Rhodotorula Glutinis—Potential Source of Lipids, Carotenoids, and Enzymes for Use in Industries
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Appl Microbiol Biotechnol DOI 10.1007/s00253-016-7611-8 MINI-REVIEW Rhodotorula glutinis—potential source of lipids, carotenoids, and enzymes for use in industries Anna M. Kot1 & Stanisław Błażejak1 & Agnieszka Kurcz1 & Iwona Gientka1 & Marek Kieliszek1 Received: 15 March 2016 /Revised: 29 April 2016 /Accepted: 2 May 2016 # The Author(s) 2016. This article is published with open access at Springerlink.com Abstract Rhodotorula glutinis is capable of synthesizing nu- times, a large number of studies have been published on the merous valuable compounds with a wide industrial usage. biotechnological uses of these yeasts, which suggest that they Biomass of this yeast constitutes sources of microbiological may constitute important group of microorganisms that might oils, and the whole pool of fatty acids is dominated by oleic, be of importance in industries in the future. Rhodotorula linoleic, and palmitic acid. Due to its composition, the lipids glutinis is considered to be the typical species of this genus. may be useful as a source for the production of the so-called These yeasts are capable of synthesizing numerous metabo- third-generation biodiesel. These yeasts are also capable of lites useful in industries, such as lipids, carotenoids, and en- synthesizing carotenoids such as β-carotene, torulene, and zymes. Their clear advantage is their capacity to grow and torularhodin. Due to their health-promoting characteristics, synthesize metabolites on substrates containing different in- carotenoids are commonly used in the cosmetic, pharmaceu- dustrial waste raw materials, which considerably elevates the tical, and food industries. They are also used as additives in economic profitability of biotechnological processes. This fodders for livestock, fish, and crustaceans. A significant char- study presents a literature review on the possibility to obtain acteristic of R. glutinis is its capability to produce numerous microbiological lipids, carotenoids, and enzymes from enzymes, in particular, phenylalanine ammonia lyase (PAL). R. glutinis biomass and their potential use in industries. This enzyme is used in the food industry in the production Moreover, the pathways of lipids and carotenoid biosynthesis of L-phenylalanine that constitutes the substrate for the and the influence of selected environmental factors on the synthesis of aspartame—a sweetener commonly used in efficiency of these processes are described. the food industry. Keywords Oleaginous yeast . β-Carotene . Torulene . History, taxonomy, morphology, and physiology of Torularhodin . Phenylalanine ammonia-lyase R. glutinis Over the years, the asexually reproducing, colored yeasts have Introduction been assigned to numerous genera, such as Torula, Mycotorula, Torulopsis, Cryptococcus,andevenSaccharomyces.Francis Until recently, the yeasts of the genus Rhodotorula were pri- Charles Harrison, a Canadian microbiologist, who worked on marily considered to be saprophytes that spoil food. In recent yeasts found in regional cheeses in the 1930s, was the first one to use the name Rhodotorula (Barnett 2004). The genus name originates from the word rhodos (red in Greek) and torula * Anna M. Kot (feminine diminutive form of the Neo-Latin torus—bulge) [email protected] (Krzyściak et al. 2007). Rhodotorula glutinis is considered to be a typical species of 1 Department of Biotechnology, Microbiology and Food Evaluation, this genus, and it was described by Georg Fresenius in 1850. Faculty of Food Sciences, Warsaw University of Life Sciences, The yeasts were isolated from the cream of sour milk and Nowoursynowska 159C, 02-776 Warsaw, Poland named Cryptococcus glutinis at that time (Barnett 2004). Appl Microbiol Biotechnol R. glutinis is included in the order Sporidiobolales, class and Nicaud 2012). In comparison to the production of vegeta- Microbotryomycetes, and phylum Basidiomycota in the ble and animal fats, this method is independent of climate, Fungi kingdom. Integrated Taxonomic Information System season, and geographical position of a country. Production cy- provides three synonyms of the Latin name of Rhodotorula cle is short, thanks to the rapid growth rate exhibited by the glutinis: R. rufula, R. glutinis var. rubescens,andR. gracilis microorganisms (Santos et al. 2013). Microbiological lipids (ITIS Standard 2016). The following varieties are distin- can be used as food additives, diet supplements, and substitu- guished within the species: Rhodotorula glutinis (Fresenius) tions for precious fats. Microbiological oils can also be used as var. glutinis, Rhodotorula glutinis var. dairenensis (yeast iso- substrates in the so-called third-generation biodiesel production lated in 1922 by Saito from