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University of Groningen Functional Carbohydrates from the Red Microalga Galdieria Sulphuraria Martínez García, Marta

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University of Groningen Functional Carbohydrates from the Red Microalga Galdieria Sulphuraria Martínez García, Marta University of Groningen Functional carbohydrates from the red microalga Galdieria sulphuraria Martínez García, Marta IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2017 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Martínez García, M. (2017). Functional carbohydrates from the red microalga Galdieria sulphuraria. University of Groningen. Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 24-09-2021 Chapter 1 General introduction 7 Chapter 1 1. Microalgal biotechnology On a planet suffering the environmental consequences of unsustainable economic growth, which has been relying on the exploitation of limited fossil resources, the urge to shift to a bio-based economy has become a top priority. In the search for new biomass resources, algae have emerged as a good alternative to terrestrial crops due to the high biomass productivity achieved without requiring arable land for growth, therefore eliminating the competition with food production (Dismukes et al., 2008; Clarens et al., 2010, Posten & Chen, 2016). Until recent years, algal biotechnology has been dominated by the cultivation of certain species of marine macroalgae to be used directly as food source or for the production of polysaccharides with gelling properties such as agar, carrageenan and alginate, widely used as hydrocolloids in a range of food, pharmaceutical and specialty products (Radmer, 1996). Microalgal biotechnology is a branch of algal biotechnology that has taken advantage of the faster growth rates and higher biomass productivity of unicellular algae compared to multicellular species (Rosenberg et al., 2008, Posten & Chen, 2016). Although in the last years the use of microalgae for biodiesel production has received much attention (Miao & Wu, 2006; Wijffels & Barbosa, 2010), microalgae can actually produce a vast range of high value products, including pigments, carotenoids, antioxidants, polysaccharides and polyunsaturated fatty acids (Pulz & Gross, 2004; Borowitzka, 2013). Most microalgae species are obligate phototrophs and their growth is necessarily linked to the availability of light to perform photosynthesis. The mass cultivation of these photosynthetic microalgae can be carried out in open- ponds, where cells can grow utilizing sunlight, or in closed photobioreactors with artificially supplied light (Lee et al., 2001). Usually, this type of microalgae cultivation is associated with low biomass yields and the market value of the product of interest needs to compensate for the high production costs (Borowitzka, 1992). Heterotrophic cultivation of microalgae, by which cells are grown in the dark using an organic compound as carbon and energy source, results in much higher biomass productivities and is thus more cost- effective (Perez-Garcia et al., 2011). However, the ability to grow heterotrophically is only restricted to certain microalgae, such as for example Hematococcus pluvialis, Aurantiocrytum limacinum and several Chlorella 8 Introduction species (Miao & Wu, 2006; Bumbak et al., 2011; Sakarika & Kornaros, 2016; Morales-Sánchez et al., 2016). Among the facultative heterotrophic microalgae, we find Galdieria sulphuraria, a red microalga that grows optimally at pH 2 utilizing a wide range of organic substrates (Gross & Schnarrenberger, 1995). Because of its acidophilic lifestyle - which minimizes considerably the risk of contamination - and its ability to grow heterotrophically, G. sulphuria shows desirable features for mass cultivation, which has until now only been explored for the production of pigments (Graveholt & Erikssen, 2007). Research and characterization of possible valuable compounds from G. sulphuraria will contribute to further exploit the biotechnological potential of this microalga. 