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Cryopreservation, Culture Recovery and Glucose Induced Programmed Cell Death in Chlorophyte Microalgae

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Cryopreservation, Culture Recovery and Glucose Induced Programmed Cell Death in Chlorophyte Microalgae Cryopreservation, culture recovery and glucose induced Programmed cell death in Chlorophyte microalgae Tony Vien Le Bui Bachelor of Biotechnology (Hon) Graduate Certificate in Technology and Innovation Management A thesis submitted for the degree of Doctor of Philosophy at The University of Queensland in 2014 Institute for Molecular Bioscience 1 Abstract Around 350,000 species of microalgae are estimated to have evolved globally (Brodie and Zuccarello 2007), many of which have not been identified. These organisms are potentially useful for a wide range of applications, including biomedical (pharma- and nutraceutical), agricultural (biochar, cattle and aquaculture feeds) and energy applications (bio oil, hydrogen and diesel) and especially high value products. High yielding microalgae strains therefore offer the potential to (at least in part) address the demands of an ever increasing human population across a number of applications. This clear potential has motivated a widespread search for suitable, superior and economically viable microalgae strains, but the workload and costs associated with maintaining larger strain collections, coupled with finite storage capacity poses a significant limitation. One solution to these problems that removes the need for continuous culturing and allows sample storage for theoretically indefinite periods is cryopreservation. There are established techniques however the underlying mechanisms of cryopreservation, which involves freezing and storage at very low temperatures (-196 oC), are poorly elaborated and required further study. The aim of this thesis is to investigate the biological mechanisms relevant to cryopreservation and to apply this knowledge to adapt cryopreservation as a viable technique for the long term storage of a broad range of microalgae. Two successful cryoprotectants were empirically identified: sucrose and dimethyl sulfoxide. They were found to have a synergistic effect in terms of the recovery of cryopreserved samples, with 6.5% (v/v) being the optimum DMSO concentration. The effect of 200mM sucrose was found to be largely due to improved cell survival and recovery after thawing. Additional factors with a beneficial effect on recovery were the elimination of centrifugation steps (minimising cell damage), the reduction of cell concentration (which is proposed to reduce the release of toxic cell wall components) and the use of low light levels during the recovery phase (proposed to reduce photo-oxidative damage). The success of the optimized two-step cryopreservation method led to similar studies on three facets of cryopreservation (Light, carbon sources and ice crystal formation). The study involved the investigations into the effect of dark incubation periods (1, 2, 3, 4, 5, 6, 18 h) after thawing, carbon sources (starch) during recovery and the investigation of high pressure freezing (HPF) as a novel method of cryopreservation (chapter 3). Due to its mechanism of rapidly vitrifying samples by the rapid application of high pressure, HPF can theoretically limit freeze induced injury due to ice crystal formation while the small size of the resultant samples has potential to reduce storage costs. Sample conditions tested included cryoprotectant types (DMSO, methanol, proline, agarose, sucrose, dextrin and trehalose), planchette toxicity (gold plated vs. aluminum), sample size (0.5, 1, 2 1.5, 2 L) and cell concentration (1, 2.5, 5, 10, 20 x 103 cells L-1). Samples grown in heterotrophic media with gold-plated or aluminum planchettes showed no significant difference to control samples. The gold-plated planchette was used for further experimentation due to the faster throughput in comparison to aluminum planchettes. While in principle, proof of viability was established in sample size and cell concentration experiments, both had low recovery rates. This may have been a result of handling processes or the high pressures involved in HPF. Both dark incubation periods and the supplementation of starch (25mg mL-1) lead to increased cell viabilities suggesting the importance of post thaw nutrition and reduction of reactive oxygen species. During culture recovery from cryopreservation, it was noted that cell death was more pronounced in the presence of glucose than that for sucrose, despite rapid initial growth. As the ability to recover cryopreserved cultures