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Production of Carotene with Chemostat Cultures of Dunaliella

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Production of Carotene with Chemostat Cultures of Dunaliella Production of carotene with chemostat cultures of Dunaliella ACADEMISCH PROEFSCHRIFT ter verkrijging van de graad van doctor aan de Universiteit van Amsterdam, op gezag van de Rector Magnificus prof. dr. P.W.M. de Meijer ten overstaan van een door het college van dekanen ingestelde commissie in het openbaar te verdedigen in de Aula der Universiteit op donderdag 19 oktober 1995 te 13.00 uur door Pieter Vorst geboren te Zijpe Promotiecommissie: Prof. Dr. H. van den Ende (promotor) Prof. Dr. L.R. Mur (promotor) Prof. Dr. A. Gibor Prof. Dr. K.J. Hellingwerf Dr. F.M. Klis Prof. Dr. J. W. de Leeuw Dr. H.C.P. Matthijs Prof. Dr. L.H.W. van de Plas The research presented in this thesis was carried out at the Research School BioCentrum Amsterdam, Institute for Molecular Cell Biology, section Plant Physiology, University of Amsterdam, Kruislaan 318, 1098!SM Amsterdam, The Netherlands. Publication of this thesis was financially assisted by contributions of Apotheken Almere Haven, the University of Amsterdam, family and friends. The cover illustration and the cartoons, introducing each chapter, were made by Sijko Florijn. voor Laura, Jonathan & Tobias Contents page Chapter 1 Introduction. 9 Chapter 2 Comparison of two species of Dunaliella with 23 emphasis on the factors influencing the specific growth rate. Chapter 3 Carotene accumulation in Dunaliella bardawil is 43 brought about by growth arrest, using nitrate-limited chemostat cultures. Chapter 4 Regulation of carotene- and starch synthesis in 65 Dunaliella bardawil, in relation to growth arrest. Chapter 5 Effect of growth arrest on carotene accumulation and 85 photosynthesis in Dunaliella. Chapter 6 General Discussion. 101 Samenvatting 105 Chapter 1 Introduction INTRODUCTION INTRODUCTION. 1. General Introduction The unicellular green alga Dunaliella is becoming an important model system for experimental biology. Especially its resistance to high salinity, high light intensi- ties and other stresses, which are most important in plant biology, makes it a popular object of research. This is strengthened by the fact that it is a quite amenable organism to study the effects of environmental variables on various cellular processes, such as photosynthesis, respiration, phospholipid metabolism and secondary metabolism. Dunaliella stands out as an organism that accumulates carotenoids in response to stress. For that reason, it is successfully applied for carotene produc- tion on an industrial scale. This thesis deals with this specific property. One of the principal aims was to explore possibilities for optimizing this carotenoid production by Dunaliella. Morphology. Members of the genus Dunaliella are unicellular green algae, with two flagella of equal length placed at the anterior side. The cell shape is usually ovoid, although this can vary with growth conditions. The cell lacks a rigid cell wall but is covered with a mucilaginous coat (Melkonian and Preisig, 1984). One large, cup-shaped chloroplast is located at the posterior side of the cell. A pyrenoid is present in the chloroplast. An eyespot (D. bioculata has two eyespots) is laterally located at the anterior part of the chloroplast. Some species are able to accumulate large amounts of carotene. These carotenoids are located in oily globules in the interthy- lakoid space of the chloroplast and they give the cells an orange or red appear- ance, depending on the amount of carotene. Taxonomy. As a member of the Chlorophyta the genus Dunaliella is placed in the class Chlorophyceae, the order Volvocales and the family Polyblepharidaceae. Ettl (1983) used a different classification and placed Dunaliella in the new order Dunaliellales with the family Dunaliellaceae. Presently 28 species of Dunaliella are recognized, of which 5 occur in freshwater and 23 in saline environments (Preisig, 1992). Distinction between species is primarily based on morphological character- - 9 - CHAPTER 1 istics. These characteristics are subject to environmental conditions and are partly to blame for the many ill-defined and misnamed species presently used in many laboratories around the world. Comparison of various reports can therefore only be done with some caution. Dunaliella is related to Asteromonas (Peterfi and Manton, 1968) and has many characteristics in common with Chlamydomonas. However, Dunaliella can- not be simply regarded as a wall-less Chlamydomonas. Large differences are ob- served, e.g. in ultrastructure (Marano et al., 1985; Melkonian and Preisig, 1984). Habitat. The halophilic members of Dunaliella are mainly found in subtropical areas throughout the world, but also in more moderate regions (Borowitzka and Borowitzka, 1988). Due to their unique capability to cope with large differences in salinity, they can be found in various environments. Depending on the species, members of Dunaliella are able to survive in low salinities of < 1% NaCl to satu- rated solutions (> 35%). For comparison, the salinity of normal sea water is ap- proximately 3% NaCl. In salt lakes, such