in the symbiotic status caused by the inhibition of photosynthetic carbon input through DCMU exposure not only caused significant changes to the lipid composition of the LB, but also affected the lipidomes of the host gastrodermal cells and the symbionts. Our data showed that carbon fixation via photosynthesis produces a large portion of the initial carbon skeletons used for lipid biosynthesis in host gastrodermal cells and in LBs. Finally, we investigated the transcriptome of the host and Symbiodinium by next generation sequencing. We found that the expression of genes involved in lipid metabolism, fatty acid metabolism and LB biogenesis exhibit diel changes. Expression levels of genes involved in these pathways were highest at dawn in host cells while the Symbiodinium had a peak in expression at noon time. Such diel changes in mRNA expression may have driven the changes in lipid composition of the three cellular compartments.
In summary, based on the examination of lipidomic dynamics the present study revealed that the LB plays a pivotal role in regulating lipid metabolism within the coral-Symbiodinium endosymbiosis. Thus, lipidomic metabolite exchange via LBs is a key endosymbiotic mechanism underlying the dynamic association of host corals with the dinoflagellate Symbiodinium.

Table of Contents - Page

審定書 - i
授權書 - ii
誌謝 - iii
摘要 - iv
Abstract - vi
Abbreviations - ix
Table of Contents - xiv
List of Figures - xxi
List of Tables - xxv
List of Appendix - xxviii

Chapter 1. Introduction - 1
1.1. Coral, Symbiodinium and endosymbiosis - 1
1.1.1. Corals and symbiotic dinoflagellates - 1
1.1.2. Photosynthesis of Symbiodinium - 2
1.1.3. Establishment and breakdown of endosymbiotic association - 4
1.1.4. The regulation of endosymbiosis - 5
1.2. Dynamics of the lipids fluxes in symbiotic corals - 6
1.2.1. Lipids in symbiotic corals - 6
1.2.2. Lipid fluxes between coral host and algal symbionts - 8
1.2.3. Lipid and fatty acid metabolism - 10
1.2.4. Lipid bodies in coral–dinoflagellate endosymbiosis - 13
1.3. Research goal - 17
1.3.1. Experiment I. Comparison of lipid profile and fatty acid moiety among the LBs, host tissue and Symbiodinium - 19
1.3.2. Experiment II. Examination of lipidomics between three compartments during the diel cycle - 19
1.3.3. Experiment III. Investigation of lipidomics in host gastrodermal cells between healthy coral and treat with photosynthesis inhibitor - 20
1.3.4. Experiment IV. Determination of the gene expression between host coal and Symbiodinium - 20
1.3.5. A combination of four specific approaches elucidate the lipidomic mechanism in coral-Symbiodinium endosymbiosis - 21

Chapter 2. Material and Methods - 23
2.1. Coral collection/maintenance and Symbiodinium culture - 23
2.2. Separation of the cellular compartments in coral host - 24
2.2.1. Separation of the tissue layer in host - 24
2.2.2. Homogenization of the gastrodermal cells - 25
2.2.3. Purification of the endosymbiotic Symbiodinium and LB - 26
2.2.4. Purification of the cell lysates from host gastrodermal cell - 27
2.3. Assessment of the purity for different cellular compartments - 28
2.4. Lipid analysis by HPLC - 30
2.5. Fatty acid and wax ester analysis by GC/MS - 32
2.6. Study of photosynthesis inhibitor-treated coral - 34
2.6.1. Exposure and recovery experiments - 34
2.6.2. Treatment of coral with DCMU - 35
2.6.3. Analysis of photosynthetic efficiency by PAM fluorometry - 36
2.6.4. Fluorescence analysis of the chlorophyll - 37
2.6.5. Ultrastructure morphology determination by TEM - 38
2.6.6. Measurement of the size of LBs in hosts by imaging analyses - 41
2.7. Expression of gene involving in lipidomic metabolism during diel cycle - 41
2.8. Statistical analysis of the data - 43

