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The Molecular Basis of Circadian and Seasonal

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The Molecular Basis of Circadian and Seasonal Department of Biological and Marine Sciences Thesis submitted for the Degree of Doctor of Philosophy The molecular basis of circadian and seasonal rhythms in the blue mussel Mytilus edulis Emma C. Chapman BSc (Hons), MSc Supervisors: Professor Jeanette Rotchell Professor Dan Parsons October 2019 This copy of the thesis has been supplied on condition that anyone who consults it is understood to recognise that its copyright rests with its author and that no quotation from the thesis and no information derived from it may be published without the author’s prior consent. i Abstract Exposure to regular environmental oscillations such as day/night have allowed organisms to evolve biological mechanisms to adaptively anticipate and prepare for rhythmic environmental change. A network of gene-protein interactions between clock genes and their proteins comprise the molecular clock mechanism at the heart of regulating biological rhythms. Though this is an endogenous and self-regulating system, elements of this network can be entrained by exogenous biotic and abiotic factors. This synchronisation process between environmental cycles and endogenous rhythms is facilitated by cues like light and temperature, which influence clock gene expression patterns. Marine bivalves often inhabit intertidal habitats under the influence of numerous oscillating environmental conditions, though little is known about how they regulate their biological timekeeping. In this thesis, we investigate the molecular regulation of biological rhythms in the ecologically and commercially important blue mussel, M. edulis, over different timeframes. For the first time in this species, we isolate and characterise a number of clock genes (Clk, Cry1, ROR/HR3, Per and Rev- erb) and clock-associated genes (ARNT, Timeout-like and aaNAT). Rhythmic clock gene expression is demonstrated in the absence of light cues, indicative of endogenous clock control. Differential expression of Cry1 expression between males and females under the same conditions indicates sex-specific regulation and/or function. In addition, diurnal temperature cycles modulated the otherwise rhythmic expression of Rev-erb to constant levels demonstrating an interaction of temperature with clock function. Instances of seasonal clock mRNA expression differences were found, in addition to a number of other putative seasonal genes, indicating a possible mechanism ii by which seasonal cues can inform rhythmic biological processes. Understanding the influence of environmental cues on the molecular clock is essential in predicting the outcomes of future environmental change on fundamental rhythmic processes, in particular the impacts of decoupled environmental cues on the already highly dynamic and stressful intertidal zone. iii Acknowledgements I would especially like to thank my supervisors Prof Jeanette M. Rotchell and Prof Daniel R. Parsons for their help, support and guidance throughout this PhD. It wouldn’t have been possible without you so thank you for everything. I would also like to thank Jennie Brigham and the School of Biological, Biomedical and Environmental Sciences/ Department of Biological and Marine Sciences for supporting my part-time studies. Many thanks also go to David O’Neill, Dr Rose Wilcox and Prof Jeanette M. Rotchell for helping with sample collection and mussel dissections at all sorts of hours of the day and night. Finally, thank you to my family for their support and encouragement. iv Publications Some aspects of this work have been published. Research from Chapters 2 to 4 appears in: Chapman, E.C., O’Dell, A.R., Meligi, N.M., Parsons, D.R. and Rotchell, J.M., 2017. Seasonal expression patterns of clock-associated genes in the blue mussel Mytilus edulis. Chronobiology International, 34(9), 1300-1314. Research from Chapters 5 and 6 appears in: Chapman, E.C., Parsons, D.R. and Rotchell, J.M., 2020. Influence of light and temperature cycles on the expression of circadian clock genes in the mussel Mytilus edulis. Marine Environmental Research, 159. 104960 Author Statement JR was responsible for conceptualization, funding and supervision in general for both papers. EC was also responsible for the conceptualization, and conducted sample investigation and formal analysis. AO, NM and BB conducted sample investigation. DP reviewed the work. EC and JR took the lead in preparing the manuscripts and the data visualization. v Contents Chapter 1 – Introduction and literature review .......................................................... 1 1.1 BIOLOGICAL RHYTHMS ......................................................................... 1 1.2 CIRCADIAN RHYTHMS ........................................................................... 4 1.2.1 The molecular clock mechanism ............................................................ 6 1.2.2 The central and peripheral clock mechanisms ..................................... 13 1.3 SEASONAL AND CIRCANNUAL RHYTHMS ..................................... 15 1.3.1 Photoperiodism .................................................................................... 16 1.3.2 Molecular regulation of photoperiodism .............................................. 19 1.4 THE MELATONIN SYNTHESIS PATHWAY ........................................ 21 1.5 RHYTHMS AND CLOCK GENES IN AQUATIC MOLLUSCS............ 23 1.5.1 Biological rhythms in aquatic molluscs ............................................... 23 1.5.2 Seasonal rhythms and photoperiodism in molluscs ............................. 32 1.5.3 Clock genes in aquatic molluscs .......................................................... 34 1.5.4 The melatonin synthesis pathway and molluscs .................................. 36 1.6 THE BLUE MUSSEL M. EDULIS ............................................................ 38 1.6.1 Description, habitat and distribution .................................................... 38 1.6.2 Life cycle and gametogenesis .............................................................. 39 1.6.3 Light perception ................................................................................... 41 1.6.4 Temperature perception ....................................................................... 42 1.6.5 Mechanoreception ................................................................................ 42 1.6.6 Relevance of M. edulis chronobiology................................................. 43 vi 1.7 THESIS AIMS AND OBJECTIVES ......................................................... 45 Chapter 2 – Isolation and characterisation of circadian rhythm-related genes from the blue mussel M. edulis ................................................................................................ 48 2.1 INTRODUCTION ..................................................................................... 48 2.2 MATERIALS AND METHODS ............................................................... 51 2.2.1 Sampling .............................................................................................. 51 2.2.2 Total RNA isolation ............................................................................. 51 2.2.3 RNA quantification .............................................................................. 52 2.2.4 Denaturing formaldehyde-agarose (FA) RNA gel ............................... 52 2.2.5 cDNA synthesis and Ribonuclease H Treatment ................................. 54 2.2.6 Species Identification ........................................................................... 54 2.2.7 PCR Primer design and selection ......................................................... 55 2.2.8 Polymerase Chain Reaction (PCR) amplification ................................ 57 2.2.8.1 Isolation of Clk.............................................................................. 58 2.2.8.2 Isolation of Cry1 ........................................................................... 59 2.2.8.3 Isolation of ARNT ......................................................................... 60 2.2.8.4 Isolation of Tim ............................................................................. 61 2.2.8.5 Isolation of ROR/HR3 ................................................................... 61 2.2.8.6 Isolation of aaNAT ........................................................................ 62 2.2.9 Agarose gel electrophoresis ................................................................. 63 2.2.10 Purification of DNA from agarose gels ............................................... 64 2.2.11 DNA quantification .............................................................................. 64 2.2.12 Cloning of PCR products ..................................................................... 65 vii 2.2.13 Purification of plasmid DNA from E. coli liquid cultures ................... 66 2.2.14 PCR on purified plasmid DNA ............................................................ 67 2.2.15 Sequencing ........................................................................................... 68 2.2.16 Rapid Amplification of cDNA Ends (RACE) ...................................... 68 2.2.16.1 Preparation of RACE-ready cDNA .............................................. 69 2.2.16.2 RACE PCR Reactions .................................................................. 70 2.2.17 Gene characterisation and analysis of sequence data ........................... 71 2.2.17.1 BLAST comparison searches........................................................ 71 2.2.17.2 Multiple sequence amino acid alignments ...................................
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