as the Great Salt Lake in Utah, U.S.A. and the salt lakes in Australia, in which the salinities are much higher, Dunaliella can be the predominant species and their presence can give the water a green or red colour (Borowitzka, 1981; Felix and Rushforth, 1979). Vegetative and sexual reproduction. Cell division in Dunaliella occurs by binary fission. The volume of the cell increases and a longitudinal division plane is formed. The duplication of the flagella can be completed before the cell division has finished, resulting in large cells with four flagella (Lerche, 1937; Teodoresco 1905, 1906; Penn, 1937). The total cell cycle can take place in 10 hours (this thesis). Using synchronized cultures, cell division occurs in the dark period every 24 h (Wegmann and Metzner, 1971; Zachleder et al., 1989). Sexual reproduction in Dunaliella has been described by Teodoresco (1905, 1906) and Lerche (1937). This process is induced by adverse conditions such as ni- trate depletion and resembles the sexual reproduction of Chlamydomonas (for re- view, see van den Ende, 1994). Two gametes fuse and a zygote is formed. In con- trast to vegetative cells, this zygote has a cell wall. After a maturation period, the zygote wall bursts and 2, 4, 8 or 16 daughter cells are released. Sexual reproduc- tion has rarely been observed in nature, and has not been reported to occur under laboratory conditions since the publications mentioned above. This lack of a sex- ual cycle, which impedes genetic research, has to some extent been circumvented - 10 - INTRODUCTION by using mutants (Brown et al., 1987; Chitlaru and Pick 1989; Hard and Gilmour 1991; Latorella et al., 1981; Shaish et al., 1991) and somatic fusion (Lee and Tan, 1988). A stable genetic system has not been attained. Vegetative survival bodies are described by Loeblich (1969). These aplanospores also contain a cell wall and are formed during adverse environmental conditions. 2. Halotolerance Dunaliella is able to withstand extremely low osmotic potentials in (hyper)saline environments by accumulating glycerol as osmoprotectant. The amount of glyc- erol present in the cytoplasm is a linear function of the osmotic potential of the environment (Avron, 1992). The production of glycerol at hyperosmotic shock mainly takes place via photosynthetic CO2 fixation or by starch degradation, whereas at hypoosmotic shock, for example by diluting the NaCl concentration in the surrounding medium, the cells increase their volume within 2-3 min and rapidly convert glycerol into osmotically inactive starch. An interesting aspect of this property is how the cell senses such changes in osmotic conditions and what the nature is of the transduction of the signal leading to the physiological response. It appears that the responses to dilution are accompanied by hydrolysis of phosphatidylinositol 4,5-bisphosphate (PIP2) within 2 min (Einspahr et al., 1988). The products of this reaction are inositol 1,4,5- trisphosphate (IP3) and diacylglycerol. It is probable that the activation of the responsible enzyme, phospholipase C, is mediated by a G-protein. Two candidate G-proteins of 34 and 42 kDa have been identified in Dunaliella through the use of antibodies raised against mammalian G-protein !-subunits (Thompson, 1994). Possibly the G-protein is activated via a stretch-activated protein present in the plasma membrane. IP3 is known to release Ca2+ from intracellular stores and presumably the resulting increased Ca2+ concentration in the cytoplasm induces the conversion of glycerol to starch. In line with this view is the observation that several Ca2+ activated protein kinases have been identified in Dunaliella (Yuasa and Muto, 1992). Diacylglycerol is expected to activate protein kinase C, but this enzyme has not been detected in Dunaliella. Cells subject to hyperosmotic shock react by increasing their content of phosphoinositol 4-phosphate and phosphoinositol 4,5-bisphosphate, suggesting an inhibition of phospholipase C or an increased polyphosphoinositol synthesis, or both. Also a plasma membrane ATP-ase is activated, resulting in a decreased ATP level and an increase of the inorganic phosphate level in the cytoplasm. This - 11 - CHAPTER 1 is thought to result in increased glycerol synthesis (Bental et al., 1990). It is notable that Dunaliella is one of the few plant systems in which several of the steps associated with PIP2-mediated signalling have been detected. It is possible that even more well-known second messenger systems are operative. For example, Cowan et al. (1992) have obtained evidence that abscisic acid is involved in hypertonic shock response, leading to increased carotenoid synthesis. We shall return to this in the next section. 3. Carotene production Historical. It was Dunal (1838) who observed that it was an alga which gave the salt water basins, used for sea salt production in southern France, their reddish colour. Teodoresco (1905) described the type species and named it after Dunal: Dunaliella salina. Later, a distinction was made between two species, D. salina and D. viridis (Teodoresco, 1906). This was based on the ability of the first species to attain a red colour under certain conditions.
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