Chapter 3. Results - 45
3.1. Experiment I. Comparison of lipid profile and fatty acid moiety among the LBs, host tissue and Symbiodinium - 45
3.1.1. Purify the host tissue, LBs and symbionts - 45
3.1.2. Difference amount of each lipid classes - 46
3.1.3. Fatty acid moieties of total lipids - 47
3.1.4. Identification of WE content and species - 48
3.1.5. Fatty acid moieties in SE - 49
3.1.6. Fatty acid moieties in TAG - 50
3.1.7. Fatty acid moieties in FFA - 51
3.1.8. Fatty acid moieties in PL - 51
3.1.9. Summary - 52
3.2. Experiment II. Diel fluctuations in the lipidomes of three compartments of the coral-dinoflagellate endosymbiosis - 54
3.2.1. Diel fluctuation in lipid amounts - 54
3.2.2. Dynamic change in total fatty acid pools - 55
3.2.3. Variation in individual lipid amounts - 57
3.2.4. Diel changes in WE amounts - 59
3.2.5. Temporal contribution of individual lipids to LB formation - 60
3.2.6. Inter-compartmental lipid involvement - 61
3.3. Experiment III. The lipidomes of multiple, cellular compartments of coral-dinoflagellate endosymbioses exposed to the photosynthesis inhibitor DCMU - 63
3.3.1. Treatment of corals with a photosynthesis inhibitor - 63
3.3.2. Effects of DCMU on coral physiology - 64
3.3.3. LB morphology changes - 65
3.3.4. Inter-compartmental lipid variation during DCMU treatment - 66
3.3.5. Inter-compartmental FA moiety variation during DCMU treatment - 67
3.3.6. Inter-compartmental WE variation during DCMU treatment - 69
3.4. Experiment IV. The diurnally variable transcriptome of a reef coral - 70
3.4.1. Illumina sequencing and de novo assembly - 70
3.4.2. Functional annotation of the transcriptome - 71
3.4.3. KEGG pathways annotation of the lipidomic transcriptome - 72
3.4.4. Cluster analysis of transcriptome involved in lipid metabolism - 73
3.4.5. Expression of genes involved in lipid metabolism and ER stress pathways over the diel cycle - 74

Chapter 4. Discussion - 77
4.1. Comparison of lipid profile and fatty acid moiety among the LBs, host tissue and Symbiodinium - 77
4.1.1. Methodological quality control - 78
4.1.2. Inter-compartmental lipid differences - 79
4.1.3. Fatty acid pool distribution - 81
4.1.4. The role of the host coral in LB lipid synthesis - 83
4.1.5. Lipid profiles of in hospite vs. cultured Symbiodinium - 84
4.1.6. Conclusion - 87
4.2. Diel fluctuations in the lipidomes of three cellular compartments of a reef coral. - 89
4.2.1. Temporal dynamic of endosymbiosis status - 89
4.2.2. Temporal lipogenesis changes result in diel rhythmicity of LB formation - 92
4.2.3. LBs as a lipid exchange point for lipid metabolites in endosymbiosis - 95
4.2.4. Conclusion - 96
4.3. The lipidomes of multiple cellular compartments of a reef-building coral exposed to a photosynthetic inhibitor - 99
4.3.1. DCMU arrest of Symbiodinium photosynthesis - 100
4.3.2. Effects of DCMU on lipid bodies - 101
4.3.3. The decrease in storage lipid levels in response to DCMU treatment - 103
4.3.4. Coral metabolic imbalance - 105
4.3.5. Conclusion - 106
4.4. The diel transcriptome of lipid metabolism in multi-cellular compartments - 108
4.4.1. Transcriptome assembly and annotation - 108
4.4.2. The diel dynamics of the lipidomic transcriptome - 109
4.4.3. Endoplasmic reticulum stress and lipid metabolism - 110
4.4.4. Conclusion - 112

Chapter 5. Summary - 115
5.1. The individual character of coral host, LBs and Symbiodinium in LB biogenesis and lipogenesis during the interactions of coral–Symbiodinium - 115
5.2. The variation of temporal lipid profiles and fatty acid moieties in diel rhythmicity of LB formation - 116
5.3. The lipidomic and related genomic could provide direct insight to understand the stable relationship of coral-Symbiodinium endosymbiosis - 116

References - 117
Figures - 153
Tables - 203
Appendixes - 245

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