2. The extremophilic red microalga Galdieria sulphuraria 2.1. Red algae Red algae (Rhodophyta) are a group of ancient photosynthetic eukaryotes which some authors claim it diverged even before the appearance of the common ancestor of plants and fungi (Stiller & Hall, 1997). However, this affirmation is not widely supported by other phylogenetical analysis, and the classification of red algae as a sister group sharing a common ancestor with plants, green algae and fungi is still the most generally accepted today (Moreira et al, 2000). Rhodophyta is a diverse group of organisms that contains both multicellular and unicellular species that can colonize a wide range of habitats, including marine and fresh waters, hot sulfur springs and volcanic environments. The taxonomic classification of red algae has been revised and updated several times, with more recent phylogenetic studies proposing a classification of red algae into two subphyla: Cyanidiophytina and Rhodophytina (Yoon et al., 2006; Yang et al., 2016). The subphylum Cyanidiophytina contains only one class, Cyanidiophyceae, and this class contains only one order named Cyanidiales. The subphylum Rhodophytina contains six classes: Floridiophyceae, Bangiophyceae, Rhodellophyceae, Compsopogonophyceae, Stylonematophyceae and Porphyridiophyceae. The class Floridiophyceae is the most diverse and contains the majority of the currently described red algae species (Guiry & Guiry, 2016), including economically relevant species such as those used for the production of the polysaccharides agar and carrageenan, two widely employed phycocolloids (Renn, 1997). 9 Chapter 1 A common characteristic of all red algae is the presence of chlorophyll a as the only major photosynthetic pigment and phycobiliproteins as accessory pigments to improve the efficiency of light harvesting. These phycobilliproteins are arranged in big macromolecular complexes named phycobilisomes, similar to those found in cyanobacteria, which are embedded in the membrane of the choloroplasts (Gantt, 1981). Although most of red algae owe their color to the orange-red pigment phycoerythrin, some species are blue-green because their major photsynthetic pigment is the blue phycocyanin (Cole & Sheath, 1990). 2.2. The extremophilic order Cyanidiales The order Cyanidiales groups the most ancient red algae that diverged from the other species more than 1200 million years ago (Yoon et al. 2006, Yang et al., 2016). This order consists of three genera: Cyanidium, Cyanidioschyzon and Galdieria. The first two genera were the first to be described and contain only one species each, Cyanidium caldarium (Hirose, 1958) and Cyanidioschyzon merolae (De Luca et al., 1978), respectively. In 1981, it was revealed that more than one species had been wrongly referred to as C. caldarium over the past years, since another very similar microalga co-existed in the same habitat. A new genus was created and the newly isolated species was given the name of Galdieria sulphuraria (Merola et al., 1981). Because of that confusion, some studies performed on G. sulphuraria prior to 1981 might have been wrongly attributed to C. caldarium. Later on, three more species isolated from acid thermal springs in Russia were included into the genus Galdieria on the basis of morphological features, and were named Galdieria maxima, Galdieria partita and Galdieria daedela (Sentsova, 1991). However, their status as new species has been challenged by some authors who claim they are just strains of G. sulphuraria (Cozzolino et al, 2000). All Cyanidiales are unicellular and display a blue-green color due to the presence of phycocyanin as their main accessory photosynthetic pigment. They are extremophiles, thriving in environments with pH values between 0-4 and temperatures up to 56 °C (Seckbach, 1999), a value close to the upper limit for eukaryotic life (Rothschild & Mancinelli, 2001). These type of environments are scattered around the world, and can be found in e.g. the hot sulfur springs of Yellowstone National Park (USA) or volcanic areas in, Iceland, Italy, Indonesia, New Zealand and Japan (Gross & Oesterhelt, 1999; Toplin et al., 2008), where 10 Introduction the Cyanidiales represent the majority of the eukaryotic biomass and the only photosynthetic organisms present. The Cyanidiales are also tolerant to high concentrations of salts (Gross et al., 2002; Pade et al., 2015) and metals (Yoshimura et al., 1999; Nagasaka et al., 2004), which are typical of these sites (Gross, 2000). Even though the three Cyanidiales genera diverged very early from each other - for example, the evolutionary distance between C. merolae and G. sulphuraria is the same as between the fruit fly and humans (Schönknecht et al., 2013) – their physiological and morphological features are very similar and have been conserved over the years, and no new species have been discovered and added to the few already described. This is likely due to the extreme conditions
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