air) (Fell and Statzell-Tallman (Lietal.2008; Papanikolaou and Aggelis 2011b; Papanikolaou 1998), and Rhodotorula glutinis var. salinaria (yeast isolated et al. 2001, 2003; Ratledge and Cohen 2008). in 1969 from salt) (Hirosawa and Takada 1969). The yeast Rhodotorula glutinis belongs to the group of The majority of the yeasts included in the species are oleaginous microorganisms (Table 1), which are defined as mesophilic, although some of them thrive under lower tem- those that are capable of producing and accumulating over peratures, and aerobic organisms. The cells are spherical, el- 20 % of lipids in dry cellular substance (Ratledge and Cohen lipsoidal, or elongated in shape. R. glutinis reproduce asexu- 2008). Fat is stored in the lipid bodies (Ham and Rhee 1998), ally by multilateral or polar budding; certain strains form re- whose structure is similar in all oleaginous yeasts. The core sidual pseudomycelium (Fell and Statzell-Tallman 1998). consists of backup hydrophobic compounds (such as triacyl- These yeasts are capable of using many compounds as glycerols, free fatty acids, and sterols), and it is surrounded by sources of carbon. They include glucose, galactose, sucrose, a layer of phospholipids bound to proteins (Fickers et al. maltose, trehalose, ethanol, glycerol, and hexadecane. A char- 2005). In these yeasts, the lipid bodies consist of neutral lipids acteristic feature of this genus is its lack of capacity to perform in the form of triglycerides, and the composition of phospho- sugar fermentation. The cells produce urease and Q-10 coen- lipids differs from this composition in other cellular organ- zyme. They can grow in the presence of 10 % NaCl, but they elles. This stems from the fact that they primarily consist of do not tolerate glucose concentration above 50 % (Fell and phosphatidylcholine (38.6 %) and phosphatidylserine (43 %) Statzell-Tallman 1998). (Ham and Rhee 1998). R. glutinis colonies that grow on permanent malt medium exhibit characteristic coloration that depends on the type of strain and growth conditions. They can be of creamy, yellow, Mechanism of lipid biosynthesis salmon, pink, orange, coral, and blood red in color. In liquid media, they grow in the form of orange ring or sediment (Fell In yeast cells, lipids may be accumulate via two pathways: de and Statzell-Tallman 1998; Hernández-Almanza et al. 2014). novo (from acetyl-CoA and malonyl-CoA molecules) and ex The colored pigmentation of the cells is due to the production novo (Beopoulos and Nicaud 2012). In the de novo method, of large amounts of carotenoids, which are responsible for saccharides or glycerol constitutes the substrates for lipids protecting the cells against the effect of singlet oxygen and production (Papanikolaou and Aggelis 2011a), whereas in excessive radiation of visible and UV light spectrum the ex novo biosynthesis, hydrophobic compounds serve as (Hernández-Almanza et al. 2014). the substrates (Beopoulos et al. 2009). Culture media primar- Rhodotorula yeasts occur in common in the environment. ily containing glucose, sucrose, glycerol, and sugar waste raw They are isolated from air, soil, grass, lakes, oceans, food (i.e., materials such as molasses and different hydrolysates are used milk, fruit juices), human skin, and feces (Wirth and Goldani as sources of carbon for the production of lipids by the yeast 2012). The majority of the representatives of the genus do not Rhodotorula glutinis (Table 1). exhibit pathogenic properties, although opportunistic patho- In the de novo synthesis, the overproduction of intracellular gens are found among them, which cause dermatophytoses, lipids occurs after the depletion of nitrogen compounds from and are referred to as rhodotorulosis. The most common etio- the culture environment, which is related to the activation of logical factors of these infections are the strains of the species AMP deaminase. This enzyme catalyzes the decomposition of + Rhodotorula mucilaginosa (Biswas et al. 2001). AMP to IMP and NH4 ions, which constitute the additional source of nitrogen. A decrease in the adenosine monophosphate level disturbs the course of the Krebs cycle Lipid biosynthesis by Rhodotorula glutinis because this compound activates isocitrate dehydrogenase that catalyzes the transformation of isocitrate to α-ketoglutarate. In recent years, there has been an increased interest in develop- Under such conditions, mitochondrion accumulates isocitrate ing new methods to obtain lipids from these yeasts. One such that remains in balance with citrate, thanks to the activity of method includes the production of microbiological lipids, re- aconitase. After attaining a critical concentration, citric acid is ferred to as SCO in the literature (single cell oil) (Beopoulos transported from mitochondrion to the cytoplasm, where it is Appl Microbiol Biotechnol