is a critical part of the cryopreservation procedure, mechanisms of this effect were investigated. It is theorised that cell death can occur during the cooling (ice crystal formation) or thawing steps (necrosis or programmed cell death) of cryopreservation procedures. It was shown that rapid death of C. sorokiniana was the result of glucose induced reactive oxygen species (ROS) formation and subsequent programmed cell death (PCD). Programmed cell death was confirmed through the observed ROS production (ascorbic acid mediated survival and dihydroethidium staining), caspase activity (caspase inhibitor sensitivity) and the detection of hall mark DNA fragmentation patterns typical of PCD (DAPI staining and agarose gel electrophoresis). These results demonstrate that glucose can induce programmed cell death and provides insights into one form of carbon source incompatibility in growth media. This constitutes chapter 4 and has been submitted for publication to the journal of Phycology. Cryopreservation is an important technical capability for microalgal research and industry. Results obtained from the studies described here demonstrate potential for application towards large scale microalgae production systems (PCD, subsequent ascorbate reducing ROS mediated cell death and varying carbon source preferences for different microalgae species), microalgae species isolation, strain development and high throughput cryostorage (underlying cryopreservation mechanisms) and vitrification solutions for fragile microalgae strains (HPF and associated growth conditions). Finally, there is potential for applications towards the cryopreservation of a broader range of algae. 3 Declaration by author This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis. I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, and any other original research work used or reported in my thesis. The content of my thesis is the result of work I have carried out since the commencement of my research higher degree candidature and does not include a substantial part of work that has been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I have clearly stated which parts of my thesis, if any, have been submitted to qualify for another award. I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the General Award Rules of The University of Queensland, immediately made available for research and study in accordance with the Copyright Act 1968. I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate I have obtained copyright permission from the copyright holder to reproduce material in this thesis. 4 Publications during candidature Peer reviewed papers Bui TVL, Ross IL, Jakob G and Hankamer B (2013) Impact of procedural steps and cryopreservation agents in the cryopreservation of chlorophyte microalgae. PLOS One 8:1-9 Bui TVL, Hankamer BD, Ross IL (2014) Glucose metabolism induces dose-dependent Programmed Cell Death in the single celled green alga Chlorella sorokiniana. J Phycology (Submitted) Publications included in this thesis Bui TVL, Ross IL, Jakob G, Hankamer B (2013) Impact of procedural steps and cryopreservation agents in the cryopreservation of chlorophyte microalgae. PlosOne 8:1-9 – Incorporated as Chapter 2 Contributor Statement of contribution Tony V L Bui (Candidate) Designed experiments (70%) Wrote the paper (70%) Ian L Ross Designed experiments (20%) Wrote and edited paper (20%) Gisela Jakob Isolated and purified microalgae strains for experiment Ben Hankamer Designed experiments (10%) Wrote the paper (10%) Bui TVL, Hankamer BD, Ross IL (2014) Glucose metabolism induces dose-dependent Programmed Cell Death in the single celled green alga Chlorella sorokiniana. J Phycology (Submitted) –Incorporated as Chapter 4 Contributor Statement of contribution Tony V L Bui (Candidate) Designed experiments (70%) Wrote the paper (70%) Ben Hankamer Designed experiments (10%) Wrote the paper (10%) Ian L Ross Designed experiments (20%) Wrote and edited paper (20%) 5 Contributions by others to the thesis Contribution by Eugene Zhang and Julianne Wolf for their routine technical work on subculturing microalgae motherstock on a monthly basis Statement of parts of the thesis submitted to qualify for the award of another degree -None 6 Acknowledgements During the course of my Ph.D, I would not have survived without the help of Eugene Zhang, Julianne Wolf and Gisela Jakob for their support in routine microalgae subculturing. Rosalba Rothnagel for her technical support in using the high pressure freezing apparatus. Anne Sawyer and Alex Foo for their scientific input and Jennifer Yarnold, Sarah Piper and Michael
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